Uso de bioestimulantes en el cultivo del garbanzo

^iDIndira López-Padrón^*✉:shari@inca.edu.cu

^iDLisbel Martínez-González

^iDGeydi Pérez-Domínguez

^iDYanelis Reyes-Guerrero

^iDMiriam Núñez-Vázquez

^iDJuan A. Cabrera-Rodríguez

Instituto Nacional de Ciencias Agrícolas (INCA), carretera San José-Tapaste, km 3½, Gaveta Postal 1, San José de las Lajas, Mayabeque, Cuba. CP 32 700.

^{^*}Autor para correspondencia: shari@inca.edu.cu

Resumen

El garbanzo (Cicer arietinum L.), es una de las leguminosas más importantes del mundo con una producción que ronda los 9 millones de toneladas. El cultivo es sensible a varios estreses abióticos como son: la salinidad, las temperaturas extremas y el exceso o deficiencia de humedad en el suelo; además, puede ser afectado por varias plagas y enfermedades. Los efectos adversos del uso indiscriminado de productos químicos en la agricultura, ha propiciado el uso de diversos bioestimulantes en el garbanzo como alternativa segura al empleo de los mismos, ya sea para el aporte de nutrientes a las plantas como para el control y manejo de plagas y enfermedades; así como para la inducción de tolerancia a estreses abióticos. El uso de bacterias promotoras del crecimiento vegetal (BPCV) como biofertilizantes, ha sido una de las prácticas más utilizadas en este cultivo, aunque también se han empleado los hongos micorrízicos arbusculares, la coinoculación de bacterias de diferentes géneros y de bacterias y hongos. Además, se ha informado el empleo de otros bioestimulantes como los productos a base de algas o quitosano, para incrementar el rendimiento y la calidad de los granos. El objetivo de esta revisión bibliográfica es dar una visión actualizada sobre el uso de bioestimulantes en el cultivo del garbanzo, haciendo énfasis en aquellos basados en microorganismos benéficos, extractos de algas y quitosano.

Palabras clave:

Cicer arietinum, rizobacterias, micorrizas, algas, quitosano

CONTENIDO

Introducción

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El garbanzo (Cicer arietinum L.), es considerado una de las legumbres más importantes del mundo por su alto valor nutritivo (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ), al ser rico en proteínas, carbohidratos, minerales (22. Bidyarani N, Prasanna R, Babu S, Hossain F, Saxena AK. Enhancement of plant growth and yields in Chickpea (Cicer arietinum L.) through novel cyanobacterial and biofilmed inoculants. Microbiological Research [Internet]. 2016 [cited 24/08/2021];188- 189:97-105. https://doi.org/10.1016/j.micres.2016.04.005 ), almidón y lípidos; sobre todo en los ácidos grasos insaturados oleico y linoleico y no poseer cantidades significativas de colesterol (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ).

Es un cultivo cuyo rendimiento varía, en gran medida, dependiendo del cultivar, las condiciones edafoclimáticas y de las atenciones culturales que reciba en el lugar donde se desarrolle (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ,33. Shagarodsky T, Chiang ML, López Y. Evaluación de cultivares de garbanzo (Cicer arietinum L.) en Cuba. Agronomía Mesoamericana [Internet]. 2001;12(1):95-8. Available from: https://www.redalyc.org/pdf/437/43712113.pdf ,44. Barrios MA, Estrada JASE, González MTR, Barrios PA. Rendimiento de garbanzo en función del tipo de suelo y niveles de nitrógeno. Revista Mexicana de Ciencias Agrícolas [Internet]. 2015;2:295-9. Available from: https://www.redalyc.org/pdf/2631/263141553035.pdf ). En dicho rendimiento también tiene gran influencia, el esquema de manejo que se siga para el control de plagas y enfermedades, las que pueden ocasionar cuantiosas pérdidas en el cultivo (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ).

La FAO (Organización de las Naciones Unidas para la Alimentación y la Agricultura), busca promover políticas y prácticas que apoyen la integración de los sectores agrícolas y productivos y que aseguren el manejo responsable y la disponibilidad de recursos naturales a largo plazo (55. Commission Regulation. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety [Internet]. OJ L, 32002R0178 CONSIL, EP; Feb 1, 2002. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32002R0178&qid=1629823328145 ,66. Colglazier W. Sustainable development agenda: 2030. Science [Internet]. 2015 [cited 24/08/2021];349(6252):1048-50. https://doi.org/10.1126/science.aad2333 ). Como se proyecta en la Agenda de Desarrollo Sostenible 2030; en la actualidad es evidente la necesidad de una Agricultura Sostenible (55. Commission Regulation. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety [Internet]. OJ L, 32002R0178 CONSIL, EP; Feb 1, 2002. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32002R0178&qid=1629823328145 ,66. Colglazier W. Sustainable development agenda: 2030. Science [Internet]. 2015 [cited 24/08/2021];349(6252):1048-50. https://doi.org/10.1126/science.aad2333 ).

El uso indiscriminado de productos químicos en la agricultura; ya sea fertilizantes o fungicidas, ha afectado severamente los agroecosistemas, contribuyendo a la contaminación del suelo, el agua, los alimentos y hasta de los agricultores (77. García-González JE. Situación actual y perspectivas de la agricultura orgánica y su relación con América Latina. Manejo Integrado de Plagas [Internet]. 2002;(64):116-24. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=oet.xis&method=post&formato=2&cantidad=1&expresion=mfn=024515,88. Shaikh SS, Sayyed RZ. Role of Plant Growth-Promoting Rhizobacteria and Their Formulation in Biocontrol of Plant Diseases. In: Arora NK, editor. Plant Microbes Symbiosis: Applied Facets [Internet]. New Delhi: Springer India; 2015 [cited 24/08/2021]. p. 337-51. https://doi.org/10.1007/978-81-322-2068-8_18 ). Además ha producido desequilibrios nutricionales en las plantas y ha afectado el equilibrio ecológico, impidiendo el desarrollo de bacterias del suelo (77. García-González JE. Situación actual y perspectivas de la agricultura orgánica y su relación con América Latina. Manejo Integrado de Plagas [Internet]. 2002;(64):116-24. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=oet.xis&method=post&formato=2&cantidad=1&expresion=mfn=024515,88. Shaikh SS, Sayyed RZ. Role of Plant Growth-Promoting Rhizobacteria and Their Formulation in Biocontrol of Plant Diseases. In: Arora NK, editor. Plant Microbes Symbiosis: Applied Facets [Internet]. New Delhi: Springer India; 2015 [cited 24/08/2021]. p. 337-51. https://doi.org/10.1007/978-81-322-2068-8_18 ). El desarrollo de plagas resistentes a los pesticidas e incluso al surgimiento de nuevas especies también ha sido observado (77. García-González JE. Situación actual y perspectivas de la agricultura orgánica y su relación con América Latina. Manejo Integrado de Plagas [Internet]. 2002;(64):116-24. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=oet.xis&method=post&formato=2&cantidad=1&expresion=mfn=024515,88. Shaikh SS, Sayyed RZ. Role of Plant Growth-Promoting Rhizobacteria and Their Formulation in Biocontrol of Plant Diseases. In: Arora NK, editor. Plant Microbes Symbiosis: Applied Facets [Internet]. New Delhi: Springer India; 2015 [cited 24/08/2021]. p. 337-51. https://doi.org/10.1007/978-81-322-2068-8_18 ). Todo esto ha propiciado el aumento del uso de bioestimulantes en la agricultura (77. García-González JE. Situación actual y perspectivas de la agricultura orgánica y su relación con América Latina. Manejo Integrado de Plagas [Internet]. 2002;(64):116-24. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=oet.xis&method=post&formato=2&cantidad=1&expresion=mfn=024515,99. Dias GA, Rocha RHC, Araújo JL, Lima JF, Guedes WA. Growth, Yield, And Postharvest Quality In Eggplant Produced Under Different Foliar Fertilizer (Spirulina platensis) Treatments. Semina: Ciências Agrárias [Internet]. 2016 [cited 24/08/2021];37(6):3893-3902. Available from: http://repositorio.unicamp.br/jspui/handle/REPOSIP/323726 ,1010. Doimeadiós Reyes Y, Sánchez Llanes A. Productividad y eficiencia en la economía cubana: una aproximación empírica. Economía y Desarrollo [Internet]. 2015 [cited 24/08/2021];153:90-107. Available from: http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S0252-85842015000100006&lng=es&nrm=iso&tlng=es ).

Un bioestimulante es cualquier sustancia o microorganismo aplicado a las plantas con el propósito de estimular la eficiencia en la nutrición, la tolerancia a estreses abióticos y la calidad del cultivo, con independencia de su contenido de nutrientes (1111. du Jardin P. Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae [Internet]. 2015 [cited 24/08/2021];196:3-14. https://doi.org/10.1016/j.scienta.2015.09.021 ).

De acuerdo con la definición anterior, dentro de las categorías de bioestimulantes se encuentran los extractos de algas marinas y de plantas, hidrolizados de proteínas y otros compuestos que contienen N, las sustancias húmicas, el quitosano y otros biopolímeros, y bacterias y hongos beneficiosos (1111. du Jardin P. Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae [Internet]. 2015 [cited 24/08/2021];196:3-14. https://doi.org/10.1016/j.scienta.2015.09.021 ).

El objetivo central de esta revisión bibliográfica es brindar una visión general y actualizada sobre el uso de bioestimulantes en el cultivo del garbanzo, fundamentalmente aquellos basados en microorganismos benéficos, extractos de algas y quitosano.

Generalidades del cultivo del garbanzo

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En el mundo se cultivan alrededor de 12 millones de hectáreas de garbanzos, con una producción que ronda los 9 millones de toneladas. Los países más productores son India, Turquía, Pakistán, Irán, México, Australia y Canadá, mientras que los principales exportadores son Turquía y Australia (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ).

Su rendimiento varía, en gran medida, dependiendo del cultivar, las condiciones edafoclimáticas y el manejo fitotécnico en el lugar donde se desarrolle (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ,33. Shagarodsky T, Chiang ML, López Y. Evaluación de cultivares de garbanzo (Cicer arietinum L.) en Cuba. Agronomía Mesoamericana [Internet]. 2001;12(1):95-8. Available from: https://www.redalyc.org/pdf/437/43712113.pdf ,44. Barrios MA, Estrada JASE, González MTR, Barrios PA. Rendimiento de garbanzo en función del tipo de suelo y niveles de nitrógeno. Revista Mexicana de Ciencias Agrícolas [Internet]. 2015;2:295-9. Available from: https://www.redalyc.org/pdf/2631/263141553035.pdf ). Por ejemplo; en un estudio realizado en Montecillo, México, en dos suelos de textura diferente, se observó que los niveles de urea afectaron la biomasa, el índice de cosecha, el rendimiento y sus componentes (44. Barrios MA, Estrada JASE, González MTR, Barrios PA. Rendimiento de garbanzo en función del tipo de suelo y niveles de nitrógeno. Revista Mexicana de Ciencias Agrícolas [Internet]. 2015;2:295-9. Available from: https://www.redalyc.org/pdf/2631/263141553035.pdf ). Por otra parte, diversas variedades cubanas cultivadas en un suelo Ferralítico Rojo, entre los años 1998-1999, mostraron rendimientos que oscilaron desde 0,48 t ha^-1 hasta 2,36 t ha^-1 (33. Shagarodsky T, Chiang ML, López Y. Evaluación de cultivares de garbanzo (Cicer arietinum L.) en Cuba. Agronomía Mesoamericana [Internet]. 2001;12(1):95-8. Available from: https://www.redalyc.org/pdf/437/43712113.pdf ).

Se puede aplicar Rhizobium del garbanzo a la semilla, normalmente la simbiosis con bacterias fijadoras de Nitrógeno es suficiente para proveer cantidades necesarias de N, no obstante, se puede aconsejar la distribución de pequeñas cantidades de N (1212. Miramontes JAÁ, Zaldo GP, Heredia DM, Santoyo FJR, Espericueta MÁC, Murrieta PO. Respuesta de algunos componentes del rendimiento del cultivo de garbanzo (Cicer arietinum L.) a la inoculación de Mesorhizobium ciceri, Trichoderma harzianum y Bacillus subtilis en la región agrícola de La Costa de Hermosillo. BIOtecnia. 2015;17(3):3-8.). También, se plantea que este cultivo demanda altos niveles de azufre (1313. Yadav SL, Verma A, Nepalia V. Effect of phosphorus, sulphur and seaweed sap on growth, yield and nutrient uptake of chickpea ( Cicer arietinum L.). Research on Crops [Internet]. 2016 [cited 24/08/2021];17(3):496. https://doi.org/10.5958/2348-7542.2016.00082.6 ), aunque todavía no existen estudios exhaustivos sobre este tema (1414. Vargas-Blandino D, Cárdenas-Travieso RM. Cultivo del garbanzo, una posible solución frente al cambio climático. Cultivos Tropicales [Internet]. 2021;42(1). Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362021000100009&script=sci_arttext&tlng=pt ,1515. Del Moral, J.; Mejías A. y López, M. El cultivo del garbanzo. Diseño para una agricultura sostenible. Hojas divulgadoras No. 12/94HD. [Internet]. Ministerio de agricultura Pesca y Alimentación: España. 1996;23. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=sibur.xis&method=post&formato=2&cantidad=1&expresion=mfn=001883 ).

