El suelo vivo: un poco de lo que ocurre en este entorno. Un énfasis en los fitopatógenos

INTRODUCCIÓN

⌅

Alimentar a la población mundial es un tema prioritario, por ello la Agenda 2030 para el Desarrollo Sostenible de Naciones Unidas incluye dentro de sus 17 Objetivos de Desarrollo Sostenible, el objetivo hambre cero (11. ONU. Objetivos del Desarrollo Sostenible de la Agenda 2030 ONU. 2021 [citado 20/07/2021]. Disponible en: https://www.un.org/sustainabledevelopment/). Lograr esto es un desafío, ya que las plantas están expuestas a muchas condiciones del suelo que podrían afectar el crecimiento y la producción. Por ejemplo, las plagas y enfermedades son de los mayores desafíos que enfrentan los productores de cultivos cada año. Además, las enfermedades emergentes constituyen uno de los mayores riesgos por la devastación que provocan en la producción agrícola (22. Avila-Quezada G, Silva-Rojas HV, Sánchez-Chávez E, Leyva-Mir G, Martínez-Bolaños L, Guerrero-Prieto V, et al. Seguridad alimentaria: la continua lucha contra las enfermedades de los cultivos. Tecnociencia Chihuahua. 2016;10(3):133-142.-55. Avila-Quezada GD, Esquivel JF, Silva-Rojas HV, Leyva-Mir G, García-Avila C, Noriega-Orozco L, et al. Emerging plant diseases under a changing climate scenario: Threats to our global food supply. Emirates Journal of Food and Agriculture. 2018;30(6):443-450.).

Es conocido que la aplicación excesiva de agroquímicos tiene un efecto inmediato sobre lo que se desea lograr durante la producción agrícola (66. Sánchez-Chávez E, Silva-Rojas HV, Leyva-Mir G, Villareal-Guerrero F, Jiménez-Castro J, Molina-Gayoso E, et al. An effective strategy to reduce the incidence of Phytophthora root and crown rot in bell pepper. Interciencia. 2017;42(4):229-235.); sin embargo, esto se logra con consecuencias ambientales y daños a la salud de los trabajadores agrícolas y de los consumidores. Tecnologías sostenibles deben utilizarse para producir los alimentos que demanda la población, sin afectar los recursos naturales.

El suelo, por albergar una gran biodiversidad, se considera la base para la producción de alimentos saludables. La diversidad microbiana tiene varias funciones, una de las cuales es la solubilidad de los minerales, haciéndolos disponibles para las plantas. Por ejemplo, las bacterias solubilizadoras de fosfato contribuyen hasta el 50% de la solubilización del elemento (77. Galvez ZYA, Burbano VEM. Solubilización de fosfatos: una función microbiana importante en el desarrollo vegetal. NOVA Publicación en Ciencias Biomédicas. 2015;12(21):67-79.). Algunos organismos, como los hongos micorrízicos, llevan los elementos a las raíces a través de sus hifas (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.), incluso las endomicorrizas los depositan en el espacio interarbuscular (dentro de la planta).

Esta actividad microbiana promueve un suelo fértil y el equilibro de organismos y microorganismos. Un ejemplo es la lombriz de tierra, la cual mejora la estructura del suelo al tiempo que reduce las poblaciones de fitopatógenos (Figura 1). También, el hongo Trichoderma tiene un amplio espectro de acción que le permite reducir una gran cantidad de patógenos de plantas.

Figura 1. Lombrices de tierra y otros microorganismos miembros del ecosistema del suelo en equilibrio, cada uno con una tarea específica

DESARROLLO

⌅

Organismos del suelo

⌅

Las lombrices de tierra, por su capacidad para cavar galerías y producir perfiles demográficos y relaciones con la microflora del suelo, son un componente clave en el ciclo de nutrientes en los suelos. Su actividad física y los efectos químicos resultantes promueven ciclos cortos y rápidos de nutrientes y carbohidratos asimilables (99. Le Bayon RC, Bullinger-Weber G, Schomburg A, Turberg P, Schlaepfer R, Guenat C. (2017). Earthworms as ecosystem engineers: A review. Earthworms: Types, Roles and Research. NOVA Science Publishers, New York, 129-178.).

Por otra parte, en la agricultura la adición de vermicomposta es una práctica común. La vermicomposta tiene un papel fundamental para promover la vida en el suelo, mejorando la textura y promoviendo niveles satisfactorios de macro y micronutrientes (1010. Sánchez-Rosales R, Hernández-Rodríguez A, Ojeda-Barrios D, Robles-Hernández L, González-Franco A, Parra-Quezada R. Comparison of three systems of decomposition of agricultural residues for the production of organic fertilizers. Chilean Journal of Agricultural Research. 2017;77(3):287-292.). Contiene muchos compuestos ricos en microorganismos beneficiosos y hormonas de crecimiento que funcionan como agentes biofertilizantes y de control biológico contra plagas y patógenos de las plantas (1111. Sulaiman ISC, Mohamad A. The use of vermiwash and vermicompost extract in plant disease and pest control. In: Natural Remedies for Pest, Disease and Weed Control. Academic Press; 2020. p. 187-201.).

Además, durante el vermicompostaje, la lombriz roja de California (Eisenia foetida) ingiere materia orgánica que progresivamente se descompone y fragmenta. Esta materia está formada por microorganismos que incluyen una gran cantidad de hongos. Las sustancias mucosas producidas por las lombrices de tierra tienen una fuerte actividad antimicrobiana y antifúngica (1212. Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pakistan Journal of Pharmaceutical Sciences. 2016;29(3):969-977.). A través de sus secreciones cutáneas y proteína antimicrobiana, controlan los microorganismos (1313. Prakash M, Gunasekaran G. Antibacterial activity of the indigenous earthworms Lampito mauritii (Kinberg) and Perionyx excavatus (Perrier). The Journal of Alternative and Complementary Medicine. 2011;17:167-170.), reduciendo así las poblaciones de fitopatógenos del suelo.

La superficie de la cutícula de la lombriz de tierra contiene péptidos antimicrobianos que la protegen del ambiente. Descarga péptidos como la lisozima a través de su cutícula, lo que produce una actividad antimicrobiana. Además, se ha demostrado que la pared corporal y la secreción intestinal reducen las poblaciones de Fusarium oxysporum (1212. Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pakistan Journal of Pharmaceutical Sciences. 2016;29(3):969-977.).

