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Resumen
La asociación entre Hongo formadores de micorrizas arbusculares (HFMA) y las plantas ha permitido la adaptación de éstas a ecosistemas terrestres, presentándose en más del 80% de las plantas. El hospedero suministra carbohidratos al hongo y éste transporta los nutrientes que la planta requiere. El establecimiento de la simbiosis requiere procesos armónicos a nivel espacio-temporal, que dependen de señales específicas, para reconocimiento, colonización e intercambio de nutrientes. Las plantas presentan respuestas de defensa frente a la posible invasión de microorganismos, sin embargo, en la simbiosis éstas son débiles, localizadas y no impiden la colonización del hongo. Estas señales se observan en todas las etapas de la simbiosis, siendo la primera señal enviada por la planta en exudados de la raíz, especialmente en condiciones de bajo fósforo. Posteriormente los HFMA activan la expresión de genes que favorecen cambios a nivel celular para la formación del apresorio, del aparato de pre-penetración y en células de la corteza, del arbúsculo y la membrana periarbuscular, para el intercambio de nutrientes. Un aspecto de interés está relacionado con los mecanismos de atenuación de las respuestas de defensa de la planta. Se han planteado diversas hipótesis para entender este fenómeno y aunque el control de la simbiosis está regulado principalmente por la planta, aún se desconoce si los HFMA generan señales que facilitan el debilitamiento de las respuestas de defensa del hospedero. Este documento está orientado a hacer una revisión de las señales de reconocimiento HFMA - plantas para cada fase de la simbiosis, así como de algunos mecanismos de regulación de las respuestas de defensa de la planta para el establecimiento de la simbiosis.
Margarita Ramírez Gómez, Corporación Colombiana de Investigación Agropecuaria (Agrosavia)
Ramírez Gómez, María Margarita. Ingeniera Agrónoma. MPhil. Microbiología de Suelos. Investigador Máster. Bogotá.
Alia Rodríguez Villate, Universidad Nacional
Rodríguez Villate, Alia. Ingeniera Agrónoma Ph. D. Facultad de Agronomía. Bogotá.
Akiyama, K.; Matsuzaki, K. and Hayashi, H. (2005). Plant Sesquiterpenes Induce Hyphal Branching in Arbuscular Mycorrhizal Fungi. Nature 435: 824-827. https://doi.org/10.1038/nature03608
Akiyama, K. and Hayashi, H. (2006). Strigolactones: Chemical Signals for Fungal Symbionts and Parasitic Weeds in Plant Roots. Annals of Botany: doi:10.1093/aob/mcl063, available online at https://doi.org/10.1093/aob/mcl063
Albrecht, C.; Geurts, R.; Lapeyrie, F. and Bisseling, T. (1998). Endomycorrhizae and Rhizobial Nod Factors Both Requi-re SYM8 to Induce the Expression of the Early Nodulin Genes PsENOD5 and PsENOD12A. Plant Journal 15; 605-614. https://doi.org/10.1046/j.1365-313x.1998.00228.x
Albrecht, C.; Geurts, R. and Bisseling, T. (1999). Legume Nodulation and Mycorrhizae Formation: Two Extremes in Host Specificity Meet. Embo J. 18: 281-288. https://doi.org/10.1093/emboj/18.2.281
Bago, B.; Pfeffer, E. and Shachar-Hill, Y. (2000). Carbon Metabolism and Transport in Arbuscular Mycorrhizas. Plant Physiology. 124: 949-958. https://doi.org/10.1104/pp.124.3.949
Bécard, G. and Piché, Y. (1989). Fungal Growth Stimulation by CO2 and Root Exudates in Vesicular-arbuscular Mycorrhizal Symbiosis. Appl Environ Microbiol 55: 2320-2325. https://doi.org/10.1128/AEM.55.9.2320-2325.1989
Blee, K.A.; Anderson, A.J. (1996). Defense-related Transcript Accumulation in Phaseolus vulgaris L. Colonized by the Arbuscular Mycorrhizal Fungus Glomus Intraradices, Schenk & Smith. Plant Physiology. 110: 675-688. https://doi.org/10.1104/pp.110.2.675
Blee, K.A.; Anderson, A.J. (2000). Defense Responses in Plants to Arbuscular Mycorrhizal Fungi. In: Podila, G,K.; Douds, D., eds. Current advances in mycorrhizae research. Minnesota, USA: The Am. Phytopathol. Soc, 27-44.