Las principales plagas que afectan al garbanzo, a nivel mundial, en las áreas de cultivo son: Liriomyza cicerina (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ), Heliothis armigera (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ), Bruchus sp. (1616. Gaur PM, Tripathi S, Gowda CL, Ranga Rao GV, Sharma HC, Pande S, et al. Chickpea seed production manual. International Crops Research Institute for the Semi- Arid Tropics. 2010;28.), Plusia orichalcea (1616. Gaur PM, Tripathi S, Gowda CL, Ranga Rao GV, Sharma HC, Pande S, et al. Chickpea seed production manual. International Crops Research Institute for the Semi- Arid Tropics. 2010;28.) y Helicover pagelotopoeon (1717. Balcazar G, Garelli I, Gerez G, Molina J, Sánchez N. Incidencia de Helicover pagelotopoeon Dyar. sobre el cultivo de garbanzo (Cicer arietinum L.) en el NE de Córdoba. [Internet]. Métodos cuantitativos para la investigación agropecuaria. 2017. [cited 24/08/2021]. Available from: http://hdl.handle.net/11086/6589 ), estando las dos primeras entre las principales plagas asociadas a este cultivo en Cuba (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ).

En el caso de las enfermedades, las principales son las conocidas como la rabia del garbanzo, causada por Ascochyta rabiei (1818. Herrera EF, Rentería MEM, Salazar SFM, Peña NJ, Bustos IIR. Bacteria of the chickpea rhizosphere with antagonistic capacity to phytopathogenous fungi and plant growth promotion. Tropical and Subtropical Agroecosystems [Internet]. 2018 [cited 24/08/2021];21(3). Available from: https://www.revista.ccba.uady.mx/ojs/index.php/TSA/article/view/2548 ,1919. de Lisi V, Reznikov S, Henriquez DD, Aguaysol NC, Acosta ME, Gonzalez V, et al. Situación sanitaria del cultivo de garbanzo en la provincia de Tucumán y detección de rabia (Ascochyta rabiei) en la provincia de Catamarca. 2013 [cited 24/08/2021]; Available from: https://ri.conicet.gov.ar/handle/11336/7321 ) y la fusariosis (causada mayormente por el hongo Fusarium oxysporum f. sp. ciceris), esta última, a nivel mundial, es uno de los principales factores limitantes del rendimiento del cultivo (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ,2020. Fierros Leyva GA, Acosta Gallegos JA, Ortega Murrieta PF, Padilla Valenzuela I, Álvarez Bravo A, Ramírez Soto M, et al. Distribución de hongos asociados a pudriciones de raíz del garbanzo. Revista mexicana de ciencias agrícolas [Internet]. 2019 [cited 24/08/2021];10(1):131-42. https://doi.org/10.29312/remexca.v10i1.1730 ). También, se pueden encontrar otras como las pudriciones de las raíces (1919. de Lisi V, Reznikov S, Henriquez DD, Aguaysol NC, Acosta ME, Gonzalez V, et al. Situación sanitaria del cultivo de garbanzo en la provincia de Tucumán y detección de rabia (Ascochyta rabiei) en la provincia de Catamarca. 2013 [cited 24/08/2021]; Available from: https://ri.conicet.gov.ar/handle/11336/7321 ,2020. Fierros Leyva GA, Acosta Gallegos JA, Ortega Murrieta PF, Padilla Valenzuela I, Álvarez Bravo A, Ramírez Soto M, et al. Distribución de hongos asociados a pudriciones de raíz del garbanzo. Revista mexicana de ciencias agrícolas [Internet]. 2019 [cited 24/08/2021];10(1):131-42. https://doi.org/10.29312/remexca.v10i1.1730 ) y la caída de almácigos o “damping off”, la cual tiene como principales agentes causales a Rhizoctonia spp. y Botritis (2121. Barbuy MV, Rodriguez AV, Cordes G. Caída de almagicos “Damping Off” en garbanzo. 2019 [cited 24/08/2021]; Available from: http://repositorio.inta.gob.ar:80/handle/20.500.12123/6413 ).

En cuanto a los estreses abióticos, el garbanzo es un cultivo sensible al estrés salino (11. Cabeza RC, Escobar IH, Zayas IU, Robaina FR, Gil MED, Dubergel EF, et al. El cultivo de algunas legumbres para la producción local de alimentos y la mitigación del cambio climático PARTE I. El cultivo del fríjol carita o caupí (Vigna unguiculata Lin). Anuario Ciencia en la UNAH [Internet]. 2018 [cited 24/08/2021];16(1). Available from: https://revistas.unah.edu.cu/index.php/ACUNAH/article/view/994 ,2222. Mantri NL, Ford R, Coram TE, Pang ECK. Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environmental and Experimental Botany [Internet]. 2010 [cited 24/08/2021];69(3):286-92. https://doi.org/10.1016/j.envexpbot.2010.05.003 -2424. Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding [Internet]. 2014 [cited 24/08/2021];133(2):163-78. https://doi.org/10.1111/pbr.12150 ), a la sequía (2222. Mantri NL, Ford R, Coram TE, Pang ECK. Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environmental and Experimental Botany [Internet]. 2010 [cited 24/08/2021];69(3):286-92. https://doi.org/10.1016/j.envexpbot.2010.05.003 ,2424. Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding [Internet]. 2014 [cited 24/08/2021];133(2):163-78. https://doi.org/10.1111/pbr.12150 ,2525. Kaloki P, Devasirvatham V, Tan DK. Chickpea abiotic stresses: combating drought, heat and cold. Abiotic and Biotic Stress in Plants [Internet]. 2019; Available from: https://www.intechopen.com/chapters/65127 ), al exceso de humedad (2424. Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding [Internet]. 2014 [cited 24/08/2021];133(2):163-78. https://doi.org/10.1111/pbr.12150 ) y a las bajas (2222. Mantri NL, Ford R, Coram TE, Pang ECK. Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environmental and Experimental Botany [Internet]. 2010 [cited 24/08/2021];69(3):286-92. https://doi.org/10.1016/j.envexpbot.2010.05.003 ,2424. Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding [Internet]. 2014 [cited 24/08/2021];133(2):163-78. https://doi.org/10.1111/pbr.12150 -2626. Nayyar H, Bains TS, Kumar S. Chilling stressed chickpea seedlings: effect of cold acclimation, calcium and abscisic acid on cryoprotective solutes and oxidative damage. Environmental and Experimental Botany [Internet]. 2005 [cited 24/08/2021];54(3):275-85. https://doi.org/10.1016/j.envexpbot.2004.09.007 ) y altas temperaturas (2424. Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breeding [Internet]. 2014 [cited 24/08/2021];133(2):163-78. https://doi.org/10.1111/pbr.12150 ,2525. Kaloki P, Devasirvatham V, Tan DK. Chickpea abiotic stresses: combating drought, heat and cold. Abiotic and Biotic Stress in Plants [Internet]. 2019; Available from: https://www.intechopen.com/chapters/65127 ). El uso de diversos bioestimulantes en la agricultura como alternativa segura al empleo de productos químicos se ha venido diversificando, ya sea para el aporte de nutrientes a las plantas, el control y manejo de plagas y enfermedades o para la inducción de tolerancia a estreses abióticos (77. García-González JE. Situación actual y perspectivas de la agricultura orgánica y su relación con América Latina. Manejo Integrado de Plagas [Internet]. 2002;(64):116-24. Available from: http://www.sidalc.net/cgi-bin/wxis.exe/?IsisScript=oet.xis&method=post&formato=2&cantidad=1&expresion=mfn=024515,99. Dias GA, Rocha RHC, Araújo JL, Lima JF, Guedes WA. Growth, Yield, And Postharvest Quality In Eggplant Produced Under Different Foliar Fertilizer (Spirulina platensis) Treatments. Semina: Ciências Agrárias [Internet]. 2016 [cited 24/08/2021];37(6):3893-3902. Available from: http://repositorio.unicamp.br/jspui/handle/REPOSIP/323726 ,1111. du Jardin P. Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae [Internet]. 2015 [cited 24/08/2021];196:3-14. https://doi.org/10.1016/j.scienta.2015.09.021 ). En el cultivo del garbanzo también se ha ido incrementando el uso de algunos de estos productos con diferentes propósitos.

Bioestimulantes más utilizados en el cultivo del garbanzo

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Entre los bioestimulantes más utilizados en el cultivo del garbanzo se encuentran los microorganismos benéficos, los extractos de algas y en los últimos años, las nanopartículas de quitosano, tanto solas como cargadas con algunos metales u otras sustancias. También, se han utilizado las sustancias húmicas y el Fitomas-E, entre otros.

Microorganismos benéficos

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Diversos trabajos han demostrado la influencia de los microorganismos benéficos en la nodulación, el crecimiento y el rendimiento (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf -3232. Kumari N, Mondal S, Mahapatra P, Meetei TT, Devi YB. Effect of Biofertilizer and Micronutrients on Yield of Chickpea. International Journal of Current Microbiology and Applied Sciences [Internet]. 2019;8(01):2389-97. Available from: https://www.ijcmas.com/8-1-2019/Nirmala%20Kumari,%20et%20al.pdf ), en el contenido de proteínas de los granos (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,2828. Saini R, Dudeja SS, Giri R, Kumar V. Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. Journal of Basic Microbiology [Internet]. 2015 [cited 24/08/2021];55(1):74-81. https://doi.org/10.1002/jobm.201300173 ,3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ) y en la biofortificación (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ). Además, ellos estimulan la absorción de N, P, K, la actividad de las enzimas antioxidantes SOD y POD y el aumento de las concentraciones de ácidos orgánicos, con lo que reducen el pH de la rizosfera (3434. Israr D, Mustafa G, Khan KS, Shahzad M, Ahmad N, Masood S. Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum L.) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiology and Biochemistry [Internet]. 2016 [cited 24/08/2021];108:304-12. https://doi.org/10.1016/j.plaphy.2016.07.023 ). Estos efectos se asocian a la capacidad de estos microorganismos de producir sideróforos y HCN (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ), solubilizar minerales como el fósforo (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3636. Ansari MF, Tipre DR, Dave SR. Efficiency evaluation of commercial liquid biofertilizers for growth of Cicer aeritinum (chickpea) in pot and field study. Biocatalysis and Agricultural Biotechnology [Internet]. 2015 [cited 24/08/2021];4(1):17-24. https://doi.org/10.1016/j.bcab.2014.09.010 ), aumentar la exudación de las raíces (3434. Israr D, Mustafa G, Khan KS, Shahzad M, Ahmad N, Masood S. Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum L.) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiology and Biochemistry [Internet]. 2016 [cited 24/08/2021];108:304-12. https://doi.org/10.1016/j.plaphy.2016.07.023 ,3737. Akrami M, Khiavi HK, Shikhlinski H, Khoshvaghtei H. Biocontrolling two pathogens of chickpea Fusarium solani and Fusarium oxysporum by different combinations of Trichoderma harzianum, Trichoderma asperellum and Trichoderma virens under field condition. International Journal of Agricultural Science Research [Internet]. 2012;1(3):41-5. Available from: https://www.internationalscholarsjournals.com/articles/bio-controlling-two-pathogens-of-chickpea-fusarium-solani-and-fusarium-oxysporum-by-differentcombinations-of- trichoderma.pdf ), quelatar el hierro (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ), fijar nitrógeno atmosférico (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ,3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ), sintetizar fitohormonas (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ,4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ) e inhibir la infección por fitopatógenos (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,3737. Akrami M, Khiavi HK, Shikhlinski H, Khoshvaghtei H. Biocontrolling two pathogens of chickpea Fusarium solani and Fusarium oxysporum by different combinations of Trichoderma harzianum, Trichoderma asperellum and Trichoderma virens under field condition. International Journal of Agricultural Science Research [Internet]. 2012;1(3):41-5. Available from: https://www.internationalscholarsjournals.com/articles/bio-controlling-two-pathogens-of-chickpea-fusarium-solani-and-fusarium-oxysporum-by-differentcombinations-of- trichoderma.pdf ,4141. Echevarría A, Triana A, Rivero D, Rodríguez A, Martínez B. Generalidades del cultivo de garbanzo y alternativa biológica para el control de la Marchitez. Cultivos Tropicales [Internet]. 2019 [cited 24/08/2021];40(4). Available from: http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S0258-59362019000400010&lng=es&nrm=iso&tlng=es ,4242. Albuquerque da Silva Campos M. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection [Internet]. 2020 [cited 24/08/2021];135:105203. https://doi.org/10.1016/j.cropro.2020.105203 ).

Entre estos microorganismos, el uso de bacterias que promueven el crecimiento vegetal (BPCV), se ha convertido en una de las opciones más atractivas para mejorar la sostenibilidad de los sistemas agrícolas en muchas partes del mundo, debido a su respeto por el medio ambiente, el bajo costo de producción y el uso reducido de recursos no renovables (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ); encontrándose como una de las prácticas más utilizadas en el cultivo del garbanzo (4343. Dibut B, Shagarodsky T, Martínez R, Ortega M, Ríos Y, Fey L. Biofertilización del garbanzo (Cicer arietinum L.) con Mesorhizobium cicerii cultivado sobre suelo Ferralítico Rojo. Cultivos Tropicales [Internet]. 2005;26(1):5-9. Available from: https://www.redalyc.org/pdf/1932/193215916001.pdf ).

Dentro de estas bacterias, las fijadoras de nitrógeno del género Rhizobium son las más utilizadas en este cultivo (3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ,4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ,4343. Dibut B, Shagarodsky T, Martínez R, Ortega M, Ríos Y, Fey L. Biofertilización del garbanzo (Cicer arietinum L.) con Mesorhizobium cicerii cultivado sobre suelo Ferralítico Rojo. Cultivos Tropicales [Internet]. 2005;26(1):5-9. Available from: https://www.redalyc.org/pdf/1932/193215916001.pdf -4747. Solaiman ARM, Rabbani MG, Hossain D, Hossain GMA, Alam MS. Influence of phosphorus and inoculation with Rhizobium and AM fungi on growth and dry matter yield of chickpea. Bangladesh Journal of Scientific Research [Internet]. 2012;25(1):23-32. Available from: https://www.researchgate.net/publication/325145221_Influence_of_phosphorus_and_inoculation_with_Rhizobium_and_AM_fungi_on_growth_and_dry_matter_yield_of_chickpea ). La aplicación de bacterias de este género a las semillas de garbanzo, normalmente ha sido suficiente para proveer cantidades necesarias de N a las plantas; no obstante, se aconseja el suministro de pequeñas cantidades de este mineral (4444. Cota AG, Yañez GA, Esquer EJ, Anduaga R, Barrón JM. Efecto de la variedad y la fertilización en indicadores de calidad proteica in-vitro de dos variedades y una línea de garbanzo (Cicer arietinum). Revista chilena de nutrición [Internet]. 2010;37(2):193-200. Available from: https://scielo.conicyt.cl/scielo.php?pid=S0717-75182010000200008&script=sci_arttext&tlng=n ).