Las lombrices de tierra se alimentan de suelos que contienen materiales orgánicos, microorganismos vivos e insectos. Una vez ingerido el alimento, se modifica en el cuerpo de la lombriz de tierra para facilitar su absorción. Al entrar por la boca, el material es tragado por la faringe que es una bomba de fuerza (Figura 2). Después de eso, los músculos se contraen y mueven la comida hacia el esófago. Luego, ésta va al buche (que se contrae más que la molleja) donde se almacena y se mueve hacia la molleja. Este es un músculo fuerte que tritura el material en partes muy pequeñas, donde la secreción de enzimas participa en la descomposición de los productos. El material finamente triturado pasa por el proceso de digestión en el intestino. Aquí se agregan más enzimas para promover la descomposición en moléculas simples (1414. Jouni F. Synergistic interaction earthworm-microbiota: a role in the tolerance and detoxification of pesticides?. Agricultural sciences. Université d’Avignon. 2018. English. ffNNT: 2018AVIG0699ff. [citado 20/07/2021]. Disponible en: https://tel.archives-ouvertes.fr/tel-02074579/document). Las enzimas que participan son la proteasa, lipasa, amilasa, liquenasa, celulasa y quitinasa (1515. Edwards CA, Fletcher KE. Interactions between earthworms and microorganisms in organic-matter breakdown. Agriculture, Ecosystems & Environment. 1988;24(1-3):235-247.). Este proceso consigue parcialmente la eliminación de fitopatógenos.

Figura 2. Órganos del cuerpo de la lombriz de tierra, donde ocurre la descomposición de la materia orgánica ingerida, por actividad enzimática

Lombrices de tierra como Eisenia foetida controlan nematodos como Pratylechus sp en tomate (1616. Nath G, Singh K. Combination of vermicomposts and biopesticides against nematode (Pratylenchus sp.) and their effect on growth and yield of tomato (Lycopersicon esculentum). IIOAB Journal. 2011;2:27-35.), Meloidogyne javanica en pepino (1717. Rostami M, Olia M, Arabi M. Evaluation of the effects of earthworm Eisenia fetida-based products on the pathogenicity of root-knot nematode (Meloidogyne javanica) infecting cucumber. International Journal of Recycling of Organic Waste in Agriculture. 2014;3(2):58.) y Meloidogyne hapla en tomate (1818. Edwards CA, Arancon NQ, Emerson E, Pulliam R. Suppressing plant parasitic nematodes and arthropod pests with vermicompost teas. Biocycle. 2007;48(12):38-39.).

Otros investigadores encontraron que la lombriz de tierra, Lumbricus terrestres, se alimentaba de esclerocios de Sclerotinia sclerotiorum cuando estaban hidratados (1919. Euteneuer P, Wagentristl H, Steinkellner S, Scheibreithner C, Zaller JG. Earthworms affect decomposition of soil-borne plant pathogen Sclerotinia sclerotiorum in a cover crop field experiment. Applied Soil Ecology. 2019;138:88-93.). L. terrestris consumió en promedio el 61% de los esclerocios que se hidrataron durante 13 semanas. Además, el humus de lombriz y los hongos micorrízicos arbsculares mejoran la calidad de los frutos (2020. Charles NJ, Martín Alonso NJ. Uso y manejo de hongos micorrízicos arbusculares (HMA) y humus de lombriz en tomate (Solanum lycopersicum L.), bajo sistema protegido. Cultivos Tropicales. 2015;36(1):55-64.).

Microorganismos, interacciones y microambientes del suelo

⌅

La estructura biológica del suelo está formada por una gran cantidad de bacterias, actinomicetos y hongos (2121. González-Escobedo R, Muñoz-Castellanos LN, Muñoz-Ramirez ZY, Guigón López C, Avila-Quezada GD. Microbial community analysis of rhizosphere of healthy and wilted pepper (Capsicum annuum L.) in an organic farming system. Microbial Ecology. 2021; Por asignar). Todos ellos están asociados a materia orgánica y materiales microbianos poliméricos como enzimas y polisacáridos extracelulares que ellos mismos producen. Los microorganismos se encuentran en tejidos densos de arcilla o materia orgánica humificada, en depósitos de mucigel, en microporos o en raíces de plantas ricas en carbohidratos. En estos sitios, los microorganismos sobreviven temporalmente a condiciones adversas.

En esta revisión abordamos dos tipos de microorganismos que benefician a las plantas y que, generalmente, se encuentran de forma natural en suelos en simbiosis con plantas, y que pueden usarse para enriquecer suelos, como los hongos micorrízicos y Trichoderma spp.

Una vez que los micros y macroelementos son solubilizados por las bacterias, se transfieren a través de la hifa del hongo micorrízico a la raíz, previamente colonizada por las micorrizas. Las enzimas transportadoras de fosfato del hongo y de la planta están involucradas en este proceso (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.).

Los hongos micorrízicos confieren protección a las plantas contra los fitopatógenos (2222. Zhang H, Franken P. Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza. 2014;24:419-430., 2323. Song Y, Chen D, Lu K, Sun Z, Zeng R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science. 2015;6:786.). En la rizosfera, los microorganismos compiten por el espacio y los nutrientes. Además, las micorrizas también estimulan los mecanismos de defensa bioquímicos de las plantas (2222. Zhang H, Franken P. Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza. 2014;24:419-430.).

Las interacciones entre las micorrizas y las plantas se autorregulan, de hecho, cuando los nutrientes minerales están disponibles en el suelo, la colonización de las micorrizas se reduce (2424. Azcón R, Ambrosano E, Charest C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Science. 2003;165(5):1137-1145.).

Aparentemente, todas las poblaciones microbianas del suelo se autorregulan, incluso la planta regula a los microorganismos en su rizosfera. Así, al añadir microorganismos al suelo, pueden estar activos durante meses o un año y desaparecer pasado ese tiempo. Algunos autores encontraron que al incorporar el hongo ectomicorrízico Pisolithus tinctorius, protegía a las plántulas de Pinus sylvestris del ataque de Fusarium moniliforme y Rhizoctonia solani; esta protección duró un año (2525. Chakravarty P, Unestam T. Differential influence of ectomycorrhizae on plant growth and disease resistance in Pinus sylvestris seedlings. Journal of Phytopathology. 1987;120(2):104-120.).

Es muy interesante conocer la simbiosis en profundidad. La interacción comienza a través de señales y, dependiendo de los requerimientos de la planta y otros factores aún desconocidos, los microorganismos del suelo se regulan.

Los hongos endomicorrízicos también protegen las raíces contra los patógenos. Por ejemplo, una mezcla de hongos micorrízicos arbusculares (HMA) compuesta por Glomus aggregatum, Gigaspora margarita y Glomus intraradices suprimió la pudrición de la raíz por Fusarium solani en Phaseolus vulgaris, en condiciones de invernadero (2626. Eke P, Adamou S, Fokom R, Nya VD, Fokou PVT, Wakam LN, et al. Arbuscular mycorrhizal fungi alter antifungal potential of lemongrass essential oil against Fusarium solani, causing root rot in common bean (Phaseolus vulgaris L.). Heliyon. 2020;6(12):e05737.).

Incluso, los hongos endomicorrízicos pueden controlar nematodos como Meloidogyne incognita (2727. da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection. 2020;135:105203.) y Meloidogyne javanica (2828. Sharma M, Saini I, Kaushik P, Al Dawsari MM, Al Balawi T, Alam P. Mycorrhizal fungi and Pseudomonas fluorescens application reduces root-knot nematode (Meloidogyne javanica) infestation in eggplant. Saudi Journal of Biological Sciences. 2021;28(7): 3685-3691.).

