An approaching to Ectomycorrhizae world
Main Article Content
Abstract
Ectomycorrhizae are generally considered the most advanced symbiotic association between higher plants and fungi, because although they involve only 3 % of seed plants, all plants species are woody species; trees and shrubs, including most fruit trees. Therefore the ectomycorrizal association is important worldwide due to the large area covered by plants and due to its economic value as source of wood. In this review, references are made to the characteristics of the association, taking into account the morphology of the symbiosis, the mechanisms used to establish the association and how they influence plant nutrition.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Those authors who have publications with this journal accept the following terms of the License Attribution-NonCommercial 4.0 International (CC BY-NC 4.0):
You are free to:
- Share — copy and redistribute the material in any medium or format
- Adapt — remix, transform, and build upon the material
The licensor cannot revoke these freedoms as long as you follow the license terms.
Under the following terms:
- Attribution — You must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.
- NonCommercial — You may not use the material for commercial purposes.
- No additional restrictions — You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits.
The journal is not responsible for the opinions and concepts expressed in the works, they are the sole responsibility of the authors. The Editor, with the assistance of the Editorial Committee, reserves the right to suggest or request advisable or necessary modifications. They are accepted to publish original scientific papers, research results of interest that have not been published or sent to another journal for the same purpose.
The mention of trademarks of equipment, instruments or specific materials is for identification purposes, and there is no promotional commitment in relation to them, neither by the authors nor by the publisher.
References
Brundrett M, Tedersoo L. Evolutionary history of mycorrhizal symbiosis and global host plant diversity. New Phytologist 220: 1108–1115. 2018. Available from:
J. André Fortin, Christian Plenchette & Yves Piché, Les mycorhizes, la nouvelle révolution verte, Éditions MultiMondes, Éditions Quae, 2008, 131 Plantilla:Nb p. Available from:
DeFries, R. S., Rudel, T., Uriarte, M., and Hansen, M. Deforestation driven by urban population growth and agricultural trade in the twenty-first century. Nat. Geosci, (2010). 3, 178–181. doi: 10.1038/ngeo756
Chazdon, R. L. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science 320, 1458–1460, 2008). doi: 10.1126/science. 1155365
Aerts, R., and Honnay, O. Forest restoration, biodiversity and ecosystem functioning. BMC Ecol. 11:29. (2011). doi: 10.1186/1472-6785-11-29
Policelli N, Horton TR, Hudon AT, Patterson TR and Bhatnagar JM. Back to Roots: The Role of Ectomycorrhizal Fungi in Boreal and Temperate Forest Restoration. Front. For. Glob. Change 3:97, (2020). doi: 10.3389/ffgc.2020.00097
B. Meyer-Berthaud, S.E. Scheckler y J. WendtArchaeopteris es el primer árbol moderno conocido. Nature '446', (1999): 904-907. Available from:
Tedersoo L & Brundrett M. chapter 19: Evolution of ectomycorrhizal symbiosis in plants. Ecol. Stu. 230, 2017. 407-467. L. Tedersoo (ed.), Biogeography of Mycorrhizal Symbiosis, Ecological Studies 230, DOI 10.1007/978-3-319-56363-3_19
Maherali H, Oberle B, Stevens PF, Cornwell WK, McGlinn DJ. Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am Nat (2016). 188:E113–E125. Available from:
B. Wang y Y.L. Qiu. Distribución filogenética y evolución de micorrizas en plantas terrestres. Mycorrhiza '16', (2006). 299-363. Available from: (http://mycorrhiza.ag.utk.edu/reviews/rev_wang1.pdf)
Strullu DG. Les mycorhizes, Handbuch der Pflanzenanatomie. Berlin, 1985. Available from:
Smith SE, Read DJ.Mycorrhizal symbiosis. Cambridge, UK: Academic Press, 2008. Available from: (https://dx.doi.org/)
Mika Tarkka Uwe Nehls, Rüdiger Hampp. Fisiología de la ectomicorriza (ECM). Progreso en Botánica, (2005). Vol 66, Parte 3, 247-276. doi 10.1007 / 3-540-27043-4_1110.1007 / 3-540-27043-4_11
Francis Martin, Annegret Kohler, Claude Murat, Claire Veneault-Fourrey and David S. Hibbett. Unearthing the roots of ectomycorrhizal symbioses. New Phytologist, 2016. 220: 1012–1030 doi: 10.1111/nph.15076
Finlay, R. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot, (2008). 59, 1115–1126. Available from:
Peterson, R. L. & Massicotte, H. B. Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can. J. Bot. 82, 1074–1088 (2004). Available from:
Tedersoo, L., May, T. W. & Smith, M. E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263 (2010). Available from:
Matheny, P. B. & Hibbett, D. S. The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biol. 7, 13 (2009). Available from:
Skrede, I. et al. Evolutionary history of Serpulaceae (Basidiomycota): molecular phylogeny, historical biogeography and evidence for a single transition of nutritional mode. BMC Evol. Biol. 11, 230 (2011). Available from:
Yamamoto K, Endo N, Degawa Y, Fukuda M, Yamada A. First detection of Endogone ectomycorrhizas in natural oak forests. Mycorrhiza, 2017. 27: 295–301. Available from:
Duplessis, S., Courty, P. E., Tagu, D. & Martin, F. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol. 165, 599–611 (2005). Available from:
Larsen, P. E. et al. Multi-omics approach identifies molecular mechanisms of plant–fungus mycorrhizal interaction. Front. Plant Sci. 6, 1061 (2016). Available from:
Luo, Z. B. et al. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol. 151, 1902–1917 (2009). Available from:
Tschaplinski, T. J. et al. Populus trichocarpa and Populus deltoides exhibit different metabolomic responses to colonization by the symbiotic fungus Laccaria bicolor. Mol. Plant Microbe Interact. 27, 546–556 (2014). Available from:
Plett, J. M. et al. Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytol. 202, 270–286 (2014). Available from:
Ditengou, F. A. et al. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat. Commun. 6, 6279 (2015). Available from:
Sukumar, P. et al. Involvement of auxin pathways in modulating root architecture during beneficial plant– microorganism interactions. Plant Cell Environ. 36, 909–919 (2013). Available from:
Garcia, K., Delaux, P. M., Cope, K. R. & Ané, J. M. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbiosis. New Phytol. 208, 79–87 (2015). Available from:
Lo Presti, L. et al. Fungal effectors and plant susceptibility. Annu. Rev. Plant Biol. 66, 513–545 (2015). Available from:
Plett, J. M. & Martin, F. Reconsidering mutualistic plant–fungal interactions through the lens of effector biology. Curr. Opin. Plant Biol. 26, 45–50 (2015).
Plett, J. M. et al. The effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses JA responsive genes. Proc. Natl Acad. Sci. USA 111, 8299 (2014).
Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410–415 (2015).
Veneault-Fourrey, C. et al. Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet. Biol. 72, 168–181 (2014).