En estudio previo se reportó que con la aplicación de dos cepas cubanas de Mesorhizobium sp., a partir de una suspensión en agua a razón de 1:10 (v:v), se favoreció, tanto el crecimiento (altura, diámetro, masa total de la planta y masa seca de los nódulos), como el rendimiento (número y masa de vainas y número y masa de granos por planta) (3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ). Resultados similares se obtuvieron en España, con dos cepas aisladas del género Mesorhizobium (FCAP 26 y FCAP 04), que fueron capaces de aumentar el número de nódulos y favorecer el desarrollo de las plantas en condiciones de invernadero y de campo, así como de incrementar la producción de granos (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ).

En Montecillo, Estado de México, la inoculación de las semillas de garbanzo con Rhizobium etlí, estimuló el índice de área foliar, el índice de verdor y el rendimiento de granos (4848. Barrios MMA, Estrada JASE, González MMTR, Barrios PA. Rendimientode garbanzo verde en función de la densidad de población, biofertilización y fertilización foliar. Academia Journals. 2017;6(2):129. Available from: https://www.researchgate.net/profile/Patricio-Apaez-Barrios/publication/322939694_RENDIMIENTO_DE_GARBANZO_VERDE_EN_FUNCION_DE_LA_DENSIDAD_DE_POBLACION_BIOFERTILIZACION_Y_FERTILIZACION_FOLIAR/links/5a78b1c2a6fdcc4ffe90b1ed/RENDIMIENTO-DE-GARBANZO-VERDE-EN-FUNCION-DE_LA_DENSIDAD_DE_POBLACION_BIOFERTILIZACION_Y_FERTILIZACION_FOLIAR.pdf ).

Además de los efectos anteriores, se ha demostrado que las cepas de Rhizobium producen compuestos volátiles que inhiben el crecimiento de algunos patógenos del suelo como R. solani (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ).

Otras bacterias también han mostrado sus efectos positivos en el cultivo del garbanzo. De esta forma, se comprobó que el uso de bacterias de las especies Azotobacter vinelandii y Burkholderia cepacia, en un suelo laterítico sódico de textura arcillosa de México, degradado y compactado, con un contenido de materia orgánica de 1,5 % y N orgánico 39 kg ha^-1 y con un 50 % de fondo nitrogenado, estimuló el crecimiento y el desarrollo de las plantas (4949. Sánchez-Yáñez JM, Villegas-Moreno J, Vela-Muzquiz GR, Marquez-Benavides L. Respuesta del garbanzo (Cicer arietinum L.) a la inoculación con Azotobacter vineladii y Burkholderia cepacia a dosis reducida de fertilizante nitrogenado. Scientia Agropecuaria [Internet]. 2014 [cited 24/08/2021];5(3):115-20. https://doi.org/10.17268/sci.agropecu.2014.03.01 ). En la India, biofertilizantes líquidos comerciales que contienen cepas de Azotobacter o solubilizadores de fosfato, mostraron efectos beneficiosos en la germinación y la longitud promedio del brote en entornos controlados y en el rendimiento en condiciones controladas y de campo (3636. Ansari MF, Tipre DR, Dave SR. Efficiency evaluation of commercial liquid biofertilizers for growth of Cicer aeritinum (chickpea) in pot and field study. Biocatalysis and Agricultural Biotechnology [Internet]. 2015 [cited 24/08/2021];4(1):17-24. https://doi.org/10.1016/j.bcab.2014.09.010 ).

En estudios realizados para el control del Fusarium oxysporum en el garbanzo, se comprobó que aislados de Trichoderma viride y Trichoderma harzianum, además de disminuir la incidencia de la marchitez por Fusarium (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ), mejoraron la germinación de las semillas (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ,5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ), estimularon indicadores del crecimiento de las plantas como la longitud de las raíces y los brotes (5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ) y la masa seca (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ), así como el rendimiento (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ,5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ). Por otra parte, en Argentina, al evaluar la actividad biocontroladora de Trichoderma atroviride frente a patógenos del suelo, se comprobó una menor incidencia de enfermedades durante el ciclo de cultivo, donde se observa un mayor poder biocontrolador cuando se usa en la semilla junto a un biopolímero, aunque también se observaron estos resultados al ser utilizado sólo en la semilla y aplicado al suelo (5252. Caballero WA, Senés PJ, Toumanián AG. Evaluación de la capacidad biocontroladora de Trichoderma atroviride en el cultivo de garbanzo (Cicer arietinum L.) [Internet]. 2016. Available from: https://rdu.unc.edu.ar/handle/11086/4847 ).

Las bacterias del género Pseudomonas también son muy utilizadas para la estimulación del crecimiento y el rendimiento en el garbanzo y se ha demostrado su efectividad para disminuir el uso de fertilizante químico (5353. Joshi D, Chandra R, Suyal DC, Kumar S, Goel R. Impacts of Bioinoculants Pseudomonas jesenii MP1 and Rhodococcus qingshengii S10107 on Chickpea (Cicer arietinum L.) Yield and Soil Nitrogen Status. Pedosphere [Internet]. 2019 [cited 24/08/2021];29(3):388-99. https://doi.org/10.1016/S1002-0160(19)60807-6 ), además de reducir en pruebas in vitro el crecimiento de Rhizoctonia bataticola y Sclerotinias clerotiorumover y aplicadas a las semillas, reducen en pruebas de campo la incidencia de la enfermedad de pudrición de la raíz seca y pudrición del tallo causadas por estos hongos (5454. Patel DB, Singh HB, Shroff S, Sahu J. Antagonistic efficiency of Pseudomonas strains against soil borne disease of chickpea crop under in vitro and in vivo. Elixir Agriculture [Internet]. 2011;30:1774-7. Available from: https://www.elixirpublishers.com/articles/1351083604_30%20(2011)%201774- 1777.pdf). También se demostró que Pseudomonas aeruginosa, suprimió la marchitez y la pudrición de la raíz causadas por Fusarium oxysporum f. sp. ciceris y Rhizoctonia solani, respectivamente (4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ). La especie Pseudomonas fluorescens influyó sobre el marchitamiento vascular del garbanzo causado por Fusarium oxysporum f. sp. ciceris (5555. Ramezani H. Efficacy of some fungal and bacterial bioagents against Fusarium oxysporum f. sp. ciceris on chickpea. Plant Protection Journal. 2009;1(1):108-113) y especies del género Pseudomonas tolerantes a la sal, han incrementado la sanidad del garbanzo sometido a estrés por salinización, observándose que Pseudomonas putida RA, moduló la expresión de genes sensibles al estrés por sal (5656. Jatan R, Chauhan PS, Lata C. Pseudomonas putida modulates the expression of miRNAs and their target genes in response to drought and salt stresses in chickpea (Cicer arietinum L.). Genomics [Internet]. 2019 [cited 24/08/2021];111(4):509-19. https://doi.org/10.1016/j.ygeno.2018.01.007 ).

En otro estudio, dos cepas bacterianas solubilizadoras de P-Zn (Bacillus sp. cepa AZ17 y Pseudomonas sp. cepa AZ5), incrementaron el rendimiento de granos, el número de nódulos, la masa seca de los nódulos y la absorción de Zn y P en dos tipos de garbanzos cultivados en suelo fertilizado y no fertilizado, obteniéndose mejores resultados con la cepa de Pseudomonas sp. (3131. Zaheer A, Malik A, Sher A, Mansoor Qaisrani M, Mehmood A, Ullah Khan S, et al. Isolation, characterization, and effect of phosphate-zinc-solubilizing bacterial strains on chickpea (Cicer arietinum L.) growth. Saudi Journal of Biological Sciences [Internet]. 2019 [cited 24/08/2021];26(5):1061-7. https://doi.org/10.1016/j.sjbs.2019.04.004 ). También, se ha informado que las cepas de Pseudomonas putida NBRIRA y Bacillus amyloliquefaciens NBRISN13, tanto solas como en consorcio, fueron capaces de mejorar el estrés provocado por la sequía en cultivares sensibles y tolerantes de garbanzo; obteniéndose una mejor respuesta cuando se emplearon las cepas en consorcio (5757. Kumar M, Mishra S, Dixit V, Kumar M, Agarwal L, Chauhan PS, et al. Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signaling & Behavior [Internet]. 2016 [cited 24/08/2021];11(1):e1071004. https://doi.org/10.1080/15592324.2015.1071004 ).

La inoculación con dos aislados del género Bacillus, de la rizosfera de plantas de garbanzo, promovió el crecimiento de las plantas en condiciones de invernadero y presentaron un fuerte antagonismo in vitro ante F. oxysporum, F. solani y R. solani, además de la producción de sideróforos en medio CAS, solubilización de fósforo inorgánico y producción de ácido giberélico (1818. Herrera EF, Rentería MEM, Salazar SFM, Peña NJ, Bustos IIR. Bacteria of the chickpea rhizosphere with antagonistic capacity to phytopathogenous fungi and plant growth promotion. Tropical and Subtropical Agroecosystems [Internet]. 2018 [cited 24/08/2021];21(3). Available from: https://www.revista.ccba.uady.mx/ojs/index.php/TSA/article/view/2548 ). Se ha comprobado que Bacillus subtilis, influyó sobre el marchitamiento vascular del garbanzo causado por Fusarium oxysporum f. sp. ciceris (5555. Ramezani H. Efficacy of some fungal and bacterial bioagents against Fusarium oxysporum f. sp. ciceris on chickpea. Plant Protection Journal. 2009;1(1):108-113).

Otros resultados han mostrado que, aislados de Serratia marcescens aumentaron el rendimiento de granos del cultivo en suelos fértiles de áreas con irrigación y suelos deficientes de nutrientes en áreas de secano (5858. Zaheer A, Mirza BS, Mclean JE, Yasmin S, Shah TM, Malik KA, et al. Association of plant growth-promoting Serratia spp. with the root nodules of chickpea. Research in Microbiology [Internet]. 2016 [cited 24/08/2021];167(6):510-20. https://doi.org/10.1016/j.resmic.2016.04.001 ) y cepas de Streptomyces sp. exhibieron mayor número y masa de nódulos, así como mayor masa de raíces y de brotes a los 30 días después de la siembra (DAS) e incrementó el número y la masa de vainas, el área foliar, las masas de hojas y tallos a los 60 DAS y por consiguiente, en la cosecha, el rendimiento en granos fue superior (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ).

Así mismo, la inoculación con una cepa de Azospirillum lipoferum (FK1), mejoró la tolerancia a la salinidad de plantas de garbanzo, expresado mediante la estimulación significativa de la absorción de nutrientes, la biomasa, la síntesis de pigmentos fotosintéticos, el intercambio gaseoso, el contenido de fenoles, flavonoides y los niveles de antioxidantes enzimáticos y no enzimáticos. Además, las plantas inoculadas revelaron porcentajes más bajos de eflujo de electrolitos, de H2O2 y MDA y exhibieron altos niveles de expresión de los genes relacionados con la tolerancia a la sal (5959. El-Esawi MA, Al-Ghamdi AA, Ali HM, Alayafi AA. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environmental and Experimental Botany [Internet]. 2019 [cited 24/08/2021];159:55-65. https://doi.org/10.1016/j.envexpbot.2018.12.001 ).

Por otra parte, una cepa de Aneurinibacillus migulanus (FSZ 28) aislada de nódulos de Cicer arietinum L. cultivados en un suelo de la localidad de Fuentesaúco en Zamora (España), presentó la capacidad de inhibir el crecimiento de diferentes especies de Fusarium (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ). Más recientemente, se aisló de la rizosfera de las plantas de garbanzo una cepa de rizobacteria promotora del crecimiento vegetal identificada como Cedecea davisae RS3, la cual mejoró el comportamiento del cultivo bajo condiciones de déficit de nitrógeno (6060. Mazumdar D, Saha SP, Ghosh S. Isolation, screening and application of a potent PGPR for enhancing growth of Chickpea as affected by nitrogen level. International Journal of Vegetable Science [Internet]. 2020 [cited 24/08/2021];26(4):333-50. https://doi.org/10.1080/19315260.2019.163240 ).

Resultados favorables se han encontrado, también, con la coinoculación de BPCV. De esta forma, en ensayos de invernadero, se encontró que la coinoculación con Mesorhizobium sp. FCAP 26 y Bacillus halotolerans FSZ 47, estimuló el crecimiento y desarrollo de las plantas y la producción de semillas. Además, al realizar un ciclo de rotación con trigo se aumentó el contenido de carbono y nitrógeno en el suelo (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ).