La reducción en la penetración de M. incognita en plantas endomicorrizadas puede deberse al hecho de que los HMA inducen cambios en la planta y, en respuesta, las raíces producen exudados, lo que sugiere que los exudados afectan la motilidad de los nematodos en el suelo. Otras posibilidades son la producción de compuestos nematicidas, aumento de la lignificación de las raíces, cambios en la composición de la pared celular y activación de los mecanismos de defensa de las plantas.

Se ha demostrado la acumulación de compuestos fenólicos, como fitoalexinas y flavonoides e isoflavonoides en raíces micorrízicas en presencia del nematodo. Los HMA también pueden aumentar la actividad de las enzimas de defensa como la peroxidasa, polifenoloxidasa, superóxido dismutasa, quitinasa y β 1,3 glucanasa (2727. da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection. 2020;135:105203.). En general, los HMA presentes de forma natural en el suelo pueden ser benéficos para la agricultura sostenible, ya que mantienen la producción al reducir a los patógenos.

Por otra parte, Trichoderma es un hongo benéfico que ha demostrado eficacia en el control de patógenos de las raíces (2929. Stummer BE, Zhang Q, Zhang X, Warren RA, Harvey PR. Quantification of Trichoderma afroharzianum, Trichoderma harzianum and Trichoderma gamsii inoculants in soil, the wheat rhizosphere and in planta suppression of the crown rot pathogen Fusarium pseudograminearum. Journal of Applied Microbiology. 2020;129(4):971-990.), incluidos los nematodos (3030. TariqJaveed M, Farooq T, Al-Hazmi AS, Hussain MD, Rehman AU. Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. Journal of Invertebrate Pathology. 2021;107626.), debido a su capacidad para secretar compuestos volátiles y no volátiles, y metabolitos secundarios. Su mecanismo directo incluye competencia, micoparasitismo, antibiosis e inducción de mecanismos de resistencia de las plantas, así también mecanismos indirectos, como la inactivación de las enzimas producidas por el patógeno (3131. Pozo-Serrano J, Cruz ERDL, Teresa-Cardoso M, Rodríguez-Pérez A, García-Pupo J, Pérez-Tejeda Y, et al. Efectividad antagónica In vitro de Trichoderma sp., frente a Stemphylium lycopersici. Cultivos Tropicales. 2019;40(3).-3333. Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R. Trichoderma secondary metabolites active on plants and fungal pathogens. The Open Mycology Journal. 2014;8(1):127-139.).

Entre los metabolitos secundarios se encuentran los terpenos, pironas, gliotoxinas, gliovirinas y peptaibols (3434. Vinale F, Ghisalberti EL, Sivasithamparam K, Marral R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology. 2009;48(6):705-711.). Los metabolitos antifúngicos producidos por Trichoderma son epipolythiodioxopiperazines, peptaibols, pironas, butenólidos, piridonas, azafilonas, koningininas, esteroides, antraquinonas, lactonas, tricotecenos y otros (3535. Khan RAA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms. 2020;8(6), 817., 3636. Sonkar P, Chandra R, Singh R, Kumar S. Study on management of Fusarium oxysporum through different mode of action of Trichoderma spp. International Journal of Current Trends Science and Technology. 2018;8:20192-20200.).

La expresión de genes relacionados con metabolitos secundarios en Trichoderma spp. depende de factores como la señalización del pH, las proteínas del complejo de terciopelo y las señales de comunicación con otros microorganismos (3737. Macheleidt J, Mattern DJ, Fischer J, Netzker T, Weber J, Schroeckh V, et al. Regulation and role of fungal secondary metabolites. Annual Review of Genetics. 2016;50:371-392.).

Estos metabolitos exhiben bioactividad contra fitopatógenos como Macrophomina phaseolina, Pythium spp., Sclerotium rolfsii, Rhizoctonia solani, Fusarium oxysporum, Verticillium dahliae, Botrytis cinerea, Ascochyta citrullina, Phytophthora parasitica, P. cinnamomi, Leptosphaeria maculans, Clavibacter spp., Gaeumannomyces graminis, Colletotrichum gloeosporioides, y otros (3434. Vinale F, Ghisalberti EL, Sivasithamparam K, Marral R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology. 2009;48(6):705-711., 3535. Khan RAA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms. 2020;8(6), 817., 3838. Shyamli S, Prem D, Rs T, Atar S. Production and antifungal activity of secondary metabolites of Trichoderma virens. Pesticide Research Journal. 2005;17(2):26-29.-4040. Sha S, Liu L, Pan S, Wang WM. Isolation and purification of antifungal components from Trichoderma harzianum ferment broth by high-speed counter-current chromatography. Chinese Journal of Biological Control. 2013;29(1):83-88.).

Plantas, microorganismos y carbono

⌅

Las plantas toman dióxido de carbono de la atmósfera y exudan algo de carbono en forma de sustancia azucarada a través de sus raíces. Esta secreción alimenta a los microorganismos del suelo. Cuando las plantas mueren, los microorganismos descomponen el carbono y lo utilizan para su metabolismo. Esta descomposición microbiana libera dióxido de carbono, por lo que el suelo almacena más carbono cuando está lleno de vida microbiana (4141. Marler TE, Krishnapillai MV. Vertical strata and stem carbon dioxide efflux in Cycas trees. Plants. 2020;9(2):230., 4242. Chikov VI, Akhtyamova GA, Khamidullina LA. Ecological significance of the interaction of photosynthesis light and dark processes. American Journal of Plant Sciences. 2021;12(04):624.).

Los hongos micorrízicos producen sustancias mucilaginosas (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.) como la glomalina. Esta es una glicoproteína recalcitrante muy estable, con una vida media de hasta 42 años, y constituye el componente más grande de la materia orgánica del suelo (4343. Ferrero Holtz EW, Gonzalez MG, Giuffré L, Ciarlo E. Glomalins and their relationship with soil carbon. International Journal of Applied Science and Technology. 2016;6(2):69-73.), también, promueve la agregación del suelo. Los hongos micorrízicos transfieren más carbono al suelo que otros microorganismos (4444. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytologist. 2015;205(4):1537-1551.) (Figura 3).