Plett, J. M. et al. Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor. Fungal Genet. Biol. 49, 199–209 (2012). Available from:
Casieri, L., Lahmidi, N. A., Doidy, J., Veneault-Fourrey, C.,Migeon, A., Bonneau, L.,et al. Biotrophic transportome in mutualistic plant fungal interactions. Mycorrhiza 23 (8), 597–625. (2013). doi: 10.1007/s00572-013-0496-9
Nehls, U., and Plassard, C. Nitrogen and phosphate metabolism in ectomycorrhizas. New Phytol, (2018). 220, 4. doi: 10.1111/nph.15257
Becquer, A., Guerrero-Galánc, C., Eibensteiner, J. L., Houdinet, G., Bücking, H., Zimmermann, S. D., et al. “The ectomycorrhizal contribution to tree nutrition,” in Advances in Botanical Research, vol. 89 Eds. F. M. Cánovas (Cambridge, MA, USA: Academic Press), (2019). Available from:
Javelle, A., Rodŕıguez-Pastrana, B. R., Jacob, C., Botton, B., Brun, A., Andre, B., et al. Molecular characterization of two ammonium transporters from the ectomycorrhizal fungus Hebeloma cylindrosporum. FEBS Lett, (2001). 505, 3. doi: 10.1016/S0014-5793(01)02802-2
Javelle, A., Morel, M., Rodŕıguez-Pastrana, B. R., Botton, B., Brun, A., Andre, B., et al. Molecular characterization, function and regulation of ammonium transporters (Amt) and ammonium-metabolizing enzymes (GS, NADP-GDH) in the ectomycorrhizal fungus Hebeloma cylindrosporum. Mol. Microbiol, (2003), 47, 2. doi: 10.1046/j.1365-2958.2003.03303.x
Montanini, B., Moretto, N., Soragni, E., Percudani, R., and Ottonello, S. A high-affinity ammonium transporter from the mycorrhizal ascomycete Tuber borchii. Fungal Genet. Biol, (2002). 36, 1. doi: 10.1016/S1087-1845(02)00001-4
Willmann, A., Weiß, M., and Nehls, U. Ectomycorrhiza-mediated repression of the high-affinity ammonium importer gene AmAMT2 in Amanita muscaria. Curr. Genet, (2007). 51, 71. doi: 10.1007/s00294-006-0106-x
Lucic, E., Fourrey, C., Kohler, A., Martin, F., Chalot, M., and Brun-Jacob, A. A gene repertoire for nitrogen transporters in Laccaria bicolor. New Phytol, (2008). 180, 2. doi: 10.1111/j.1469-8137.2008.02580.x
Hortal, S., Plett, K. L., Plett, J. M., Cresswell, T., Johansen, M., Pendall, E., et al. Role of plant-fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi. ISME J, (2017). 11, 12. doi: 10.1038/ismej.2017.116
Kemppainen, M. J., Alvarez Crespo, M. C., and Pardo, A. G. fHANT-ACgenes of the ectomycorrhizal fungus Laccaria bicolor are not repressed by lglutamine allowing simultaneous utilization of nitrate and organic nitrogen sources. Environ. Microbiol, (2010). Rep. 2, 4. doi: 10.1111/j.1758-2229.2009.00111.x
Jargeat, P., Rekangalt, D., Verner, M. C., Gay, G., Debaud, J. C., Marmeisse, R.,et al. Characterization and expression analysis of a nitrate transporter and nitrite reductase genes, two members of a gene cluster for nitrate assimilation from the symbiotic basidiomycete Hebeloma cylindrosporum. Curr. Genet. (2003). 43, 3. doi: 10.1007/s00294-003-0387-2
Kemppainen, M. J., Dupessis, S., Martin, F. M., and Pardo, A. G. RNA silencing in the model mycorrhizal fungus Laccaria bicolor: Gene knock-down of nitrate reductase results in inhibition of symbiosis with Populus. Environ. Microbiol. (2009). 11, 7. doi: 10.1111/j.1462-2920.2009.01912.x
Stuart EK and Plett KL. Digging Deeper: In Search of the Mechanisms of Carbon and Nitrogen Exchange in Ectomycorrhizal Symbioses. Front. Plant Sci. (2020). 10:1658. doi: 10.3389/fpls.2019.01658