Otros resultados mostraron que la coinoculación con Bacillus lentus, Pseudomonas putida y Trichoderma harzianum, produjo el mayor rendimiento en granos, además, propició un mayor contenido de N, P2O5, K2O, Fe y Mg en las hojas y los granos, nutrientes que juegan un papel fundamental en la síntesis de clorofilas y en la fotosíntesis (6161. Mohammadi K, Ghalavand A, Aghaalikhani M. Effect of organic matter and biofertilizers on chickpea quality and biological nitrogen fixation. World Academy of Science, Engineering and Technology [Internet]. 2010;44:1154-9. Available from: https://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.294.2140&rep=rep1&type=pdf ). Por otra parte, la coinoculación con Rhizobium y bacterias solubilizadoras de fosfato estimuló la acumulación de masa seca, el rendimiento y el contenido de proteínas de los granos (6262. Jat RS, Ahlawat IPS. Direct and Residual Effect of Vermicompost, Biofertilizers and Phosphorus on Soil Nutrient Dynamics and Productivity of Chickpea-Fodder Maize Sequence. Journal of Sustainable Agriculture [Internet]. 2006 [cited 24/08/2021];28(1):41-54. https://doi.org/10.1300/J064v28n01_05 ).

También, se han utilizado, en este cultivo, microorganismos a base de hongos micorrízicos arbusculares, HMA (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ,4747. Solaiman ARM, Rabbani MG, Hossain D, Hossain GMA, Alam MS. Influence of phosphorus and inoculation with Rhizobium and AM fungi on growth and dry matter yield of chickpea. Bangladesh Journal of Scientific Research [Internet]. 2012;25(1):23-32. Available from: https://www.researchgate.net/publication/325145221_Influence_of_phosphorus_and_inoculation_with_Rhizobium_and_AM_fungi_on_growth_and_dry_matter_yield_of_chickpea ), los cuales estimularon la productividad de los cultivos (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ) y mejoraron la absorción de P, Mn, K, Cu y Fe en las plantas (6363. Farzaneh M, Vierheilig H, Lössl A, Kaul HP. Arbuscular mycorrhiza enhances nutrient uptake in chickpea. Plant, Soil and Environment [Internet]. 2011;57(10):465-70. Available from: https://www.agriculturejournals.cz/publicFiles/133_2011-PSE.pdf ).

La inoculación del garbanzo con los hongos micorrízicos arbusculares Funneliformis mosseae y Rhizophagus irregularis, aumentó la biomasa y el rendimiento de las plantas y fueron efectivos para mejorar el valor nutricional del grano estimulando la concentración de proteínas, Fe y Zn, siendo mayores estos resultados cuando se utilizó un inóculo de origen local en lugar de uno foráneo (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ).

Se ha comprobado que la inoculación con HMA y la coinoculación HMA + Rhizobium etli, incrementó la altura, el número y la masa de los granos por planta (6464. Borbón-Gracia A, Pérez-Márquez J, García-Camarena MG, Ramírez-Soto M. Aplicación de biofertilizantes en el cultivo de garbanzo en Sinaloa. In: Primer Simposium Internacional de Agricultura Ecológica. México: INIFAP. Memoria Científica Número 1. p. 287-291 [Internet]. yumpu.com. 2009 [cited 19/09/2021]. Available from: https://www.yumpu.com/es/document/read/13989131/primer-simposium-internacional-de-agricultura-ecologica ), mientras que la coinoculación con Rhizobium, HMA y bacterias solubilizadoras de fosfato mejoró significativamente los indicadores de crecimiento y rendimiento de las plantas (4545. Pramanik K, Bera AK. Response of biofertilizers and phytohormone on growth and yield of chickpea (Cicer arietinium L.). Journal of Crop and Weed [Internet]. 2012;8(2):45-9. Available from: https://www.cropandweed.com/archives/2012/vol8issue2/10.pdf ).

Los resultados expuestos demuestran la efectividad de la inoculación de las semillas de garbanzo tanto con rizobacterias promotoras del crecimiento (RPCV) como con HMA o con la combinación de ellos para estimular el crecimiento y desarrollo de las plantas, lo que se traduce en un incremento del rendimiento y además en una mejor calidad nutricional de los granos. Por otra parte, se estimula la tolerancia de las plantas a estreses abióticos, así como se inhibe el crecimiento de diferentes patógenos causantes de enfermedades en el cultivo del garbanzo.

Productos a base de algas

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El uso de algas y productos elaborados a partir de estas se ha extendido a diferentes cultivos (6565. Povero G, Mejia JF, Di Tommaso D, Piaggesi A, Warrior P. A Systematic Approach to Discover and Characterize Natural Plant Biostimulants. Frontiers in Plant Science [Internet]. 2016 [cited 24/08/2021];7:435. https://doi.org/10.3389/fpls.2016.00435 -6868. Renuka N, Guldhe A, Prasanna R, Singh P, Bux F. Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnology Advances [Internet]. 2018 [cited 24/08/2021];36(4):1255-73. https://doi.org/10.1016/j.biotechadv.2018.04.004 ) y en el garbanzo, también se informa su uso para estimular el rendimiento y contrarrestar los efectos dañinos inducidos por plagas, enfermedades y estreses abióticos (6969. Beghdady MS. Influence of foliar spray with seaweed extract on growth, yield and its quality, profile of protein pattern and anatomical structure of chickpea plant (Cicer arietinum L.). Middle East Journal of Applied Sciences [Internet]. 2016 [cited 24/08/2021];6(1):207-221. Available from: http://www.publications.zu.edu.eg/Pages/PubShow.aspx?ID=34150&&pubID=18 -7171. Ahmadpour R, Salimi A, Armand N, Hosseinzadeh SR. The effects of Ascophyllum nodosum extract on the stimulation of germination indices in chickpea (Cicer arietinum) under drought stress. Nova Biologica Reperta [Internet]. 2019 [cited 24/08/2021];6(2):206-16. https://doi.org/10.29252/nbr.6.2.206 ).

Dos aplicaciones de 1 mL L^-1 de extracto de algas marinas, indujeron efectos promotores significativos sobre el crecimiento y el rendimiento e indujo cambios favorables en la calidad de la semilla y el perfil del patrón proteico del garbanzo. Además, indujo cambios favorables en la estructura anatómica de hojas y tallos, debido principalmente a un incremento marcado en el grosor de los tejidos de la corteza, el floema y el xilema (6969. Beghdady MS. Influence of foliar spray with seaweed extract on growth, yield and its quality, profile of protein pattern and anatomical structure of chickpea plant (Cicer arietinum L.). Middle East Journal of Applied Sciences [Internet]. 2016 [cited 24/08/2021];6(1):207-221. Available from: http://www.publications.zu.edu.eg/Pages/PubShow.aspx?ID=34150&&pubID=18 ).

Resultados similares muestran que, la aplicación foliar de extractos preparados a partir de las algas Kappaphycus alvarezzi y Gracilaria sp. al 10 %, mejoraron significativamente el rendimiento y sus componentes (1313. Yadav SL, Verma A, Nepalia V. Effect of phosphorus, sulphur and seaweed sap on growth, yield and nutrient uptake of chickpea ( Cicer arietinum L.). Research on Crops [Internet]. 2016 [cited 24/08/2021];17(3):496. https://doi.org/10.5958/2348-7542.2016.00082.6 ).

Por otra parte, la inoculación con la cianobacteria Anabaena laxa y la coinoculación de una biopelícula de Anabaena laxa-Rhizobium, han estimulado el contenido de leghemoglobina de los nódulos, así como la fijación de nitrógeno, el nitrógeno disponible y la actividad microbiana del suelo, lo que repercutió favorablemente sobre el crecimiento de la planta y el rendimiento en granos, obteniéndose el mejor resultado con la inoculación de Anabaena laxa (22. Bidyarani N, Prasanna R, Babu S, Hossain F, Saxena AK. Enhancement of plant growth and yields in Chickpea (Cicer arietinum L.) through novel cyanobacterial and biofilmed inoculants. Microbiological Research [Internet]. 2016 [cited 24/08/2021];188- 189:97-105. https://doi.org/10.1016/j.micres.2016.04.005 ).

Al tratar plantas de garbanzo con la microalga Chroococcus minutus y efluentes de destilería, se observó un mejor porcentaje de germinación, crecimiento y desarrollo de las plantas (7272. Murugesan S, Padmapriya C, Kotteswari M, Shanthi N. Effects of distillery effluent and micro alga (Chroococcus minutes) treated effluent on germination and seedling growth of Cicer arietinum L. International Journal of Applied Research [Internet]. 2017 [cited 24/08/2021];3(10):95-101. Available from: https://www.semanticscholar.org/paper/Effects-of-distillery-effluent-and-micro-alga-on-of-Murugesan-Padmapriya/41e36add67267c17ddc8c689be16583deb4cc7c9 ). También se ha observado que el uso de las cianobacterias Nostoc commune y Anabaena circinalis aisladas en el sudeste de Iraq, incrementó la habilidad de las plantas para fijar nitrógeno, lo cual influyó en el crecimiento y rendimiento del cultivo, ayudando a una reducción de 30-50 % del fertilizante químico (7373. Sanaa j B, Jawad A latif M, Al-Ani NK. Effect of Two Species of Cyanobacteria as Biofertilizers on Characteristics and Yield of Chickpea Plant. Iraqi Journal of Science [Internet]. 2014 [cited 24/08/2021];55(2Supplement). Available from: https://www.iasj.net/iasj/article/91918 ).

En tejidos de garbanzo tratados con preparaciones de polisacáridos de Hypnea musciformis (algas rojas), Padina tetrastromatica (algas pardas) y Ulva lactulus (algas verdes), se identificaron fitoalexinas inducidas (6767. Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, et al. Seaweed Extracts as Biostimulants of Plant Growth and Development. Journal of Plant Growth Regulation [Internet]. 2009 [cited 24/08/2021];28(4):386-99. https://doi.org/10.1007/s00344-009-9103-x ). También se comprobó que un inductor de resistencia a estrés biótico (k-carragenano), obtenido de Hypnea musciformis, indujo fitoalexinas en los tejidos de las semillas (7474. Arman M. LC-ESI-MS characterisation of phytoalexins induced in chickpea and pea tissues in response to a biotic elicitor of Hypnea musciformis (red algae). Natural Product Research [Internet]. 2011 [cited 24/08/2021];25(14):1352-60. https://doi.org/10.1080/14786419.2011.553952 ). Además, la aplicación de una solución de este polisacárido alrededor de las semillas, en el momento de la siembra, estimuló los indicadores de crecimiento, indujo una floración temprana y produjo un alto contenido de metabolitos secundarios asociados a la resistencia a enfermedades en hojas, tallos y granos de las plantas (7575. Arman M. Carrageenan as an elicitor of induced secondary metabolites and its effects on various growth characters of chickpea... Journal of Saudi Chemical Society [Internet]. 2011;15:269-73. Available from: https://d1wqtxts1xzle7.cloudfront.net/50686815/Carrageenan_as_an_elicitor_of_induced_se20161202-16827-dpg3he-with-cover-page-v2.pdf?Expires=1632536358&Signature=fqnTjxgnvr42mW5voun6QlSp9UhqTOnGvEkDB1CaEjYY1BT6ooJp2IZkhrNX1YQiVQToT7if8pH3tt~CBuCFeKW5FEMJYF7o62VuxEBcNNyKcxmcawmTNEczMk7JtnrebfIo9NQPDHPPQ5N1R4mB2Q1W~Nx63~po7mIjkaMBtBTM2h79z21GPy~FKG68nTb8nc2ApsmxNQ-dkw-28fQ1qgvxu67Ee4JzgqXqq2Su0-txHYPTCqgEpz5JfGKaqLpWUAYD4Nadn14xruXp5rSCzpleMNBEM6~7AVNDxfZHbNWPqEwEVtooyGM5eOARf10SwJ9-nir0Z2kROlXTfmpa-Q&Key-Pair-Id=APKAJLOHF5GGSLRBV4ZA ).

Otros resultados muestran que extractos fenólicos de Spirulina presentan actividad antifúngica contra Fusarium graminearum (7676. Pagnussatt FA, Kupski L, Darley FT, Filoda PF, Ponte ÉMD, Garda-Buffon J, et al. Fusarium graminearum growth inhibition mechanism using phenolic compounds from Spirulina sp. Food Science and Technology [Internet]. 2013;33:75-80. Available from: https://www.scielo.br/j/cta/a/mkt7HrHsZDSnHgGfZy4rZPm/?lang=en&format=pdf ,7777. Pagnussatt FA, de Lima VR, Dora CL, Costa JAV, Putaux J-L, Badiale-Furlong E. Assessment of the encapsulation effect of phenolic compounds from Spirulina sp. LEB-18 on their antifusarium activities. Food Chemistry [Internet]. 2016 [cited 24/08/2021];211:616-23. https://doi.org/10.1016/j.foodchem.2016.05.098 ). Por otra parte, extractos de Sargassum muticum y Jania rubens, mejoraron los indicadores de crecimiento en plantas de garbanzo sometidas a estrés salino y estimularon las actividades de las enzimas superóxido dismutasa y peroxidasa. A la vez se identificaron en estos extractos, cuatro aminoácidos claves, incluyendo serina, treonina, prolina y ácido aspártico a partir de sus raíces, los cuales contribuyen a mejorar la tolerancia ante un estrés salino (7878. Abdel Latef AAH, Srivastava AK, Saber H, Alwaleed EA, Tran L-SP. Sargassum muticum and Jania rubens regulate amino acid metabolism to improve growth and alleviate salinity in chickpea. Scientific Reports [Internet]. 2017 [cited 24/08/2021];7(1):10537. https://doi.org/10.1038/s41598-017-07692-w ).

Además, se ha recomendado el uso de extractos de Ascophyllum nodosum para reducir los efectos negativos del estrés por sequía en la germinación de semillas de garbanzo (7171. Ahmadpour R, Salimi A, Armand N, Hosseinzadeh SR. The effects of Ascophyllum nodosum extract on the stimulation of germination indices in chickpea (Cicer arietinum) under drought stress. Nova Biologica Reperta [Internet]. 2019 [cited 24/08/2021];6(2):206-16. https://doi.org/10.29252/nbr.6.2.206 ). Los productos formulados a base de algas en el garbanzo, no sólo presentan efectos sobre la estimulación de la germinación, el crecimiento y el rendimiento, sino también ayudan a mejorar la calidad de las cosechas y estimulan la tolerancia a diferentes estreses abióticos, además de presentar propiedades antifúngicas.