Figura 3. Esquema del dioxido de carbono (CO₂) desde que ingresa al dosel del árbol hasta su filtración en el suelo, y la actividad de los microorganismos

Parte del carbono permanece en el suelo, desde días hasta algunos años. Los microorganismos pueden digerir este carbono, emitiendo así dióxido de carbono. Así es como el carbono puede permanecer durante años o décadas en un sitio (4545. Kittredge J. Soil Carbon Restoration: Can Biology do the Job?. NE Organic farming association, Massachusetts Chapter, 16. 2015. [citado 20/07/2021]. Disponible en: https://www.unifiedfieldcorporation.com/wp-content/uploads/2015/11/2015_White_Paper_web.pdf). Una actividad agrícola importante es la aplicación de composta al suelo. La composta alberga microorganismos y puede retener carbono durante siglos. La labranza mínima hace que el carbono del suelo no esté expuesto al oxígeno y los agregados del suelo permanezcan intactos, protegiendo su carbono (4545. Kittredge J. Soil Carbon Restoration: Can Biology do the Job?. NE Organic farming association, Massachusetts Chapter, 16. 2015. [citado 20/07/2021]. Disponible en: https://www.unifiedfieldcorporation.com/wp-content/uploads/2015/11/2015_White_Paper_web.pdf-4747. Tarango-Rivero SH, Ávila-Quezada GD, Jacobo-Cuellar JL, Ramírez-Valdespino CA, Orrantia-Borunda E, Rodríguez-Heredia R, Olivas-Tarango AL. Chelated zinc and beneficial microorganisms: A sustainable fertilization option for pecan production. Revista Chapingo. Serie horticultura, 2022;28(3):145-159.).

El secuestro de carbono del suelo es una forma natural de eliminar el dióxido de carbono de la atmósfera, y esto se puede lograr con prácticas agrícolas sostenibles. Estas prácticas mejorarán la capacidad de los suelos para almacenar carbono y ayudarán a minimizar los efectos del calentamiento global.

CONCLUSIONES

⌅

Esta revisión presenta cómo las plantas extraen CO₂ del aire, sintetizan carbohidratos, que exudan de las raíces, para alimentar, atraer o repeler microorganismos. Adicionalmente, se destaca la importante actividad de los organismos y microorganismos del suelo para el beneficio de las plantas, con énfasis en lombrices de tierra, hongos micorrízicos y Trichoderma, debido a que pueden reducir las poblaciones de patógenos vegetales. Todos ellos, dentro de su especialidad, logran mediante la competencia por el espacio, o con mecanismos físicos y químicos, reducir los fitopatógenos del suelo.
Las lombrices de tierra, los hongos micorrízicos y Trichoderma presentes de forma natural en el suelo, pueden ser muy benéficos para la agricultura sostenible, manteniendo la producción y el equilibrio biológico en los suelos. Concluimos que el manejo integrado de cultivos promueve la competencia y el equilibrio, esenciales para mantener la salud del suelo y asegurar la producción de alimentos. Finalmente, el conocimiento de la diversidad de la biota edáfica en los agroecosistemas permite la implementación de estrategias de uso del suelo.

AGRADECIMIENTOS

⌅

Los autores agradecen a los Programas de Postgrado del Consejo Nacional de Ciencia y Tecnología (Conacyt), de la Facultad de Ciencias Agrotecnológicas de la Universidad Autónoma de Chihuahua, México.

BIBLIOGRAFÍA

⌅

1. ONU. Objetivos del Desarrollo Sostenible de la Agenda 2030 ONU. 2021 [citado 20/07/2021]. Disponible en: https://www.un.org/sustainabledevelopment/

2. Avila-Quezada G, Silva-Rojas HV, Sánchez-Chávez E, Leyva-Mir G, Martínez-Bolaños L, Guerrero-Prieto V, et al. Seguridad alimentaria: la continua lucha contra las enfermedades de los cultivos. Tecnociencia Chihuahua. 2016;10(3):133-142.

3. Cintora-Martínez EA, Leyva-Mir SG, Ayala-Escobar V, Avila-Quezada G, Camacho-Tapia M, Tovar-Pedraza JM. Pomegranate fruit rot caused by Pilidiella granati in Mexico. Australasian Plant Disease Notes. 2017;12(1):4.

4. García-González T, Sáenz-Hidalgo HK, Silva-Rojas HV, Morales-Nieto C, Vancheva T, Koebnik R, et al. Enterobacter cloacae, an emerging plant-pathogenic bacterium affecting chili pepper seedlings. The Plant Pathology Journal. 2018;34(1):1-10.

5. Avila-Quezada GD, Esquivel JF, Silva-Rojas HV, Leyva-Mir G, García-Avila C, Noriega-Orozco L, et al. Emerging plant diseases under a changing climate scenario: Threats to our global food supply. Emirates Journal of Food and Agriculture. 2018;30(6):443-450.

6. Sánchez-Chávez E, Silva-Rojas HV, Leyva-Mir G, Villareal-Guerrero F, Jiménez-Castro J, Molina-Gayoso E, et al. An effective strategy to reduce the incidence of Phytophthora root and crown rot in bell pepper. Interciencia. 2017;42(4):229-235.

7. Galvez ZYA, Burbano VEM. Solubilización de fosfatos: una función microbiana importante en el desarrollo vegetal. NOVA Publicación en Ciencias Biomédicas. 2015;12(21):67-79.

8. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.

9. Le Bayon RC, Bullinger-Weber G, Schomburg A, Turberg P, Schlaepfer R, Guenat C. (2017). Earthworms as ecosystem engineers: A review. Earthworms: Types, Roles and Research. NOVA Science Publishers, New York, 129-178.

10. Sánchez-Rosales R, Hernández-Rodríguez A, Ojeda-Barrios D, Robles-Hernández L, González-Franco A, Parra-Quezada R. Comparison of three systems of decomposition of agricultural residues for the production of organic fertilizers. Chilean Journal of Agricultural Research. 2017;77(3):287-292.

11. Sulaiman ISC, Mohamad A. The use of vermiwash and vermicompost extract in plant disease and pest control. In: Natural Remedies for Pest, Disease and Weed Control. Academic Press; 2020. p. 187-201.

12. Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pakistan Journal of Pharmaceutical Sciences. 2016;29(3):969-977.

13. Prakash M, Gunasekaran G. Antibacterial activity of the indigenous earthworms Lampito mauritii (Kinberg) and Perionyx excavatus (Perrier). The Journal of Alternative and Complementary Medicine. 2011;17:167-170.

14. Jouni F. Synergistic interaction earthworm-microbiota: a role in the tolerance and detoxification of pesticides?. Agricultural sciences. Université d’Avignon. 2018. English. ffNNT: 2018AVIG0699ff. [citado 20/07/2021]. Disponible en: https://tel.archives-ouvertes.fr/tel-02074579/document

15. Edwards CA, Fletcher KE. Interactions between earthworms and microorganisms in organic-matter breakdown. Agriculture, Ecosystems & Environment. 1988;24(1-3):235-247.

16. Nath G, Singh K. Combination of vermicomposts and biopesticides against nematode (Pratylenchus sp.) and their effect on growth and yield of tomato (Lycopersicon esculentum). IIOAB Journal. 2011;2:27-35.

17. Rostami M, Olia M, Arabi M. Evaluation of the effects of earthworm Eisenia fetida-based products on the pathogenicity of root-knot nematode (Meloidogyne javanica) infecting cucumber. International Journal of Recycling of Organic Waste in Agriculture. 2014;3(2):58.