Blilou, I.; Ocampo, J.; García-Garrido, J. (2000a). Induction of Catalase and Ascorbate Peroxidase Activities in Tobacco Roots Inoculated with Arbuscular Mycorrhizal Glomus Mosseae. Mycol. Res. 104: 722-725. https://doi.org/10.1017/S095375629900204X
Blilou, I.; Ocampo, J.; García-Garrido, J. (2000b). Induction of Ltp (Lipid Transfer Protein) and Pal (Phenylalanine Ammonialyase) Gene Expression in Rice Roots Colonized by the Arbuscular Mycorrhizal Fungus Glomus Mosseae. J. Exp. Bot. 51: 1969-1977. https://doi.org/10.1093/jexbot/51.353.1969
Bonanomi, A.; Oetiker, J.H.; Guggenheim, R.; Boller, T.; Wiemken, A.; Vögeli-Lange, R. (2001). Arbuscular Mycorrhizas in Minimycorrhizotrons: First Contact of Medicago truncatula Roots with Glomus Intraradices Induces Chalcone Synthase. New Phytologist 150: 573-582. https://doi.org/10.1046/j.1469-8137.2001.00135.x
Bonfante, P.; Genre, A.; Faccio, A.; Martini, I.; Schauser, L.; Stougaard, J.; Webb, J.; and Parniske, M. (2000). The Lotus japonicus LjSym4 Gene is Required for the Successful Symbiotic Infection of Root Epidermal Cells. Mol. Plant Microbe Interact. 13: 1109-1120. https://doi.org/10.1094/MPMI.2000.13.10.1109
Bonfante, P. and Genre, A. (2008). Plants and Arbuscular Mycorrhizal Fungi: an Evolutionary-developmental Perspective. Trends in Plant Science 13: 9. https://doi.org/10.1016/j.tplants.2008.07.001
Breuninger, M. and Requena, N. (2004). Recognition Events in AM Symbiosis: Analysis of Fungal Gene Expression at the Early Appressorium Stage. Fungal Genetics and Biology. 41: 794-80. https://doi.org/10.1016/j.fgb.2004.04.002
Catoira, R.; Galera, C.; Billy, F.; Penmetsa, R.V.; Journet, E.; Maillet, F.; Rosenberg, C.; Cook, D.; Gough, C.; Denarie, J. (2000). Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway. Plant Cell. 12:1647-65. https://doi.org/10.1105/tpc.12.9.1647
Dodd, J.C.; Boddington, C.; Rodríguez, A.; González-Chávez, C. and Mansur, I. (2000) Mycelium of Arbuscular Mycorrhizal Fungi (AMF) From Different Genera: Form, Function and Detection. Plant and Soil. 226 (2): 131-151. https://doi.org/10.1023/A:1026574828169
Douds, D.D.; Galvez, L.; Bécard, G.; Kapulnik, Y. (1998). Regulation of Arbuscular Mycorrhizal Development by Plant Host and Fungus Species in Alfalfa. New Phytologist. 138: 27-35. https://doi.org/10.1046/j.1469-8137.1998.00876.x