Bödeker, I. T., Clemmensen, K. E., de Boer, W., Martin, F., Olson, Å., and Lindahl, B. D. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytol. (2014). 203, 1. doi:10.1111/nph.12791
Corrêa, A., Strasser, R. J., and Martins-Loução, M. A. Response of plants to ectomycorrhizae in N-limited conditions: which factors determine its variation? Mycorrhiza 18, (2008). 8. doi: 10.1007/s00572-008-0195-0
Albarracín, M. V., Six, J., Houlton, B. Z., and Bledsoe, C. S. (2013). A nitrogen fertilization field study of carbon-13 and nitrogen-15 transfers in ectomycorrhizas of Pinus sabiniana. Oecologia 173 (4), 1439–1450. doi: 10.1007/s00442-013-2734-4
Valtanen, K., Eissfeller, V., Beyer, F., Hertel, D., Scheu, S., and Polle, A. (2014). Carbon and nitrogen fluxes between beech and their ectomycorrhizal assemblage. Mycorrhiza 24, 8. doi: 10.1007/s00572-014-0581-8
Hasselquist, N. J., Metcalfe, D. B., Marshall, J. D., Lucas, R. W., and Högberg, P. Seasonality and nitrogen supply modify carbon partitioning in understory vegetation of a boreal coniferous forest. Ecology 97, (2016). 3. doi:10.1890/15-0831.1
Näsholm, T., Högberg, P., Franklin, O., Metcalfe, D., Keel, S. G., Campbell, C., et al. Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol, (2013). 198, 1. doi: 10.1111/nph.12139
Turner ,B.L .Resource partitioning for soil phosphorus: a hypothesis. J. Ecol, (2008). 96, 698–702. doi:10.1111/j.1365-2745.2008.01384.x
Rennenberg, H., and Herschbach, C. Phosphorus nutrition of woody plants: many questions – few answers. Plant Biol, (2013). 15, 785–788. doi:10.1111/plb.12078
Becquer A, Trap J , Irshad U, Ali MA, Plassard C. From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association. Frontiers in Plant Science, (2014). 1-7, DOI: 10.3389/fpls.2014.00548
Plassard, C., and Dell, B. Phosphorus nutrition of mycorrhizal trees. Tree Physiol, (2010). 30, 1129–1139. doi:10.1093/treephys/tpq063
Turner,B.L., Paphazy,M.J., Haygarth,P.M., and Mckelvie,I.D. Inositol phosphates in the environment. Philos.Trans.R.Soc.Lond. BBiol.Sci, (2002). 357, 449–469. doi:10.1098/rstb.2001.0837
Rayboy,V. “Seed phosphorus and the development of low-phytatecrops,” in Inositol Phosphates: Linking Agriculture and the Environment, eds B.L. Turner, A. E.Richardson, and E.J. Mullaney (Wallingford:CABInternational), (2007). 111–132. Available from:
Antibus,R.K., Sinsabaugh, R.L., and Linkins,A.E. Phosphatase activities and phosphorus uptake from inositolphosphate by ectomycorrhizal fungi. Can. J. Bot, (1992). 70, 794–801.doi:10.1139/b92-101
Mc Elhinney,C., andMitchell,D.T. Phosphatase activity of four ectomycorrhizal fungi found in a Sitka spruce-Japanese larch plantation in Ireland. Mycol. Res, (1993). 97, 725–732.doi:10.1016/S0953-7562(09)80154-8
Mousain,D., Bousquet,N., and Polard,C. Comparaison des activités phosphatases ? Homobasidiomycètes ectomycorhiziens en culture in vitro. Eur.J.For. Pathol, (1988). 18, 299–309.doi:10.1111/j.1439-0329.1988.tb00217.x
Louche,J., Ali,M.A., Cloutier-Hurteau,B., Sauvage,F.-X., Quiquampoix,H., and Plassard,C. Efficiency of acidphosphatases secreted from the ectomycorrhizal fungus Hebeloma cylindrosporum to hydrolyse organic phosphorus in pod- zols. FEMS Microbiol.Ecol, 73, 323–335.doi:10.1111/j.1574-6941.2010.00899.x
Richardson,A.E., George,T.S., Jakobsen,I., Simpson,R. “Plantutilization of inositolphosphates,” in InositolPhosphates:Linking Agriculture and the Environment, eds. B.L, (2007). Turner, A.E. Richardson, and E.J. Mullaney (Wallingford:CAB International), 242–260.