18. Edwards CA, Arancon NQ, Emerson E, Pulliam R. Suppressing plant parasitic nematodes and arthropod pests with vermicompost teas. Biocycle. 2007;48(12):38-39.

19. Euteneuer P, Wagentristl H, Steinkellner S, Scheibreithner C, Zaller JG. Earthworms affect decomposition of soil-borne plant pathogen Sclerotinia sclerotiorum in a cover crop field experiment. Applied Soil Ecology. 2019;138:88-93.

20. Charles NJ, Martín Alonso NJ. Uso y manejo de hongos micorrízicos arbusculares (HMA) y humus de lombriz en tomate (Solanum lycopersicum L.), bajo sistema protegido. Cultivos Tropicales. 2015;36(1):55-64.

21. González-Escobedo R, Muñoz-Castellanos LN, Muñoz-Ramirez ZY, Guigón López C, Avila-Quezada GD. Microbial community analysis of rhizosphere of healthy and wilted pepper (Capsicum annuum L.) in an organic farming system. Microbial Ecology. 2021; Por asignar

22. Zhang H, Franken P. Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza. 2014;24:419-430.

23. Song Y, Chen D, Lu K, Sun Z, Zeng R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science. 2015;6:786.

24. Azcón R, Ambrosano E, Charest C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Science. 2003;165(5):1137-1145.

25. Chakravarty P, Unestam T. Differential influence of ectomycorrhizae on plant growth and disease resistance in Pinus sylvestris seedlings. Journal of Phytopathology. 1987;120(2):104-120.

26. Eke P, Adamou S, Fokom R, Nya VD, Fokou PVT, Wakam LN, et al. Arbuscular mycorrhizal fungi alter antifungal potential of lemongrass essential oil against Fusarium solani, causing root rot in common bean (Phaseolus vulgaris L.). Heliyon. 2020;6(12):e05737.

27. da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection. 2020;135:105203.

28. Sharma M, Saini I, Kaushik P, Al Dawsari MM, Al Balawi T, Alam P. Mycorrhizal fungi and Pseudomonas fluorescens application reduces root-knot nematode (Meloidogyne javanica) infestation in eggplant. Saudi Journal of Biological Sciences. 2021;28(7): 3685-3691.

29. Stummer BE, Zhang Q, Zhang X, Warren RA, Harvey PR. Quantification of Trichoderma afroharzianum, Trichoderma harzianum and Trichoderma gamsii inoculants in soil, the wheat rhizosphere and in planta suppression of the crown rot pathogen Fusarium pseudograminearum. Journal of Applied Microbiology. 2020;129(4):971-990.

30. TariqJaveed M, Farooq T, Al-Hazmi AS, Hussain MD, Rehman AU. Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. Journal of Invertebrate Pathology. 2021;107626.

31. Pozo-Serrano J, Cruz ERDL, Teresa-Cardoso M, Rodríguez-Pérez A, García-Pupo J, Pérez-Tejeda Y, et al. Efectividad antagónica In vitro de Trichoderma sp., frente a Stemphylium lycopersici. Cultivos Tropicales. 2019;40(3).

32. Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science. 2019;10:845.

33. Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R. Trichoderma secondary metabolites active on plants and fungal pathogens. The Open Mycology Journal. 2014;8(1):127-139.

34. Vinale F, Ghisalberti EL, Sivasithamparam K, Marral R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology. 2009;48(6):705-711.

35. Khan RAA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms. 2020;8(6), 817.

36. Sonkar P, Chandra R, Singh R, Kumar S. Study on management of Fusarium oxysporum through different mode of action of Trichoderma spp. International Journal of Current Trends Science and Technology. 2018;8:20192-20200.

37. Macheleidt J, Mattern DJ, Fischer J, Netzker T, Weber J, Schroeckh V, et al. Regulation and role of fungal secondary metabolites. Annual Review of Genetics. 2016;50:371-392.

38. Shyamli S, Prem D, Rs T, Atar S. Production and antifungal activity of secondary metabolites of Trichoderma virens. Pesticide Research Journal. 2005;17(2):26-29.

39. Shi M, Chen L, Wang XW, Zhang T, Zhao PB, Song XY, Sun CY, Chen XL, Zhou BC, Zhang YZ. Antimicrobial peptaibols from Trichoderma pseudokoningii induce programmed cell death in plant fungal pathogens. Microbiology. 2012;158:166-175.

40. Sha S, Liu L, Pan S, Wang WM. Isolation and purification of antifungal components from Trichoderma harzianum ferment broth by high-speed counter-current chromatography. Chinese Journal of Biological Control. 2013;29(1):83-88.

41. Marler TE, Krishnapillai MV. Vertical strata and stem carbon dioxide efflux in Cycas trees. Plants. 2020;9(2):230.

42. Chikov VI, Akhtyamova GA, Khamidullina LA. Ecological significance of the interaction of photosynthesis light and dark processes. American Journal of Plant Sciences. 2021;12(04):624.

43. Ferrero Holtz EW, Gonzalez MG, Giuffré L, Ciarlo E. Glomalins and their relationship with soil carbon. International Journal of Applied Science and Technology. 2016;6(2):69-73.

44. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytologist. 2015;205(4):1537-1551.

45. Kittredge J. Soil Carbon Restoration: Can Biology do the Job?. NE Organic farming association, Massachusetts Chapter, 16. 2015. [citado 20/07/2021]. Disponible en: https://www.unifiedfieldcorporation.com/wp-content/uploads/2015/11/2015_White_Paper_web.pdf

46. Olivas‑Tarango AL, Tarango‑Rivero SH, Ávila‑Quezada GD. Pecan production improvement by zinc under drip irrigation in calcareous soils. Terra Latinoamericana, 2021;39:1-12.

47. Tarango-Rivero SH, Ávila-Quezada GD, Jacobo-Cuellar JL, Ramírez-Valdespino CA, Orrantia-Borunda E, Rodríguez-Heredia R, Olivas-Tarango AL. Chelated zinc and beneficial microorganisms: A sustainable fertilization option for pecan production. Revista Chapingo. Serie horticultura, 2022;28(3):145-159.

INTRODUCTION

⌅

Feeding the world's population is a priority issue, therefore the 2030 Agenda for Sustainable Development of the United Nations includes within its 17 Sustainable Development Goals, the goal zero hunger (11. ONU. Objetivos del Desarrollo Sostenible de la Agenda 2030 ONU. 2021 [citado 20/07/2021]. Disponible en: https://www.un.org/sustainabledevelopment/).