Franken, P.; Requena, N.; Bütehorn, B.; Krajinski, F.; Kuhn, G.; Laponin, L.; Mann, P.; Rhody, D.; Stommel, M. (2000). Molecular Analysis of the Arbuscular Mycorrhizas Symbiosis. Archives of Agronomy and Soil Science. 45: 271-286. https://doi.org/10.1080/03650340009366129
Gadkar, V.; Schwartz, R.; Kunik, T. and Kapulnik, Y. (2001). Arbuscular Mycorrhizal Fungal Colonization. Factors Involved in Host Recognition. Plant Physiology. 127: 1493-1499. https://doi.org/10.1104/pp.010783
García-Garrido, J.M. and Ocampo, J.A. (2002). Regulation of the Plant Defense Response in Arbuscular Mycorrhizal Symbiosis. Journal of Experimental Botany. 53 (373): 1377-1386. https://doi.org/10.1093/jexbot/53.373.1377
García-Garrido, J.M.; Tribak, M.; Rejón-Palomares, A.; Ocampo, J.A.; García-Romero, I. (2000). Hydrolitic Enzymes and Ability of Arbuscular Mycorrhizal Fungi to Colonize Roots. J. of Experimental Botany. 51: 1443-1448. https://doi.org/10.1093/jexbot/51.349.1443
Genre, A.; Chabaud, M.; Timmers, T.; Bonfante, P. and Barkerb, D. (2005). Arbuscular Mycorrhizal Fungi Elicit a Novel Intracellular Apparatus in M. truncatula Root Epidermal Cells before Infection. Plant Cell. 17: 3489-3499. https://doi.org/10.1105/tpc.105.035410
Genre, A.; Chabaud, M.; Faccio, A.; Barker, D. and Bonfante, P. (2008). Prepenetration Apparatus Assembly Precedes and Predicts the Colonization Patterns of Arbuscular Mycorrhizal Fungi within the Root Cortex of Both Medicago truncatula and Daucus carota. The Plant Cell. 20:1407-1420. https://doi.org/10.1105/tpc.108.059014
Gianinazzi-Pearson, V.; Gianinazzi, S.; Guillemin, J.P.; Trouvelot, A.; Duc, G. (1991). Genetic and Cellular Analysis of Resistance to Vesicular Arbuscular (VA) Mycorrhizal Fungi in Pea Mutants. In: Hennecke, H.; Verma, D.P.S. eds. Advances in Molecular Genetics of Plant-microbe Interactions. Dordrecht, Kluwer Acad. Publishers, 336-342. https://doi.org/10.1007/978-94-015-7934-6_52
Gianinazzi-Pearson, V. (1996). Plant Cell Responses to Arbuscular Mycorrhizal Fungi: Getting to the Root of the Symbiosis. Plant Cell. 8: 1871-1883. https://doi.org/10.1105/tpc.8.10.1871
Gianinazzi-Pearson, V. and Dénarié, J. (1997). Red Carpet Genetic Programmes for Root Endosymbiosis. Trends Plant Sci. 2: 371-372. https://doi.org/10.1016/S1360-1385(97)87120-8
Ginzberg, I.; David, R.; Shaul, O.; Elad, Y.; Wininger, S.; Ben-Dor, B.; Badani, H.; Fang, Y.; van Rhijn, P.; Li, Y.; Hirsch, A.; Kapulnik, Y. (1998). Glomus Intraradices Colonization Regulates Gene Expression in Tobacco Roots. Symbiosis. 25; 145 p.