Productos a base de quitosano

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El quitosano es un biopolímero que actúa como promotor del crecimiento vegetal en algunos cultivos, incrementa la producción y protege a las plantas contra patógenos. Tiene un efecto significativo sobre el crecimiento de raíces y tallos y estimula la floración y el número de flores. Estas moléculas son fuertemente hidrofílicas y atenúan el daño provocado por el estrés en las células vegetales (7979. Pandey P, Verma MK, De N. Chitosan in agricultural context-A review. Bull. Environ. Pharmacol. Life Sci [Internet]. 2018;7:87-96. Available from: https://www.researchgate.net/profile/Priyal-Pandey/publication/326682315_Chitosan_in_agricultural_context_-_A_review/links/5b72ddc792851ca6505d7c61/Chitosan-in-agricultural-context-A-review.pdf ). Por estas razones ha sido utilizado por los agricultores como biopesticida y biofertilizante desde la década del 80 del pasado siglo y para esto se ha aplicado como enmienda del suelo, por aspersión foliar, a frutos y semillas, tanto solo como en combinación con otros tratamientos para prevenir el desarrollo de enfermedades en las plantas o acelerar las defensas innatas de las mismas contra patógenos (8080. Malerba M, Cerana R. Recent Applications of Chitin- and Chitosan-Based Polymers in Plants. Polymers [Internet]. 2019 [cited 24/08/2021];11(5):839. https://doi.org/10.3390/polym11050839 -8383. Jabnoun-Khiareddine H, El-Mohamedy RSR, Abdel-Kareem F, Abdallah RAB, Gueddes-Chahed M, Daami-Remadi M. Variation in chitosan and salicylic acid efficacy towards soil-borne and air-borne fungi and their suppressive effect of tomato wilt severity. J Plant Pathol Microbiol. 2015;6(325):2.).

En el cultivo del garbanzo se ha comprobado que, durante la germinación, semillas tratadas con quitosano excretaron varias proteínas, que tienen un efecto inhibitorio in vitro sobre el crecimiento del hongo Fusarium oxysporum f. sp. ciceris y, por ende, estos exudados protegen a las semillas de los patógenos del suelo, durante la germinación (8484. Anusuya S, Sathiyabama M. Identification of defence proteins from the seed exudates of Cicer arietinum L. and its effect on the growth of Fusarium oxysporum f.sp. ciceri. Archives of Phytopathology and Plant Protection [Internet]. 2014 [cited 24/08/2021];47(13):1611-20. https://doi.org/10.1080/03235408.2013.853457 ). Más recientemente, se identificaron 325 proteínas y 65 metabolitos asociados a la respuesta inmune estimulada por el quitosano ante Fusarium en este cultivo, los cuales están relacionados con la producción de especies activas de oxígeno, el movimiento estomático, el desarrollo de los nódulos y la arquitectura de las raíces (8585. Narula K, Elagamey E, Abdellatef MAE, Sinha A, Ghosh S, Chakraborty N, et al. Chitosan-triggered immunity to Fusarium in chickpea is associated with changes in the plant extracellular matrix architecture, stomatal closure and remodeling of the plant metabolome and proteome. The Plant Journal [Internet]. 2020 [cited 24/08/2021];103(2):561-83. https://doi.org/10.1111/tpj.14750 ).

En los últimos años, se ha comprobado que las nanopartículas de quitosano pueden actuar como estimuladores del crecimiento y como agentes antimicrobianos contra hongos patógenos y bacterias en la agricultura. Además, pueden actuar como nanoconductores para otros agroquímicos existentes (8686. Maluin FN, Hussein MZ. Chitosan-Based Agronanochemicals as a Sustainable Alternative in Crop Protection. Molecules [Internet]. 2020 [cited 24/08/2021];25(7):1611. https://doi.org/10.3390/molecules25071611 ). Así, se ha demostrado que nanocompuestos de quitosano y de quitosano-metales mostraron una buena actividad antifúngica contra Fusarium oxysporum f. sp. ciceris en el cultivo del garbanzo y además, estimularon el crecimiento de las plantas, en comparación con las plantas control. Se destacaron los nanocompuestos quitosano-CuO y quitosano-ZnO en la reducción de la enfermedad provocada por el patógeno (8787. Kaur P, Duhan JS, Thakur R. Comparative pot studies of chitosan and chitosan- metal nanocomposites as nano-agrochemicals against fusarium wilt of chickpea (Cicer arietinum L.). Biocatalysis and Agricultural Biotechnology [Internet]. 2018 [cited 24/08/2021];14:466-71. https://doi.org/10.1016/j.bcab.2018.04.014 ).

También, nanopartículas de quitosano-Ag mostraron un efecto promotor sustancial del crecimiento, dado por una estimulación en la germinación de las semillas, en la longitud y masa fresca y seca de las plantas. Se encontró un incremento en el contenido de clorofilas y en las actividades de las enzimas ascorbato peroxidasa, catalasa y peroxidasa, lo que abre la posibilidad de usar estas nanopartículas como estimuladores del crecimiento en el cultivo del garbanzo (8888. Anusuya S, Banu KN. Silver-chitosan nanoparticles induced biochemical variations of chickpea (Cicer arietinum L.). Biocatalysis and Agricultural Biotechnology [Internet]. 2016 [cited 24/08/2021];8:39-44. https://doi.org/10.1016/j.bcab.2016.08.005 ). Un efecto positivo en la germinación, el crecimiento y en la inducción de enzimas defensivas de plantas de garbanzo, se encontró además, cuando se utilizaron nanopartículas de quitosano cargadas con tiamina (8989. Muthukrishnan S, Murugan I, Selvaraj M. Chitosan nanoparticles loaded with thiamine stimulate growth and enhances protection against wilt disease in Chickpea. Carbohydrate Polymers [Internet]. 2019 [cited 24/08/2021];212:169-77. https://doi.org/10.1016/j.carbpol.2019.02.037 ).

Todos estos resultados revelan las potencialidades de los productos a base de quitosano para ser usados como estimuladores del crecimiento y el rendimiento y como bioprotectores ante el ataque de determinados patógenos en el cultivo del garbanzo.

Otros bioestimulantes

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Varios resultados han mostrado que la aplicación de determinadas dosis de ácidos húmicos al suelo en el momento de la siembra y en prefloración, estimuló el crecimiento y el rendimiento en granos (9090. Kahraman A. Effect of humic acid applications on the yield components in chickpea. Journal of Agricultural Faculty of Gaziosmanpasa University [Internet]. 2017;34(1):218-22. Available from: https://www.researchgate.net/profile/Ali- Kahraman-8/publication/316446044_Humik_Asit_Uygulamalarinin_Nohutta_Verim_Bilesenleri_Uzerine_Etkileri/links/59cac8e2aca272bb0507977f/Humik-Asit-Uygulamalarinin- Nohutta-Verim_Bilesenleri-Uezerine-Etkileri.pdf ), así como el rendimiento en proteínas de plantas de garbanzo de la variedad 'Çağatay' en Turquía (9191. Kahraman A. Managing the Humic Acid Fertilizing of Chickpea and Protein Status. Selcuk Journal of Agriculture and Food Sciences [Internet]. 2020 [cited 24/08/2021];34(1):107-10. https://doi.org/10.15316/SJAFS.2020.202 ). Resultados similares fueron informados, posteriormente, en cuanto a la estimulación del rendimiento y sus componentes en plantas sometidas a diferentes regímenes de riego (9292. Abhari A, Gholinezhad E. Effect of humic acid on grain yield and yield components in chickpea under different irrigation levels. Journal of Plant Physiology and Breeding [Internet]. 2019 [cited 24/08/2021];9(2):19-29. https://doi.org/10.22034/jppb.2019.10441 ).

Además, la aspersión foliar de ácidos húmicos y ácido naftalenacético (ANA) estimuló el crecimiento de las plantas a través del incremento de indicadores como la altura, el número de ramas, el área foliar, la masa seca total, así como componentes del rendimiento como el número de vainas por planta, la masa de 100 semillas y el rendimiento de semillas por hectárea (9393. Kapase PV, Deotale RD, Sawant PP, Sahane AN, Banginwar AD. Effect of foliar sprays of humic acid through vermicompost wash and NAA on morpho-physiological parameters, yield and yield contributing parameters of chickpea. Journal of Soils and Crops [Internet]. 2014;24(1):107-14. Available from: https://www.ascrsnagpur.com/DemoPaper/botony.pdf ).

Por otra parte, se ha informado, también, la eficacia de los ácidos húmicos en reducir la severidad del marchitamiento de las plantas de garbanzo cv. Giza 3, causado por el hongo Fusarium oxysporum f. sp. ciceris (9494. Abdel-Monaim MF, Morsy M K, Zyan AH. Efficacy of some organic compounds in controlling Fusarium wilt disease, growth and yield parameters in Chickpea plants. Egyptian Journal of Agricultural Research [Internet]. 2018;96(2):351-64. Available from: https://ejar.journals.ekb.eg/article_132936_c86bccaf9568ec257c34ed7acb3a5d55.pdf ).

En Cuba, el uso de Fitomas-E, a razón de 0,5 L ha^-1 en plantas de garbanzo variedad N-27, incrementó el número de vainas y granos por planta, la masa de 100 granos y el rendimiento, en condiciones normales y bajo estrés por sequía (2323. Meriño-Hernández Y, Rodríguez-Hernández P, Cartaya-Rubio O, Dell’Amico- Rodríguez JM, Boicet-Fabré T, Shagarodsky-Scull T, et al. Acumulación de iones y tolerancia a la salinidad en diferentes cultivares cubanos de garbanzo (Cicer arietinum L.). Cultivos Tropicales [Internet]. 2018 [cited 24/08/2021];39(4):42-50. Available from: http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S0258-59362018000400006&lng=es&nrm=iso&tlng=pt ).

El tratamiento de semillas de garbanzo sometidas a estrés osmótico leve, con ácido elágico (50 ppm), aislado y purificado a partir de Padina boryana Thivy, aceleró la germinación y el crecimiento de las plántulas; además, estimuló la capacidad antioxidante total, a través del incremento de algunos metabolitos y enzimas antioxidantes (9595. El-Soud WA, Hegab MM, AbdElgawad H, Zinta G, Asard H. Ability of ellagic acid to alleviate osmotic stress on chickpea seedlings. Plant Physiology and Biochemistry [Internet]. 2013 [cited 24/08/2021];71:173-83. https://doi.org/10.1016/j.plaphy.2013.07.007 ).

Use of biostimulants in chickpea cultivation

^iDIndira López-Padrón^*✉:shari@inca.edu.cu

^iDLisbel Martínez-González

^iDGeydi Pérez-Domínguez

^iDYanelis Reyes-Guerrero

^iDMiriam Núñez-Vázquez

^iDJuan A. Cabrera-Rodríguez

Instituto Nacional de Ciencias Agrícolas (INCA), carretera San José-Tapaste, km 3½, Gaveta Postal 1, San José de las Lajas, Mayabeque, Cuba. CP 32 700.

^{^*}Author for correspondence: shari@inca.edu.cu

Abstract

Chickpea (Cicer arietinum L.) is one of the most important legumes in the world with a production of around 9 million tons. The crop is sensitive to several abiotic stresses such as: salinity, extreme temperatures and excess or deficiency of soil moisture; in addition, it can be affected by several pests and diseases. Adverse effects of the indiscriminate use of chemical products in agriculture have led to the use of various biostimulants in chickpea as a safe alternative to the use of these products, both for the supply of nutrients to plants and for the control and management of pests and diseases, as well as for the induction of tolerance to abiotic stresses. The use of plant growth-promoting bacteria (PGPB) as biofertilizers has been one of the most widely used practices in this crop, although arbuscular mycorrhizal fungi, co-inoculation of bacteria of different genera and of bacteria and fungi have also been used. In addition, the use of other biostimulants such as algae or chitosan-based products has been reported to increase grain yield and quality. The aim of this literature review is to give an updated view on biostimulant use in chickpea cultivation, with emphasis on those based on beneficial microorganisms, algal extracts and chitosan.

Key words:

Cicer arietinum, rhizobacteria, mycorrhizae, algae, chitosan

Most used biostimulants in chickpea cultivation

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Among the most widely used biostimulants in chickpea cultivation are beneficial microorganisms, algae extracts and, in recent years, chitosan nanoparticles, either alone or loaded with some metals or other substances. Humic substances and Fitomas-E, among others, have also been used.