Achieving this is challenging, as plants are exposed to many soil conditions that could affect growth and production. For instance, pests and diseases are one of the biggest challenges crop growers face every year. In addition, emerging diseases constitute one of the greatest risks due to the devastation they cause in agricultural production (22. Avila-Quezada G, Silva-Rojas HV, Sánchez-Chávez E, Leyva-Mir G, Martínez-Bolaños L, Guerrero-Prieto V, et al. Seguridad alimentaria: la continua lucha contra las enfermedades de los cultivos. Tecnociencia Chihuahua. 2016;10(3):133-142.-55. Avila-Quezada GD, Esquivel JF, Silva-Rojas HV, Leyva-Mir G, García-Avila C, Noriega-Orozco L, et al. Emerging plant diseases under a changing climate scenario: Threats to our global food supply. Emirates Journal of Food and Agriculture. 2018;30(6):443-450.).

It is known that the excessive application of agrochemicals have an immediate effect on what is desired to achieve during agricultural production (66. Sánchez-Chávez E, Silva-Rojas HV, Leyva-Mir G, Villareal-Guerrero F, Jiménez-Castro J, Molina-Gayoso E, et al. An effective strategy to reduce the incidence of Phytophthora root and crown rot in bell pepper. Interciencia. 2017;42(4):229-235.); however, this is achieved with environmental consequences and damage to the health of agricultural workers and consumers. Sustainable technologies must be used to produce the food demanded by the population without affecting natural resources.

The soil, because it shelters a great biodiversity, is considered the basis for the production of healthy foods. Microbial diversity has several roles, one of which is the solubility of minerals to make them more available to plants. For example, phosphate solubilizing bacteria contribute up to 50 % of the element solubilization (77. Galvez ZYA, Burbano VEM. Solubilización de fosfatos: una función microbiana importante en el desarrollo vegetal. NOVA Publicación en Ciencias Biomédicas. 2015;12(21):67-79.). Some organisms such as mycorrhizal fungi carry the elements to roots through their hyphae (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.), even endomycorrhizae deposit them in the interarbuscular space (inside the plant).

This microbial activity promotes fertile soil and a balance of organisms and microorganisms. For instance, the earthworm improves the soil structure while reducing the populations of phytopathogens (Figure 1). Also the fungus Trichoderma has a broad spectrum of action that allows it to reduce a large number of plant pathogens.

Figure 1. Eartworms and other microorganisms, members of the soil ecosystem in equilibrium, each with a specific task

DEVELOPMENT

⌅

Soil organisms

⌅

Earthworms, by its ability to dig galleries and produce demographic profiles and relationships with the soil microflora, are a key component in the nutrient cycling in soils. Their physical activities and resultant chemical effects, promote short and rapid cycles of nutrients and assimilable carbohydrates (99. Le Bayon RC, Bullinger-Weber G, Schomburg A, Turberg P, Schlaepfer R, Guenat C. (2017). Earthworms as ecosystem engineers: A review. Earthworms: Types, Roles and Research. NOVA Science Publishers, New York, 129-178.).

Moreover, in agriculture the addition of vermicompost is a common practice. Vermicompost has an essential role to promote life in the soil by improving the texture and promoting satisfactory levels of macro and micronutrients (1010. Sánchez-Rosales R, Hernández-Rodríguez A, Ojeda-Barrios D, Robles-Hernández L, González-Franco A, Parra-Quezada R. Comparison of three systems of decomposition of agricultural residues for the production of organic fertilizers. Chilean Journal of Agricultural Research. 2017;77(3):287-292.). It contains many compounds rich in beneficial microorganisms and growth hormones that function as biofertilizing and biological control agent against plant pests and pathogens (1111. Sulaiman ISC, Mohamad A. The use of vermiwash and vermicompost extract in plant disease and pest control. In: Natural Remedies for Pest, Disease and Weed Control. Academic Press; 2020. p. 187-201.). In addition, during vermicomposting, the Californian Red worm (Eisenia foetida) ingests organic matter, which progressively decomposes and fragments. This matter is made up of microorganisms including a large number of fungi. The mucous substances yielded by earthworms have strong antimicrobial and antifungal activity (1212. Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pakistan Journal of Pharmaceutical Sciences. 2016;29(3):969-977.). Through their skin secretions and antimicrobial protein, they control microorganisms (1313. Prakash M, Gunasekaran G. Antibacterial activity of the indigenous earthworms Lampito mauritii (Kinberg) and Perionyx excavatus (Perrier). The Journal of Alternative and Complementary Medicine. 2011;17:167-170.), thus reducing the populations of soil plant pathogens.

The surface of the earthworm's skin contains antimicrobial peptides that protect it from the environment. It discharges peptides such as lysozyme through its skin, resulting in antimicrobial activity. In addition, the body wall and intestinal secretion have been shown to reduce Fusarium oxysporum (1212. Andleeb S, Ejaz M, Awan UA, Ali S, Kiyani A, Shafique I, et al. In vitro screening of mucus and solvent extracts of Eisenia foetida against human bacterial and fungal pathogens. Pakistan Journal of Pharmaceutical Sciences. 2016;29(3):969-977.).

Earthworms feed on soils that contain organic materials, live microorganisms, and insects. Once the food is ingested, it is modified in the earthworm body to facilitate its absorption. When entering through the mouth, the material is swallowed by the pharynx which is a force pump (Figure 2). After that, the muscles contract and move the food up the esophagus. Then, it goes to the crop (which contracts more than the gizzard) where it is stored and moves towards the gizzard. This is a strong muscle that grinds the material into very small parts, where the enzyme secretion take part in breaking down the products. The finely crushed material goes through the digestion process in the intestine. Here more enzymes are added to promote the breakdown into simple molecules (1414. Jouni F. Synergistic interaction earthworm-microbiota: a role in the tolerance and detoxification of pesticides?. Agricultural sciences. Université d’Avignon. 2018. English. ffNNT: 2018AVIG0699ff. [citado 20/07/2021]. Disponible en: https://tel.archives-ouvertes.fr/tel-02074579/document). Enzymes include protease, lipase, amylase, lichenase, cellulase and chitinase (1515. Edwards CA, Fletcher KE. Interactions between earthworms and microorganisms in organic-matter breakdown. Agriculture, Ecosystems & Environment. 1988;24(1-3):235-247.). All this process achieves partially the elimination of plant pathogens.

Figure 2. Earthworm's body organs, where the decomposing of ingested organic matter occurs, due to enzymatic activity

Earthworms as Eisenia foetida is reported to control nematodes as Pratylechus sp in tomato (1616. Nath G, Singh K. Combination of vermicomposts and biopesticides against nematode (Pratylenchus sp.) and their effect on growth and yield of tomato (Lycopersicon esculentum). IIOAB Journal. 2011;2:27-35.), Meloidogyne javanica in cucumber (1717. Rostami M, Olia M, Arabi M. Evaluation of the effects of earthworm Eisenia fetida-based products on the pathogenicity of root-knot nematode (Meloidogyne javanica) infecting cucumber. International Journal of Recycling of Organic Waste in Agriculture. 2014;3(2):58.), and Meloidogyne hapla in tomato (1818. Edwards CA, Arancon NQ, Emerson E, Pulliam R. Suppressing plant parasitic nematodes and arthropod pests with vermicompost teas. Biocycle. 2007;48(12):38-39.).