Giovanetti, M.; Sbrana, C.; Citernesi, A.S.; Avio, L. (1996). Analysis of Factors Involved in Fungal Recognition Responses to Host Derived Signals by Arbuscular Mycorrhizal Fungi. New Phytol. 133: 65-71. https://doi.org/10.1111/j.1469-8137.1996.tb04342.x
Guenoune, D.; Galili, S.; Phillips, D.; Volpin, H.; Chet, I.; Okon, Y.; Kapulnik, Y. (2001). The Defense Response Elicited by the Pathogen Rhizoctonia Solani is Suppressed by Colonization of the AMfungus G. Intraradices. Plant Sci. 160: 925-932. https://doi.org/10.1016/S0168-9452(01)00329-6
Harley, J.L. and Smith, S.E. (1983). Mycorrhizal Symbiosis. Academic Press, London Harrison M and Dixon R, 1994. Spation Patterns of Expression of Flavonoid/isoflavonoid Pathway Genes During Interactions Between Roots of Medicago truncatula and the Mycorrhizal Fungus G.versiforme. Plant J. 6: 9-20. https://doi.org/10.1046/j.1365-313X.1994.6010009.x
Harrison, M.J. (2005). Signaling in the Arbuscular Mycorrhizal Symbiosis. Annu Rev Microbiol, 59: 19-42. https://doi.org/10.1146/annurev.micro.58.030603.123749
Harrison, M. (1999). Molecular and Cellular Aspects of the Arbuscular Mycorrhizal Symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 50:361-389. https://doi.org/10.1146/annurev.arplant.50.1.361
Hause, B.; Mrosk, C.; Isayenkov, S. and Dieter, S. (2007). Jasmonates in Arbuscular Mycorrhizal Interactions. Phytochem. 68: 101-110. https://doi.org/10.1016/j.phytochem.2006.09.025
Herbers, K.; Meuwly, P.; Frommer, W.B.; Metraux, J.P.; Sonnewald, U. (1996). Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase, Possible Hexose Sensing in the Secretory Pathway. The Plant Cell. 8: S.P. https://doi.org/10.2307/3870282
Jasper, D.A.; Robson, A.D.; Abbott, L.K. (1979). Phosphorus and the Formation of Vesicular-arbuscular Mycorrhizas. Soil Biology and Biochemistry. 11: 501-505. https://doi.org/10.1016/0038-0717(79)90009-9
Kistner, C.; Winzer, T.; Pitzschke, A.; Mulder, L.; Sato, S.; Kaneko, T.; Tabata, S.; Sandal, N.; Stougaard, J.; Webb, K.J. (2005). Seven Lotus japonicus Genes Required for Transcriptional Reprogramming of the Root During Fungal and Bacterial Symbiosis. Plant Cell. 17: 2217. https://doi.org/10.1105/tpc.105.032714
Kogel, K.H. (2008). Compatible Host-microbe Interactions: Mechanistic Studies Enabling Future Agronomical Solutions. Journal of Plant Physiology. 165: 1-8. https://doi.org/10.1016/j.jplph.2007.08.007
Kosuta, S.; Chabaud, M.; Lougnon, G.; Gough, C.; Dénarié, J.; Barker, D. and Bécard, G. (2003). A Diffusible Factor from Arbuscular Mycorrhizal Fungi Induces Symbiosis-Specific MtENOD11 Expression in Roots of Medicago truncatula. Plant Physiol, 131: 952-962. https://doi.org/10.1104/pp.011882
Lambais, M.R.; Mehdy, M.C. (1998). Spatial Distribution of Chitinases and ß-1,3-Glucanase Transcripts in Bean Arbuscular Mycorrhizal Roots Under Low and High Soil Phosphate Conditions. New Phytologist. 140: 33-42. https://doi.org/10.1046/j.1469-8137.1998.00259.x
Marsh, J. and Shultze, M. (2001). Analysis of Arbuscular Mycorrhizas Using Symbiosis-Defective Plant Mutants. New Phytol. 150: 525-532. https://doi.org/10.1046/j.1469-8137.2001.00140.x
Martínez-Abarca, F.; Herrera-Cervera, J.; Bueno, P.; Sanjuan, J.; Bisseling, T.; Olivares, J. (1998). Involvement of Salicylic Acid in the Establishment of the R. meliloti-Alfalfa Symbiosis. Molecular Plant - Microbe Interaction. 11: 153-155. https://doi.org/10.1094/MPMI.1998.11.2.153