Beneficial microorganisms

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Several studies have demonstrated the influence of beneficial microorganisms on nodulation, growth and yield (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf -3232. Kumari N, Mondal S, Mahapatra P, Meetei TT, Devi YB. Effect of Biofertilizer and Micronutrients on Yield of Chickpea. International Journal of Current Microbiology and Applied Sciences [Internet]. 2019;8(01):2389-97. Available from: https://www.ijcmas.com/8-1-2019/Nirmala%20Kumari,%20et%20al.pdf ), on grain protein content (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,2828. Saini R, Dudeja SS, Giri R, Kumar V. Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. Journal of Basic Microbiology [Internet]. 2015 [cited 24/08/2021];55(1):74-81. https://doi.org/10.1002/jobm.201300173 ,3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ) and on biofortification (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ). In addition, they stimulate the N, P, K uptake, the activity of the antioxidant enzymes SOD and POD and the increase of organic acid concentrations, thereby reducing rhizosphere pH (3434. Israr D, Mustafa G, Khan KS, Shahzad M, Ahmad N, Masood S. Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum L.) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiology and Biochemistry [Internet]. 2016 [cited 24/08/2021];108:304-12. https://doi.org/10.1016/j.plaphy.2016.07.023 ). These effects are associated with the ability of these microorganisms to produce siderophores and HCN (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ), solubilize minerals such as phosphorus (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3636. Ansari MF, Tipre DR, Dave SR. Efficiency evaluation of commercial liquid biofertilizers for growth of Cicer aeritinum (chickpea) in pot and field study. Biocatalysis and Agricultural Biotechnology [Internet]. 2015 [cited 24/08/2021];4(1):17-24. https://doi.org/10.1016/j.bcab.2014.09.010 ), increase root exudation (3434. Israr D, Mustafa G, Khan KS, Shahzad M, Ahmad N, Masood S. Interactive effects of phosphorus and Pseudomonas putida on chickpea (Cicer arietinum L.) growth, nutrient uptake, antioxidant enzymes and organic acids exudation. Plant Physiology and Biochemistry [Internet]. 2016 [cited 24/08/2021];108:304-12. https://doi.org/10.1016/j.plaphy.2016.07.023 ,3737. Akrami M, Khiavi HK, Shikhlinski H, Khoshvaghtei H. Biocontrolling two pathogens of chickpea Fusarium solani and Fusarium oxysporum by different combinations of Trichoderma harzianum, Trichoderma asperellum and Trichoderma virens under field condition. International Journal of Agricultural Science Research [Internet]. 2012;1(3):41-5. Available from: https://www.internationalscholarsjournals.com/articles/bio-controlling-two-pathogens-of-chickpea-fusarium-solani-and-fusarium-oxysporum-by-differentcombinations-of- trichoderma.pdf ), chelate iron (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ), fix atmospheric nitrogen (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ,3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ), synthesize phytohormones (3535. Verma J, Yadav J. Evaluation of plant growth promoting rhizobacteria and their effect on plant growth and grain yield of chickpea (Cicer arietinum L.) under sustainable agriculture production. Int. J. Res. Eng. IT Soc. Sci. [Internet]. 2012;2:51-7. Available from: https://www.researchgate.net/publication/285880641_Evaluation_of_plant_growth_promoting_rhizobacteria_and_their_effect_on_plant_growth_and_grain_yield_of_chickpea_Cicer_arietinum_L_under_sustainable_agriculture_production ,3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ,4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ), and inhibit infection by phytopathogens (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,3737. Akrami M, Khiavi HK, Shikhlinski H, Khoshvaghtei H. Biocontrolling two pathogens of chickpea Fusarium solani and Fusarium oxysporum by different combinations of Trichoderma harzianum, Trichoderma asperellum and Trichoderma virens under field condition. International Journal of Agricultural Science Research [Internet]. 2012;1(3):41-5. Available from: https://www.internationalscholarsjournals.com/articles/bio-controlling-two-pathogens-of-chickpea-fusarium-solani-and-fusarium-oxysporum-by-differentcombinations-of- trichoderma.pdf ,4141. Echevarría A, Triana A, Rivero D, Rodríguez A, Martínez B. Generalidades del cultivo de garbanzo y alternativa biológica para el control de la Marchitez. Cultivos Tropicales [Internet]. 2019 [cited 24/08/2021];40(4). Available from: http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S0258-59362019000400010&lng=es&nrm=iso&tlng=es ,4242. Albuquerque da Silva Campos M. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection [Internet]. 2020 [cited 24/08/2021];135:105203. https://doi.org/10.1016/j.cropro.2020.105203 ).

Among these microorganisms, the use of plant growth-promoting bacteria (PGPB) has become one of the most attractive options to improve the sustainability of agricultural systems in many parts of the world, due to its respect for the environment, the low cost of production and the reduced use of non-renewable resources (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ); being one of the most used practices in chickpea crop (4343. Dibut B, Shagarodsky T, Martínez R, Ortega M, Ríos Y, Fey L. Biofertilización del garbanzo (Cicer arietinum L.) con Mesorhizobium cicerii cultivado sobre suelo Ferralítico Rojo. Cultivos Tropicales [Internet]. 2005;26(1):5-9. Available from: https://www.redalyc.org/pdf/1932/193215916001.pdf ).

Among these bacteria, the nitrogen fixing bacteria of the genus Rhizobium are the most used in this crop (3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ,4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ,4343. Dibut B, Shagarodsky T, Martínez R, Ortega M, Ríos Y, Fey L. Biofertilización del garbanzo (Cicer arietinum L.) con Mesorhizobium cicerii cultivado sobre suelo Ferralítico Rojo. Cultivos Tropicales [Internet]. 2005;26(1):5-9. Available from: https://www.redalyc.org/pdf/1932/193215916001.pdf -4747. Solaiman ARM, Rabbani MG, Hossain D, Hossain GMA, Alam MS. Influence of phosphorus and inoculation with Rhizobium and AM fungi on growth and dry matter yield of chickpea. Bangladesh Journal of Scientific Research [Internet]. 2012;25(1):23-32. Available from: https://www.researchgate.net/publication/325145221_Influence_of_phosphorus_and_inoculation_with_Rhizobium_and_AM_fungi_on_growth_and_dry_matter_yield_of_chickpea ). The application of bacteria of this genus to chickpea seeds has normally been sufficient to provide the necessary amounts of N to plants; nevertheless, it is advisable to supply small amounts of this mineral (4444. Cota AG, Yañez GA, Esquer EJ, Anduaga R, Barrón JM. Efecto de la variedad y la fertilización en indicadores de calidad proteica in-vitro de dos variedades y una línea de garbanzo (Cicer arietinum). Revista chilena de nutrición [Internet]. 2010;37(2):193-200. Available from: https://scielo.conicyt.cl/scielo.php?pid=S0717-75182010000200008&script=sci_arttext&tlng=n ).

In a previous study, it was reported that the application of two Cuban strains of Mesorhizobium sp. from a suspension in water at a ratio of 1:10 (v:v) enhanced both growth (height, diameter, total plant mass and dry mass of nodules) and yield (number and pod mass and number and mass of grains per plant) (3939. Ortega García M, Shagarodsky Scull T, Dibut Álvarez BL, Ríos Rocafull Y, Tejeda González G, Gómez Jorrin LA. Influencia de la interacción entre el cultivo del garbanzo (Cicer arietinum L.) y la inoculación con cepas seleccionadas de Mesorhizobium spp. Cultivos Tropicales [Internet]. 2016;37:20-7. Available from: http://scielo.sld.cu/scielo.php?pid=S0258-59362016000500003&script=sci_arttext&tlng=pt ). Similar results were obtained in Spain, with two isolated strains of the genus Mesorhizobium (FCAP 26 and FCAP 04), which were able to increase the number of nodules and enhance plant development under greenhouse and field conditions, as well as to increase grain production (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ).

In Montecillo, Mexico State, inoculation of chickpea seeds with Rhizobium etli stimulated leaf area index, greenness index and grain yield (4848. Barrios MMA, Estrada JASE, González MMTR, Barrios PA. Rendimientode garbanzo verde en función de la densidad de población, biofertilización y fertilización foliar. Academia Journals. 2017;6(2):129. Available from: https://www.researchgate.net/profile/Patricio-Apaez-Barrios/publication/322939694_RENDIMIENTO_DE_GARBANZO_VERDE_EN_FUNCION_DE_LA_DENSIDAD_DE_POBLACION_BIOFERTILIZACION_Y_FERTILIZACION_FOLIAR/links/5a78b1c2a6fdcc4ffe90b1ed/RENDIMIENTO-DE-GARBANZO-VERDE-EN-FUNCION-DE_LA_DENSIDAD_DE_POBLACION_BIOFERTILIZACION_Y_FERTILIZACION_FOLIAR.pdf ).

In addition, Rhizobium strains have been shown to produce volatile compounds that inhibit the growth of some soil pathogens such as R. solani (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ).

Other bacteria have also shown their positive effects on chickpea cultivation. Thus, it was found that the use of bacteria of Azotobacter vinelandii and Burkholderia cepacia species, in a degraded and compacted sodic lateritic soil of clayey texture from Mexico, with an organic matter content of 1.5 % and organic N 39 kg ha-1 and with 50 % nitrogenous background, stimulated the growth and plant development (4949. Sánchez-Yáñez JM, Villegas-Moreno J, Vela-Muzquiz GR, Marquez-Benavides L. Respuesta del garbanzo (Cicer arietinum L.) a la inoculación con Azotobacter vineladii y Burkholderia cepacia a dosis reducida de fertilizante nitrogenado. Scientia Agropecuaria [Internet]. 2014 [cited 24/08/2021];5(3):115-20. https://doi.org/10.17268/sci.agropecu.2014.03.01 ). In India, commercial liquid biofertilizers containing Azotobacter strains or phosphate solubilizers showed beneficial effects on germination and average sprout length in controlled environments and on yield under controlled and field conditions (3636. Ansari MF, Tipre DR, Dave SR. Efficiency evaluation of commercial liquid biofertilizers for growth of Cicer aeritinum (chickpea) in pot and field study. Biocatalysis and Agricultural Biotechnology [Internet]. 2015 [cited 24/08/2021];4(1):17-24. https://doi.org/10.1016/j.bcab.2014.09.010 ).

In studies conducted for the Fusarium oxysporum control in chickpea, it was found that isolates of Trichoderma viride and Trichoderma harzianum, besides decreasing the incidence of Fusarium wilt (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ), improved seed germination (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ,5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ), stimulated plant growth indicators such as root and sprout length (5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ) and dry mass (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ), as well as yield (5050. Shabir-U-Rehman, Dar WA, Ganie SA, Bhat JA, Mir GH, Lawrence R, et al. Comparative efficacy of Trichoderma viride and Trichoderma harzianum against Fusarium oxysporum f sp. ciceris causing wilt of chickpea. African Journal of Microbiology Research [Internet]. 2013 [cited 24/08/2021];7(50):5731-6. https://doi.org/10.5897/AJMR2013.6442 ,5151. Dubey SC, Suresh M, Singh B. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biological Control [Internet]. 2007 [cited 24/08/2021];40(1):118-27. https://doi.org/10.1016/j.biocontrol.2006.06.006 ). On the other hand, in Argentina, when evaluating the biocontrol activity of Trichoderma atroviride against soil pathogens, a lower incidence of diseases during the crop cycle was found, where a higher biocontrol power was observed when used on the seed together with a biopolymer, although these results were also observed when used only on the seed and applied to the soil (5252. Caballero WA, Senés PJ, Toumanián AG. Evaluación de la capacidad biocontroladora de Trichoderma atroviride en el cultivo de garbanzo (Cicer arietinum L.) [Internet]. 2016. Available from: https://rdu.unc.edu.ar/handle/11086/4847 ).

Bacteria of the genus Pseudomonas are also widely used for growth and yield stimulation in chickpea and it has been demonstrated their effectiveness to reduce the use of chemical fertilizer (5353. Joshi D, Chandra R, Suyal DC, Kumar S, Goel R. Impacts of Bioinoculants Pseudomonas jesenii MP1 and Rhodococcus qingshengii S10107 on Chickpea (Cicer arietinum L.) Yield and Soil Nitrogen Status. Pedosphere [Internet]. 2019 [cited 24/08/2021];29(3):388-99. https://doi.org/10.1016/S1002-0160(19)60807-6 ), besides reducing in in vitro tests the growth of Rhizoctonia bataticola and Sclerotinias clerotiorumover and applied to seeds, they reduce in field tests the incidence of dry root rot disease and stem rot caused by these fungi (5454. Patel DB, Singh HB, Shroff S, Sahu J. Antagonistic efficiency of Pseudomonas strains against soil borne disease of chickpea crop under in vitro and in vivo. Elixir Agriculture [Internet]. 2011;30:1774-7. Available from: https://www.elixirpublishers.com/articles/1351083604_30%20(2011)%201774- 1777.pdf). Pseudomonas aeruginosa was also shown to suppress wilt and root rot caused by Fusarium oxysporum f. sp. ciceris and Rhizoctonia solani, respectively (4040. Yadav J, Verma JP. Effect of seed inoculation with indigenous Rhizobium and plant growth promoting rhizobacteria on nutrients uptake and yields of chickpea (Cicer arietinum L.). European Journal of Soil Biology [Internet]. 2014 [cited 24/08/2021];63:70-7. https://doi.org/10.1016/j.ejsobi.2014.05.001 ). The species Pseudomonas fluorescens influenced vascular wilt of chickpea caused by Fusarium oxysporum f. sp. ciceris (5555. Ramezani H. Efficacy of some fungal and bacterial bioagents against Fusarium oxysporum f. sp. ciceris on chickpea. Plant Protection Journal. 2009;1(1):108-113) and salt-tolerant species of the genus Pseudomonas have increased the health of chickpea subjected to salinity stress, observing that Pseudomonas putida RA modulated the expression of genes sensitive to salt stress (5656. Jatan R, Chauhan PS, Lata C. Pseudomonas putida modulates the expression of miRNAs and their target genes in response to drought and salt stresses in chickpea (Cicer arietinum L.). Genomics [Internet]. 2019 [cited 24/08/2021];111(4):509-19. https://doi.org/10.1016/j.ygeno.2018.01.007 ).