Other reserchers found that the earthworm Lumbricus terrestris fed on sclerotia of Sclerotinia sclerotiorum when they were hydrated (1919. Euteneuer P, Wagentristl H, Steinkellner S, Scheibreithner C, Zaller JG. Earthworms affect decomposition of soil-borne plant pathogen Sclerotinia sclerotiorum in a cover crop field experiment. Applied Soil Ecology. 2019;138:88-93.). L. terrestris consumed an average of 61 % of sclerotia that were hydrated for 13 weeks. Besides, worm humus and arbscular mycorrhizal fungi improve the quality of fruits (2020. Charles NJ, Martín Alonso NJ. Uso y manejo de hongos micorrízicos arbusculares (HMA) y humus de lombriz en tomate (Solanum lycopersicum L.), bajo sistema protegido. Cultivos Tropicales. 2015;36(1):55-64.).

Soil microorganisms, interactions and microenvironments

⌅

The biological structure of the soil is made up of a large number of bacteria, actinomycetes and fungi (2121. González-Escobedo R, Muñoz-Castellanos LN, Muñoz-Ramirez ZY, Guigón López C, Avila-Quezada GD. Microbial community analysis of rhizosphere of healthy and wilted pepper (Capsicum annuum L.) in an organic farming system. Microbial Ecology. 2021; Por asignar). All of them are associated with organic matter and polymeric microbial materials such as enzymes and extracellular polysaccharides that they themselves produce.

Microorganisms are found in dense tissues of clay or humified organic matter, in mucigel deposits, in micropores, or in carbohydrate-rich root plants. At these sites, microorganisms temporarily survive adverse conditions.

In this review we address two types of microorganisms that benefit plants and that are generally found naturally in soils in symbiosis with plants, and that can be used to enrich soils, such as mycorrhizal fungi and Trichoderma spp.

Once the micro and macroelements are solubilized by bacteria, they are transferred through the hypha of the mycorrhizal fungus to the previously mycorrhizal root. Phosphate transporter enzymes of the fungus and the plant are involved in this process (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.).

The protection against plant pathogens that mycorrhizal fungi confer on plants has been demonstrated (2222. Zhang H, Franken P. Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza. 2014;24:419-430., 2323. Song Y, Chen D, Lu K, Sun Z, Zeng R. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science. 2015;6:786.). In the rhizosphere, microorganisms compete for space and nutrients. In addition, mycorrhizae also stimulate the biochemical defense mechanisms of plants (2222. Zhang H, Franken P. Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza. 2014;24:419-430.).

The interactions between mycorrhizae and plants are self-regulating, in fact, when mineral nutrients are available in the soil, the colonization of mycorrhizae is reduced (2424. Azcón R, Ambrosano E, Charest C. Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Science. 2003;165(5):1137-1145.). Apparently, all microbial populations in the soil are self-regulating, even the plant regulates microorganisms in its rhizosphere. Thus, by adding microorganisms to the soil, they can be active for months or a year and disappear after that time. Some authors found that by incorporating the ectomycorrhizal fungus Pisolithus tinctorius, it protected Pinus sylvestris seedlings from the attack of Fusarium moniliforme and Rhizoctonia solani; this protection lasted one year (2525. Chakravarty P, Unestam T. Differential influence of ectomycorrhizae on plant growth and disease resistance in Pinus sylvestris seedlings. Journal of Phytopathology. 1987;120(2):104-120.).

It is very interesting to know the symbiosis in depth. The interaction begins through signals, and depending on the requirements of the plant and other as yet unknown factors, soil microorganisms regulate themselves.

Endomycorrhizal fungi are also root protectors against pathogens. For instance, a mixture of Arbuscular mycorrhizal fungi (AMF) composed by Glomus aggregatum, Gigaspora margarita and Glomus intraradices suppressed root rot by Fusarium solani in Phaseolus vulgaris under greenhouse conditions (2626. Eke P, Adamou S, Fokom R, Nya VD, Fokou PVT, Wakam LN, et al. Arbuscular mycorrhizal fungi alter antifungal potential of lemongrass essential oil against Fusarium solani, causing root rot in common bean (Phaseolus vulgaris L.). Heliyon. 2020;6(12):e05737.).

Even endomycorrhizal fungi can control nematodes such as Meloidogyne incognita (2727. da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection. 2020;135:105203.) and Meloidogyne javanica (2828. Sharma M, Saini I, Kaushik P, Al Dawsari MM, Al Balawi T, Alam P. Mycorrhizal fungi and Pseudomonas fluorescens application reduces root-knot nematode (Meloidogyne javanica) infestation in eggplant. Saudi Journal of Biological Sciences. 2021;28(7): 3685-3691.).

The reduction in the penetration of M. incognita in endomycorrhized plants may be due to the fact that AMF induce changes in the plant, and in response, the roots produce exudates, which suggests that exudates affect the motility of nematodes in the soil.

Other possibilities are the production of nematicidal compounds, increased lignification of the roots, changes in the composition of the cell wall and activation of the defense mechanisms of plants.

The accumulation of phenolic compounds, such as phytoalexins and flavonoids and isoflavonoids has been demonstrated in mycorrhizal roots in the presence of the nematode. AMF can also increase the activity of defense enzymes such as peroxidase, polyphenoloxidase, superoxide dismutase, chitinase and β 1,3 glucanase (2727. da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative. Crop Protection. 2020;135:105203.). In general, AMF naturally present in soil may be highly beneficial to sustainable agriculture, maintaining plant production by reducing pathogens.

Moreover, Trichoderma is a beneficial fungus that has demonstrated efficiency in the control of root pathogens (2929. Stummer BE, Zhang Q, Zhang X, Warren RA, Harvey PR. Quantification of Trichoderma afroharzianum, Trichoderma harzianum and Trichoderma gamsii inoculants in soil, the wheat rhizosphere and in planta suppression of the crown rot pathogen Fusarium pseudograminearum. Journal of Applied Microbiology. 2020;129(4):971-990.) including nematodes (3030. TariqJaveed M, Farooq T, Al-Hazmi AS, Hussain MD, Rehman AU. Role of Trichoderma as a biocontrol agent (BCA) of phytoparasitic nematodes and plant growth inducer. Journal of Invertebrate Pathology. 2021;107626.), due to its ability to secrete volatile and non-volatile compounds, and secondary metabolites. Its direct mechanism includes competition, mycoparasitism, antibiosis, and induction of plant resistance mechanisms, as well as indirect mechanisms such as the inactivation of the enzymes produced by the pathogen (3131. Pozo-Serrano J, Cruz ERDL, Teresa-Cardoso M, Rodríguez-Pérez A, García-Pupo J, Pérez-Tejeda Y, et al. Efectividad antagónica In vitro de Trichoderma sp., frente a Stemphylium lycopersici. Cultivos Tropicales. 2019;40(3)., 3333. Vinale F, Sivasithamparam K, Ghisalberti EL, Woo SL, Nigro M, Marra R. Trichoderma secondary metabolites active on plants and fungal pathogens. The Open Mycology Journal. 2014;8(1):127-139.).