Plassard,C., Louche,J., Ali,M.A., Duchemin,M., Legname,E., and Cloutier- Hurteau,B. Diversity in phosphorus mobilization and uptake in ectomycorrhizal fungi. Ann.For.Sci. (2011). 68, 33–43. doi:10.1007/s13595-010- 0005-7
Kothe,E., Muller,D., and Krause,K. Different high affinity phosphate uptake systems of ectomycorrhizal Tricholoma species in relation to substrate specificity. J. Appl.Bot, (2002). 76, 127–132. Available from:
Karandashov,V., and Bucher,M. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci, (2005). 10, 22–29. doi:10.1016/j.tplants.2004.12.003
Martinez,P., and Persson,B. Identification, cloning and charaterization of a de repressible Na+-coupled phosphate transporter in Saccharomy cescerevisiae. Mol.Gen.Genet, (1998). 258, 628–638. doi:10.1007/s004380050776
Tatry,M.-V., ElKassis,E., Lambilliotte,R., Corratgé,C., vanAarle,I., Amenc, L. K., et al. Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaster. Plant J, (2009). 57, 1092–1102. doi:10.1111/j.1365- 313X.2008.03749.x
Wang,J., Li,T., Wu,X., and Zhao,Z. Molecular cloning and functional analysis of H+-dependent phosphate transporter gene from the ectomycorrhizal fungus Boletus edulis in southwest China. Fungal Biol, (2014). 118, 453–461. doi: 10.1016/j.funbio.2014.03.003
Peterson,R.L., and Bonfante,P. Comparative structure of vesicular- arbuscular mycorrhizas and ectomycorrhizas. PlantSoil 159, (1994). 79–88. doi: 10.1007/BF00000097
Smith,S.E., and Smith,F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Ann.Rev. Plant Biol, (2011). 62, 227–250. doi:10.1146/annurev-arplant-042110-103846
Bucher,M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol, (2007). 173, 11–26. doi:10.1111/j.1469-8137.2006. 01935.x
Javot,H., Pumplin,N., and Harrison,M.J. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles: phos- phate transport in the AM symbiosis. Plant Cell Environ, (2007). 30, 310–322.doi: 10.1111/j.1365-3040.2006.01617.x
Bücking,H. Phosphate absorption and efflux of three ectomycorrhizal fungi as affected by external phosphate, cation and carbohydrate concentrations. Mycol. Res, (2004). 108, 599–609. doi:10.1017/S0953756204009992
Cairney,J.W.G., and Smith,S.E. Influence of intracellular phosphorus concentration on phosphate absorption by the ectomycorrhizal basidiomycete Pisolithus tinctorius. Mycol. Res, (1992). 96, 673–676. doi:10.1016/S0953-7562(09) 80496-6
Loth-Pereda, V., Orsini, E., Courty, P .-E., Lota, F., Kohler, A., Diss, L., et al. Structure and expression profile of the phosphate Pht1 transporter gene family in mycorrhizal Populus trichocarpa. Plant Physiol, (2011). 156, 2141–2154. doi: 10.1104/pp.111.180646
Kariman,K., Barker,S.J., Jost,R., Finnegan,P.M., and Tibbett,M. A novel plant-fungus symbiosis benefits the host without forming mycorrhizal structures. New Phytol, (2014). 201, 1413–1422. doi:10.1111/nph.12600
Javot,H., Pumplin,N., and Harrison,M.J. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles: phosphate transport in the AM symbiosis. Plant Cell Environ, (2007). 30, 310–322. doi: 10.1111/j.1365-3040.2006.01617.x
Maltz, M. R.,Treseder, K. K. Sources of inocula influence mycorrhizal colonization of plants in restoration projects: a meta-analysis. Restor. Ecol, (2015). 15:12231. doi: 10.1111/rec.12231
Asmelash, F., Bekele, T., and Birhane, E. (2016). The potential role of arbuscular mycorrhizal fungi in the restoration of degraded lands. Front.Microbiol. 7: 1095. doi: 10.3389/fmicb.2016.01095
Harris, J. (2009). Soil microbial communities and restoration ecology: Facilitators or followers? Science 325, 573–574. doi: 10.1126/science.1172975
Kalucka, I. L., and Jagodzinski, A. M. Successional traits of ectomycorrhizal fungi in forest reclamation after surface mining and agricultural disturbances: a review. Dendrobiology, (2016). 76, 91–104. doi:10.12657/denbio.076.009
Koziol, L., Schultz, P. A., House, G. L., Bauer, J. T., Middleton, E. L., and Bever, J. D. The plant microbiome and native plant restoration: the example of native mycorrhizal fungi. (2018). Bioscience 68, 996–1006. doi: 10.1093/biosci/biy125