In another study, two P-Zn solubilizing bacterial strains (Bacillus sp. strain AZ17 and Pseudomonas sp. strain AZ5) increased grain yield, nodule number, nodule dry mass, and Zn and P uptake in two types of chickpea grown in fertilized and unfertilized soil, with better results obtained with the Pseudomonas sp. strain (3131. Zaheer A, Malik A, Sher A, Mansoor Qaisrani M, Mehmood A, Ullah Khan S, et al. Isolation, characterization, and effect of phosphate-zinc-solubilizing bacterial strains on chickpea (Cicer arietinum L.) growth. Saudi Journal of Biological Sciences [Internet]. 2019 [cited 24/08/2021];26(5):1061-7. https://doi.org/10.1016/j.sjbs.2019.04.004 ). It has also been reported that Pseudomonas putida NBRIRA and Bacillus amyloliquefaciens NBRISN13 strains, both alone and in consortium, were able to improve drought stress in sensitive and tolerant chickpea cultivars; obtaining a better response when strains were used in consortium (5757. Kumar M, Mishra S, Dixit V, Kumar M, Agarwal L, Chauhan PS, et al. Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signaling & Behavior [Internet]. 2016 [cited 24/08/2021];11(1):e1071004. https://doi.org/10.1080/15592324.2015.1071004 ). Inoculation with two isolates of the genus Bacillus, from the rhizosphere of chickpea plants, promoted plant growth under greenhouse conditions and presented strong in vitro antagonism to F. oxysporum, F. solani and R. solani, in addition to the production of siderophores in CAS medium, solubilization of inorganic phosphorus and production of gibberellic acid (1818. Herrera EF, Rentería MEM, Salazar SFM, Peña NJ, Bustos IIR. Bacteria of the chickpea rhizosphere with antagonistic capacity to phytopathogenous fungi and plant growth promotion. Tropical and Subtropical Agroecosystems [Internet]. 2018 [cited 24/08/2021];21(3). Available from: https://www.revista.ccba.uady.mx/ojs/index.php/TSA/article/view/2548 ). It has been proved that Bacillus subtilis influenced the vascular wilt of chickpea caused by Fusarium oxysporum f. sp. ciceris (5555. Ramezani H. Efficacy of some fungal and bacterial bioagents against Fusarium oxysporum f. sp. ciceris on chickpea. Plant Protection Journal. 2009;1(1):108-113).

Other results have shown that isolates of Serratia marcescens increased crop grain yield in fertile soils in irrigated areas and nutrient-deficient soils in rainfed areas (5858. Zaheer A, Mirza BS, Mclean JE, Yasmin S, Shah TM, Malik KA, et al. Association of plant growth-promoting Serratia spp. with the root nodules of chickpea. Research in Microbiology [Internet]. 2016 [cited 24/08/2021];167(6):510-20. https://doi.org/10.1016/j.resmic.2016.04.001 ) and strains of Streptomyces sp. exhibited greater number and mass of nodules, as well as greater root and sprout mass at 30 days after sowing (DAS) and increased the number and pod mass, leaf area, leaf and stem masses at 60 DAS, and consequently, at harvest, grain yield was higher (3838. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Rathore A, et al. The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus [Internet]. 2015 [cited 24/08/2021];4(1):31. https://doi.org/10.1186/s40064-015-0811-3 ).

Likewise, inoculation with a strain of Azospirillum lipoferum (FK1) improved the salinity tolerance of chickpea plants, expressed by significant stimulation of nutrient uptake, biomass, photosynthetic pigment synthesis, gas exchange, phenol and flavonoid content, and enzymatic and non-enzymatic antioxidant levels. In addition, inoculated plants revealed lower percentages of electrolyte efflux, H2O2 and MDA and exhibited high levels of expression of genes related to salt tolerance (5959. El-Esawi MA, Al-Ghamdi AA, Ali HM, Alayafi AA. Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environmental and Experimental Botany [Internet]. 2019 [cited 24/08/2021];159:55-65. https://doi.org/10.1016/j.envexpbot.2018.12.001 ).

On the other hand, a strain of Aneurinibacillus migulanus (FSZ 28) isolated from nodules of Cicer arietinum L. grown in soil from Fuentesaúco locality in Zamora (Spain), showed the ability to inhibit the growth of different Fusarium species (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ). More recently, a plant growth-promoting rhizobacterial strain identified as Cedecea davisae RS3 was isolated from the rhizosphere of chickpea plants, which improved crop performance under nitrogen deficit conditions (6060. Mazumdar D, Saha SP, Ghosh S. Isolation, screening and application of a potent PGPR for enhancing growth of Chickpea as affected by nitrogen level. International Journal of Vegetable Science [Internet]. 2020 [cited 24/08/2021];26(4):333-50. https://doi.org/10.1080/19315260.2019.163240 ).

Favorable results have also been found with the co-inoculation of PGPB. Thus, in greenhouse trials, it was found that co-inoculation with Mesorhizobium sp. FCAP 26 and Bacillus halotolerans FSZ 47 stimulated plant growth and development and seed production. In addition, a rotation cycle with wheat increased soil carbon and nitrogen content (4646. Cruz González XA. Análisis genotípico, fenotípico y funcional de bacterias aisladas de nódulos de Cicer arietimum L. para la evaluación de su potencial como biofertilizantes agrícolas en cultivos de garbanzo y trigo. 2018 [cited 24/08/2021]; https://doi.org/10.14201/gredos.139493 ).

Other results showed that co-inoculation with Bacillus lentus, Pseudomonas putida and Trichoderma harzianum, produced the highest yield in grains, besides, it propitiated a higher content of N, P2O5, K2O, Fe and Mg in leaves and grains, nutrients that play a fundamental role in the synthesis of chlorophylls and photosynthesis (6161. Mohammadi K, Ghalavand A, Aghaalikhani M. Effect of organic matter and biofertilizers on chickpea quality and biological nitrogen fixation. World Academy of Science, Engineering and Technology [Internet]. 2010;44:1154-9. Available from: https://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.294.2140&rep=rep1&type=pdf ). On the other hand, co-inoculation with Rhizobium and phosphate solubilizing bacteria stimulated dry mass accumulation, yield and grain protein content (6262. Jat RS, Ahlawat IPS. Direct and Residual Effect of Vermicompost, Biofertilizers and Phosphorus on Soil Nutrient Dynamics and Productivity of Chickpea-Fodder Maize Sequence. Journal of Sustainable Agriculture [Internet]. 2006 [cited 24/08/2021];28(1):41-54. https://doi.org/10.1300/J064v28n01_05 ).

Microorganisms based on arbuscular mycorrhizal fungi, AMF, have also been used in this crop (2727. Rahman GM, Monira S. Performance of Biofertilizers on Growth and Yield of Chickpea. 2018; Available from: http://bsmrau.edu.bd/seminar/wp- content/uploads/sites/318/2018/05/Seminar-Paper-Sirajum-Munira.pdf ,3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ,4747. Solaiman ARM, Rabbani MG, Hossain D, Hossain GMA, Alam MS. Influence of phosphorus and inoculation with Rhizobium and AM fungi on growth and dry matter yield of chickpea. Bangladesh Journal of Scientific Research [Internet]. 2012;25(1):23-32. Available from: https://www.researchgate.net/publication/325145221_Influence_of_phosphorus_and_inoculation_with_Rhizobium_and_AM_fungi_on_growth_and_dry_matter_yield_of_chickpea ), which stimulated crop productivity (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ) and improved the P, Mn, K, Cu and Fe absorption in plants (6363. Farzaneh M, Vierheilig H, Lössl A, Kaul HP. Arbuscular mycorrhiza enhances nutrient uptake in chickpea. Plant, Soil and Environment [Internet]. 2011;57(10):465-70. Available from: https://www.agriculturejournals.cz/publicFiles/133_2011-PSE.pdf ).

Inoculation of chickpea with arbuscular mycorrhizal fungi Funneliformis mosseae and Rhizophagus irregularis, increased plant biomass and yield and they were effective in improving the nutritional value of the grain by stimulating the concentration of proteins, Fe and Zn, these results being greater when an inoculum of local origin was used instead of a foreign one (3333. Pellegrino E, Bedini S. Enhancing ecosystem services in sustainable agriculture: Biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biology and Biochemistry [Internet]. 2014 [cited 24/08/2021];68:429-39. https://doi.org/10.1016/j.soilbio.2013.09.030 ).

It has been proven that inoculation with AMF and co-inoculation with AMF + Rhizobium etli increased the height, number and mass of grains per plant (6464. Borbón-Gracia A, Pérez-Márquez J, García-Camarena MG, Ramírez-Soto M. Aplicación de biofertilizantes en el cultivo de garbanzo en Sinaloa. In: Primer Simposium Internacional de Agricultura Ecológica. México: INIFAP. Memoria Científica Número 1. p. 287-291 [Internet]. yumpu.com. 2009 [cited 19/09/2021]. Available from: https://www.yumpu.com/es/document/read/13989131/primer-simposium-internacional-de-agricultura-ecologica ), while co-inoculation with Rhizobium, AMF and phosphate solubilizing bacteria significantly improved plant growth and yield indicators (4545. Pramanik K, Bera AK. Response of biofertilizers and phytohormone on growth and yield of chickpea (Cicer arietinium L.). Journal of Crop and Weed [Internet]. 2012;8(2):45-9. Available from: https://www.cropandweed.com/archives/2012/vol8issue2/10.pdf ).

The above results demonstrate the effectiveness of inoculation of chickpea seeds with both growth-promoting rhizobacteria (GPRB) and AMF or their combination to stimulate plant growth and development, which translates into increased yield and improved grain nutritional quality. On the other hand, plant tolerance to abiotic stresses is stimulated, as well as the growth of different pathogens that cause diseases in the chickpea crop is inhibited.

Algae-based products

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The use of seaweed and seaweed products has been extended to different crops (6565. Povero G, Mejia JF, Di Tommaso D, Piaggesi A, Warrior P. A Systematic Approach to Discover and Characterize Natural Plant Biostimulants. Frontiers in Plant Science [Internet]. 2016 [cited 24/08/2021];7:435. https://doi.org/10.3389/fpls.2016.00435 -6868. Renuka N, Guldhe A, Prasanna R, Singh P, Bux F. Microalgae as multi-functional options in modern agriculture: current trends, prospects and challenges. Biotechnology Advances [Internet]. 2018 [cited 24/08/2021];36(4):1255-73. https://doi.org/10.1016/j.biotechadv.2018.04.004 ) and in chickpea, its use is also reported to stimulate yield and counteract the damaging effects induced by pests, diseases and abiotic stresses (6969. Beghdady MS. Influence of foliar spray with seaweed extract on growth, yield and its quality, profile of protein pattern and anatomical structure of chickpea plant (Cicer arietinum L.). Middle East Journal of Applied Sciences [Internet]. 2016 [cited 24/08/2021];6(1):207-221. Available from: http://www.publications.zu.edu.eg/Pages/PubShow.aspx?ID=34150&&pubID=18 -7171. Ahmadpour R, Salimi A, Armand N, Hosseinzadeh SR. The effects of Ascophyllum nodosum extract on the stimulation of germination indices in chickpea (Cicer arietinum) under drought stress. Nova Biologica Reperta [Internet]. 2019 [cited 24/08/2021];6(2):206-16. https://doi.org/10.29252/nbr.6.2.206 ).

Two applications of 1 mL L^-1 of seaweed extract induced significant promoting effects on growth and yield and induced favorable changes in seed quality and protein pattern profile of chickpea. In addition, it induced favorable changes in the anatomical structure of leaves and stems, mainly due to a marked increase in the thickness of bark, phloem and xylem tissues (6969. Beghdady MS. Influence of foliar spray with seaweed extract on growth, yield and its quality, profile of protein pattern and anatomical structure of chickpea plant (Cicer arietinum L.). Middle East Journal of Applied Sciences [Internet]. 2016 [cited 24/08/2021];6(1):207-221. Available from: http://www.publications.zu.edu.eg/Pages/PubShow.aspx?ID=34150&&pubID=18 ).

Similar results show that foliar application of extracts prepared from Kappaphycus alvarezzi and Gracilaria sp. algae at 10 % significantly improved yield and its components (1313. Yadav SL, Verma A, Nepalia V. Effect of phosphorus, sulphur and seaweed sap on growth, yield and nutrient uptake of chickpea ( Cicer arietinum L.). Research on Crops [Internet]. 2016 [cited 24/08/2021];17(3):496. https://doi.org/10.5958/2348-7542.2016.00082.6 ).

On the other hand, inoculation with the cyanobacterium Anabaena laxa and co- inoculation of an Anabaena laxa-Rhizobium biofilm stimulated the leghemoglobin content of nodules, as well as nitrogen fixation, available nitrogen and soil microbial activity, which had a favorable effect on plant growth and grain yield, the best result being obtained with the Anabaena laxa inoculation (22. Bidyarani N, Prasanna R, Babu S, Hossain F, Saxena AK. Enhancement of plant growth and yields in Chickpea (Cicer arietinum L.) through novel cyanobacterial and biofilmed inoculants. Microbiological Research [Internet]. 2016 [cited 24/08/2021];188- 189:97-105. https://doi.org/10.1016/j.micres.2016.04.005 ).

When chickpea plants were treated with the microalgae Chroococcus minutus and distillery effluents, a better percentage of germination, growth and development of the plants was observed (7272. Murugesan S, Padmapriya C, Kotteswari M, Shanthi N. Effects of distillery effluent and micro alga (Chroococcus minutes) treated effluent on germination and seedling growth of Cicer arietinum L. International Journal of Applied Research [Internet]. 2017 [cited 24/08/2021];3(10):95-101. Available from: https://www.semanticscholar.org/paper/Effects-of-distillery-effluent-and-micro-alga-on-of-Murugesan-Padmapriya/41e36add67267c17ddc8c689be16583deb4cc7c9 ). It has also been observed that the use of cyanobacteria Nostoc commune and Anabaena circinalis isolated in southeastern Iraq, increased the ability of plants to fix nitrogen, which influenced crop growth and yield, helping to a 30-50 % reduction of chemical fertilizer (7373. Sanaa j B, Jawad A latif M, Al-Ani NK. Effect of Two Species of Cyanobacteria as Biofertilizers on Characteristics and Yield of Chickpea Plant. Iraqi Journal of Science [Internet]. 2014 [cited 24/08/2021];55(2Supplement). Available from: https://www.iasj.net/iasj/article/91918 ).