Among secondary metabolites are terpenes, pyrones, gliotoxin, gliovirin, and peptaibols (3434. Vinale F, Ghisalberti EL, Sivasithamparam K, Marral R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology. 2009;48(6):705-711.). Antifungal metabolites produced by Trichoderma are epipolythiodioxopiperazines, peptaibols, pyrones, butenolides, pyridones, azaphilones, koninginins, steroids, anthraquinones, lactones, trichothecenes, and other (3535. Khan RAA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms. 2020;8(6), 817., 3636. Sonkar P, Chandra R, Singh R, Kumar S. Study on management of Fusarium oxysporum through different mode of action of Trichoderma spp. International Journal of Current Trends Science and Technology. 2018;8:20192-20200.).

The expression of genes related to secondary metabolites in Trichoderma spp. depends on factors such as pH signaling, velvet complex proteins and communication signals with other microorganisms (3737. Macheleidt J, Mattern DJ, Fischer J, Netzker T, Weber J, Schroeckh V, et al. Regulation and role of fungal secondary metabolites. Annual Review of Genetics. 2016;50:371-392.).

These metabolites exhibit bioactivity against plant pathogens as Macrophomina phaseolina, Pythium spp., Sclerotium rolfsii, Rhizoctonia solani, Fusarium oxysporum, Verticillium dahliae, Botrytis cinerea, Ascochyta citrullina, Phytophthora parasitica, P. cinnamomi, Leptosphaeria maculans, Clavibacter spp., Gaeumannomyces graminis, Colletotrichum gloeosporioides, among others (3434. Vinale F, Ghisalberti EL, Sivasithamparam K, Marral R, Ritieni A, Ferracane R, Woo S, Lorito M. Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Letters in Applied Microbiology. 2009;48(6):705-711., 3535. Khan RAA, Najeeb S, Hussain S, Xie B, Li Y. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms. 2020;8(6), 817., 3838. Shyamli S, Prem D, Rs T, Atar S. Production and antifungal activity of secondary metabolites of Trichoderma virens. Pesticide Research Journal. 2005;17(2):26-29.-4040. Sha S, Liu L, Pan S, Wang WM. Isolation and purification of antifungal components from Trichoderma harzianum ferment broth by high-speed counter-current chromatography. Chinese Journal of Biological Control. 2013;29(1):83-88.).

Plants, microorganisms and carbon

⌅

Plants take carbon dioxide from the atmosphere and exude some carbon as a sugary substance through their roots. This secretion feeds the microorganisms in the soil. When plants die, microorganisms break down carbon and use it for metabolism. This microbial decomposition releases carbon dioxide, therefore the soil stores more carbon when it is full of microbial life (4141. Marler TE, Krishnapillai MV. Vertical strata and stem carbon dioxide efflux in Cycas trees. Plants. 2020;9(2):230., 4242. Chikov VI, Akhtyamova GA, Khamidullina LA. Ecological significance of the interaction of photosynthesis light and dark processes. American Journal of Plant Sciences. 2021;12(04):624.).

Mycorrhizal fungi produce mucilaginous substances (88. Madrid-Delgado G, Orozco-Miranda M, Cruz-Osorio M, Hernández-Rodríguez A, Rodríguez-Heredia R, Roa-Huerta M, et al. Pathways of phosphorus absorption and early signaling between the mycorrhizal fungi and plants. Phyton International Jornal of Experimental Botany. 2021;90(5):1321-1338.) such as glomalin. This is a very stable recalcitrant glycoprotein, with a half-life of up to 42 years, and constitutes the largest component of soil organic matter (4343. Ferrero Holtz EW, Gonzalez MG, Giuffré L, Ciarlo E. Glomalins and their relationship with soil carbon. International Journal of Applied Science and Technology. 2016;6(2):69-73.), it also promotes soil aggregation. Mycorrhizal fungi transfer more carbon to the soil than other microorganisms (4444. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, et al. Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytologist. 2015;205(4):1537-1551.) (Figure 3).

Figure 3. Carbon dioxide (CO₂) scheme from entering the tree canopy to its filtration into the soil, and the activity of microorganisms

Some of the carbon remains in the soil from days to a few years. Microorganisms can digest this carbon, thus emitting carbon dioxide. Thus is how carbon can remain for years or decades in a site (4545. Kittredge J. Soil Carbon Restoration: Can Biology do the Job?. NE Organic farming association, Massachusetts Chapter, 16. 2015. [citado 20/07/2021]. Disponible en: https://www.unifiedfieldcorporation.com/wp-content/uploads/2015/11/2015_White_Paper_web.pdf). An important agricultural activity is the application of compost to the soil. Compost harbors microorganisms and can retain carbon for centuries.

Minimum tillage causes that the soil carbon is not exposed to oxygen and the soil aggregates remain intact, protecting their carbon (4545. Kittredge J. Soil Carbon Restoration: Can Biology do the Job?. NE Organic farming association, Massachusetts Chapter, 16. 2015. [citado 20/07/2021]. Disponible en: https://www.unifiedfieldcorporation.com/wp-content/uploads/2015/11/2015_White_Paper_web.pdf-4747. Tarango-Rivero SH, Ávila-Quezada GD, Jacobo-Cuellar JL, Ramírez-Valdespino CA, Orrantia-Borunda E, Rodríguez-Heredia R, Olivas-Tarango AL. Chelated zinc and beneficial microorganisms: A sustainable fertilization option for pecan production. Revista Chapingo. Serie horticultura, 2022;28(3):145-159.).

Soil carbon sequestration is a natural way to remove carbon dioxide from the atmosphere, and this can be achieved with sustainable agricultural practices. These practices will improve the ability of soils to store carbon and help minimize the effects of global warming.

CONCLUSIONS

⌅

This review presents how plants drawn CO₂ from the air, synthesize carbohydrates, which exude from roots, to feed, attract or repel microorganisms. Additionally, the important activity of soil organisms and microorganisms for the plant benefit is highlighted, focusing on earthworms, mycorrhizal fungi and Trichoderma since they can reduce plant pathogens populations. All of them within their specialty, achieve by competition for space, or with physical and chemical mechanisms, reduce soil plant pathogens.
Earthworms, mycorrhizal fungi and Trichoderma, naturally present in soil may be highly beneficial to sustainable agriculture, maintaining plant production and biological balance in soils. We conclude that integrated crop management promotes competition and balance, essential to maintaining soil health and ensuring food production. Finally, knowledge of the diversity of edaphic biota in agroecosystems allows the implementation of strategies for land use.

ACKNOWLEDGMENTS

⌅

The authors thank the Postgraduate programs of National Council of Science and Technology (Conacyt), of the Faculty of Agrotechnological Sciences of the Autonomous University of Chihuahua, Mexico.