In chickpea tissues treated with polysaccharide preparations of Hypnea musciformis (red algae), Padina tetrastromatica (brown algae) and Ulva lactulus (green algae), induced phytoalexins were identified (6767. Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, et al. Seaweed Extracts as Biostimulants of Plant Growth and Development. Journal of Plant Growth Regulation [Internet]. 2009 [cited 24/08/2021];28(4):386-99. https://doi.org/10.1007/s00344-009-9103-x ). A biotic stress resistance inducer (k-carrageenan), obtained from Hypnea musciformis, was also found to induce phytoalexins in seed tissues (7474. Arman M. LC-ESI-MS characterisation of phytoalexins induced in chickpea and pea tissues in response to a biotic elicitor of Hypnea musciformis (red algae). Natural Product Research [Internet]. 2011 [cited 24/08/2021];25(14):1352-60. https://doi.org/10.1080/14786419.2011.553952 ). In addition, the application of a solution of this polysaccharide around the seeds at the time of sowing stimulated growth indicators, induced early flowering and produced a high content of secondary metabolites associated with disease resistance in leaves, stems and grains of plants (7575. Arman M. Carrageenan as an elicitor of induced secondary metabolites and its effects on various growth characters of chickpea... Journal of Saudi Chemical Society [Internet]. 2011;15:269-73. Available from: https://d1wqtxts1xzle7.cloudfront.net/50686815/Carrageenan_as_an_elicitor_of_induced_se20161202-16827-dpg3he-with-cover-page-v2.pdf?Expires=1632536358&Signature=fqnTjxgnvr42mW5voun6QlSp9UhqTOnGvEkDB1CaEjYY1BT6ooJp2IZkhrNX1YQiVQToT7if8pH3tt~CBuCFeKW5FEMJYF7o62VuxEBcNNyKcxmcawmTNEczMk7JtnrebfIo9NQPDHPPQ5N1R4mB2Q1W~Nx63~po7mIjkaMBtBTM2h79z21GPy~FKG68nTb8nc2ApsmxNQ-dkw-28fQ1qgvxu67Ee4JzgqXqq2Su0-txHYPTCqgEpz5JfGKaqLpWUAYD4Nadn14xruXp5rSCzpleMNBEM6~7AVNDxfZHbNWPqEwEVtooyGM5eOARf10SwJ9-nir0Z2kROlXTfmpa-Q&Key-Pair-Id=APKAJLOHF5GGSLRBV4ZA ).

Other results show that Spirulina phenolic extracts have antifungal activity against Fusarium graminearum (7676. Pagnussatt FA, Kupski L, Darley FT, Filoda PF, Ponte ÉMD, Garda-Buffon J, et al. Fusarium graminearum growth inhibition mechanism using phenolic compounds from Spirulina sp. Food Science and Technology [Internet]. 2013;33:75-80. Available from: https://www.scielo.br/j/cta/a/mkt7HrHsZDSnHgGfZy4rZPm/?lang=en&format=pdf ,7777. Pagnussatt FA, de Lima VR, Dora CL, Costa JAV, Putaux J-L, Badiale-Furlong E. Assessment of the encapsulation effect of phenolic compounds from Spirulina sp. LEB-18 on their antifusarium activities. Food Chemistry [Internet]. 2016 [cited 24/08/2021];211:616-23. https://doi.org/10.1016/j.foodchem.2016.05.098 ). On the other hand, extracts of Sargassum muticum and Jania rubens improved growth indicators in chickpea plants subjected to salt stress and stimulated the activities of superoxide dismutase and peroxidase enzymes. At the same time, four key amino acids, including serine, threonine, proline and aspartic acid, were identified in these extracts from their roots, which contribute to improve tolerance to salt stress (7878. Abdel Latef AAH, Srivastava AK, Saber H, Alwaleed EA, Tran L-SP. Sargassum muticum and Jania rubens regulate amino acid metabolism to improve growth and alleviate salinity in chickpea. Scientific Reports [Internet]. 2017 [cited 24/08/2021];7(1):10537. https://doi.org/10.1038/s41598-017-07692-w ). In addition, the use of Ascophyllum nodosum extracts has been recommended to reduce the negative effects of drought stress on chickpea seed germination (7171. Ahmadpour R, Salimi A, Armand N, Hosseinzadeh SR. The effects of Ascophyllum nodosum extract on the stimulation of germination indices in chickpea (Cicer arietinum) under drought stress. Nova Biologica Reperta [Internet]. 2019 [cited 24/08/2021];6(2):206-16. https://doi.org/10.29252/nbr.6.2.206 ).

Products formulated with algae in chickpea not only have effects on germination stimulation, growth and yield, but also help to improve crop quality and stimulate tolerance to different abiotic stresses, in addition to having antifungal properties.

Chitosan-based products

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Chitosan is a biopolymer that acts as a plant growth promoter in some crops, increases yields and protects plants against pathogens. It has a significant effect on root and stem growth and stimulates flowering and flower number. These molecules are strongly hydrophilic and attenuate the damage caused by stress in plant cells (7979. Pandey P, Verma MK, De N. Chitosan in agricultural context-A review. Bull. Environ. Pharmacol. Life Sci [Internet]. 2018;7:87-96. Available from: https://www.researchgate.net/profile/Priyal-Pandey/publication/326682315_Chitosan_in_agricultural_context_-_A_review/links/5b72ddc792851ca6505d7c61/Chitosan-in-agricultural-context-A-review.pdf ). For these reasons it has been used by farmers as a biopesticide and biofertilizer since the 80's of the last century and for this it has been applied as a soil amendment, by foliar spraying, to fruits and seeds, both alone and in combination with other treatments to prevent the development of diseases in plants or to accelerate their innate defenses against pathogens (8080. Malerba M, Cerana R. Recent Applications of Chitin- and Chitosan-Based Polymers in Plants. Polymers [Internet]. 2019 [cited 24/08/2021];11(5):839. https://doi.org/10.3390/polym11050839 -8383. Jabnoun-Khiareddine H, El-Mohamedy RSR, Abdel-Kareem F, Abdallah RAB, Gueddes-Chahed M, Daami-Remadi M. Variation in chitosan and salicylic acid efficacy towards soil-borne and air-borne fungi and their suppressive effect of tomato wilt severity. J Plant Pathol Microbiol. 2015;6(325):2.).

In chickpea cultivation, it has been shown that, during germination, seeds treated with chitosan excreted several proteins, which have an in vitro inhibitory effect on the growth of the fungus Fusarium oxysporum f. sp. Ciceris, these exudates protect seeds from soil pathogens during germination (8484. Anusuya S, Sathiyabama M. Identification of defence proteins from the seed exudates of Cicer arietinum L. and its effect on the growth of Fusarium oxysporum f.sp. ciceri. Archives of Phytopathology and Plant Protection [Internet]. 2014 [cited 24/08/2021];47(13):1611-20. https://doi.org/10.1080/03235408.2013.853457 ). More recently, 325 proteins and 65 metabolites associated with the chitosan-stimulated immune response to Fusarium were identified in this crop, which are related to the production of active oxygen species, stomatal movement, nodule development, and root architecture (8585. Narula K, Elagamey E, Abdellatef MAE, Sinha A, Ghosh S, Chakraborty N, et al. Chitosan-triggered immunity to Fusarium in chickpea is associated with changes in the plant extracellular matrix architecture, stomatal closure and remodeling of the plant metabolome and proteome. The Plant Journal [Internet]. 2020 [cited 24/08/2021];103(2):561-83. https://doi.org/10.1111/tpj.14750 ).

In recent years, chitosan nanoparticles can act as growth stimulators and as antimicrobial agents against pathogenic fungi and bacteria in agriculture. In addition, they can act as nanoconductors for other existing agrochemicals (8686. Maluin FN, Hussein MZ. Chitosan-Based Agronanochemicals as a Sustainable Alternative in Crop Protection. Molecules [Internet]. 2020 [cited 24/08/2021];25(7):1611. https://doi.org/10.3390/molecules25071611 ). Thus, it has been demonstrated that chitosan and chitosan-metal nanocomposites showed good antifungal activity against Fusarium oxysporum f. sp. ciceris in chickpea crop and also stimulated plant growth compared to control plants. Chitosan-CuO and chitosan-ZnO nanocomposites were highlighted in reducing the disease caused by the pathogen (8787. Kaur P, Duhan JS, Thakur R. Comparative pot studies of chitosan and chitosan- metal nanocomposites as nano-agrochemicals against fusarium wilt of chickpea (Cicer arietinum L.). Biocatalysis and Agricultural Biotechnology [Internet]. 2018 [cited 24/08/2021];14:466-71. https://doi.org/10.1016/j.bcab.2018.04.014 ).

Also, chitosan-Ag nanoparticles showed a substantial growth-promoting effect, given by a stimulation in seed germination, length and fresh and dry mass of plants. An increase in chlorophyll content and in the activities of ascorbate peroxidase, catalase and peroxidase enzymes was found, which opens the possibility of using these nanoparticles as growth stimulators in chickpea cultivation (8888. Anusuya S, Banu KN. Silver-chitosan nanoparticles induced biochemical variations of chickpea (Cicer arietinum L.). Biocatalysis and Agricultural Biotechnology [Internet]. 2016 [cited 24/08/2021];8:39-44. https://doi.org/10.1016/j.bcab.2016.08.005 ). A positive effect on germination, growth and induction of defensive enzymes in chickpea plants was also found when thiamine- loaded chitosan nanoparticles were used (8989. Muthukrishnan S, Murugan I, Selvaraj M. Chitosan nanoparticles loaded with thiamine stimulate growth and enhances protection against wilt disease in Chickpea. Carbohydrate Polymers [Internet]. 2019 [cited 24/08/2021];212:169-77. https://doi.org/10.1016/j.carbpol.2019.02.037 ).

All these results reveal the potential of chitosan-based products to be used as growth and yield stimulators and as bioprotectors against the attack of certain pathogens in chickpea crops.

Other biostimulants

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Several results have shown that the application of certain doses of humic acids to the soil at sowing and pre-flowering stimulated growth and grain yield (9090. Kahraman A. Effect of humic acid applications on the yield components in chickpea. Journal of Agricultural Faculty of Gaziosmanpasa University [Internet]. 2017;34(1):218-22. Available from: https://www.researchgate.net/profile/Ali- Kahraman-8/publication/316446044_Humik_Asit_Uygulamalarinin_Nohutta_Verim_Bilesenleri_Uzerine_Etkileri/links/59cac8e2aca272bb0507977f/Humik-Asit-Uygulamalarinin- Nohutta-Verim_Bilesenleri-Uezerine-Etkileri.pdf ), as well as protein yield of chickpea plants of the 'Çağatay' variety in Turkey (9191. Kahraman A. Managing the Humic Acid Fertilizing of Chickpea and Protein Status. Selcuk Journal of Agriculture and Food Sciences [Internet]. 2020 [cited 24/08/2021];34(1):107-10. https://doi.org/10.15316/SJAFS.2020.202 ). Similar results were subsequently reported for yield stimulation and yield components in plants subjected to different irrigation regimes (9292. Abhari A, Gholinezhad E. Effect of humic acid on grain yield and yield components in chickpea under different irrigation levels. Journal of Plant Physiology and Breeding [Internet]. 2019 [cited 24/08/2021];9(2):19-29. https://doi.org/10.22034/jppb.2019.10441 ).

Foliar spraying of humic acids and naphthaleneacetic acid (NAA) stimulated plant growth by increasing indicators such as height, number of branches, leaf area, total dry mass, as well as yield components such as number of pods per plant, 100-seed mass and seed yield per hectare (9393. Kapase PV, Deotale RD, Sawant PP, Sahane AN, Banginwar AD. Effect of foliar sprays of humic acid through vermicompost wash and NAA on morpho-physiological parameters, yield and yield contributing parameters of chickpea. Journal of Soils and Crops [Internet]. 2014;24(1):107-14. Available from: https://www.ascrsnagpur.com/DemoPaper/botony.pdf ).

On the other hand, the efficacy of humic acids in reducing the severity of wilt of chickpea plants cv. Giza 3, caused by the fungus Fusarium oxysporum f. sp. ciceris, has also been reported (9494. Abdel-Monaim MF, Morsy M K, Zyan AH. Efficacy of some organic compounds in controlling Fusarium wilt disease, growth and yield parameters in Chickpea plants. Egyptian Journal of Agricultural Research [Internet]. 2018;96(2):351-64. Available from: https://ejar.journals.ekb.eg/article_132936_c86bccaf9568ec257c34ed7acb3a5d55.pdf ).

In Cuba, Fitomas-E use, at a rate of 0.5 L ha^-1 on chickpea plants variety N-27, increased the number of pods and grains per plant, the mass of 100 grains and yield, under normal conditions and under drought stress (2323. Meriño-Hernández Y, Rodríguez-Hernández P, Cartaya-Rubio O, Dell’Amico- Rodríguez JM, Boicet-Fabré T, Shagarodsky-Scull T, et al. Acumulación de iones y tolerancia a la salinidad en diferentes cultivares cubanos de garbanzo (Cicer arietinum L.). Cultivos Tropicales [Internet]. 2018 [cited 24/08/2021];39(4):42-50. Available from: http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S0258-59362018000400006&lng=es&nrm=iso&tlng=pt ).

Treatment of chickpea seeds subjected to mild osmotic stress with ellagic acid (50 ppm), isolated and purified from Padina boryana Thivy, accelerated germination and seedling growth; it also stimulated total antioxidant capacity by increasing some antioxidant metabolites and enzymes (9595. El-Soud WA, Hegab MM, AbdElgawad H, Zinta G, Asard H. Ability of ellagic acid to alleviate osmotic stress on chickpea seedlings. Plant Physiology and Biochemistry [Internet]. 2013 [cited 24/08/2021];71:173-83. https://doi.org/10.1016/j.plaphy.2013.07.007 ).