Mathesius, U. (2009). Comparative Proteomic Studies of Root-microbe Interactions Ulrike J. Proteoimics. 72: 353-366. https://doi.org/10.1016/j.jprot.2008.12.006
Oldroyd, G. and Downie, J.A. (2006). Nuclear Calcium Changes at the Core of Symbiosis Signaling. Current Opinion in Plant Biology. 9: 351-357. https://doi.org/10.1016/j.pbi.2006.05.003
Oldroyd, G.; Harrison, M.; Paszkowski, U. (2009). Reprogramming Plant Cells for Endosymbiosis. Science. 324: 753-754. https://doi.org/10.1126/science.1171644
Paszkowski, U. (2006). Mutualism and Parasitism: the Yin and Yang of Plant Symbioses. Curr Opinion in Plant Biol. 2006: 9: 364-37. https://doi.org/10.1016/j.pbi.2006.05.008
Parniske, M. (2000). Intracellular Accommodation of Microbes by Plants: A Common Developmental Program for Symbiosis and Disease? Curr. Opin. Plant Biol. 3: 320-328. https://doi.org/10.1016/S1369-5266(00)00088-1
Parniske, M. (2004). Molecular Genetics of the Arbuscular Mycorrhizal Symbiosis. Curr Opinion Plant Biol. 7: 414- 421. https://doi.org/10.1016/j.pbi.2004.05.011
Parniske, M. (2008). Arbuscular Mycorrhiza: the Mother of Plant Root Endosymbioses. Nat Rev. Microbiol. 6: 10 - 763. https://doi.org/10.1038/nrmicro1987
Pozo, M.J.; Dumas-Gaudot, E.; Slezack, S.; Cordier, C.; Asselin, A.; Gianinazzi, S.; Gianinazzi-Pearson, V.; Azcón-Aguilar, C.; Barea, J.M. (1996). Detection of New Chitinase Isoforms in Arbuscular Mycorrhizal Tomato Roots: Possible Implications in Protection Against Phytophthora nicotianae var. parasitica. Agronomie 16: 689-697. https://doi.org/10.1051/agro:19961014
Pozo, M.J.; Dumas-Gaudot, E.; Azcón-Aguilar, C.; Barea, J.M. (1998). Chitosanase and Chitinase Activities in Tomato Roots During Interactions with Arbuscular Mycorrhizal Fungi or Phytophthora parasitica. J. Exp Bot. 49: 1729-1739. https://doi.org/10.1093/jxb/49.327.1729
Reinhardt, D. (2007). Programming Good Relations-development of the Arbuscular Mycorrhizal Simbiosis. Current Opinion in Plant Biology. 10: 98-105. https://doi.org/10.1016/j.pbi.2006.11.001
Remy, W.; Taylor, T.N.; Hass, H.; Kerp, H. (1994). Four Hundred million Year Old Vesicular Arbuscular Mycorrhizae. Proc Natl Acad Sci USA. 91: 11841-11843. https://doi.org/10.1073/pnas.91.25.11841
Requena, N.; Serrano, E.; Oco'n, A.; Breuninger, M. (2007). Plant Signals and Fungal Perception During Arbuscular Mycorrhizae Establishment. Phytochemistry. 68: 33-40. https://doi.org/10.1016/j.phytochem.2006.09.036
Requena, N.; Mann, P.; Hampp, R.; Franken, P. (2002). Early Developmentally Regulated Genes in the Arbuscular Mycorrhizal Fungus Glomus Mosseae: Identification of GmGin1 a Novel Gene with Homology to the C-terminus of Metazoan Hedgehog Proteins. Plant Soil 244: 129-139. https://doi.org/10.1007/978-94-017-1284-2_13
Salzer, P.; Corbière, H.; Boller, T. (1999). Hydrogen Peroxide Accumulation in Medicago Truncatula Roots Colonized by the Arbuscular Mycorrhizaforming Fungus Glomus Mosseae. Planta 208: 319-325. https://doi.org/10.1007/s004250050565
Salzer; P.; Boller, T. (2000). Elicitor Induced Reactions in Mycorrhizae and their Suppression. In: Podila, G.K.; Douds, D.D. eds. Current Advances in Mycorrhizae Research. APS Press, St. Paul, pp. 1-10.
Shaul, O.; David, R.; Sinvani, G.; Ginzberg, I.; Ganon, D.; Wininger, S.; Ben-Dor, B.; Badani, H.; Ovdat, N.; Kapulnik, Y. (2000). Plant Defense Responses During Arbuscular Mycorrhizal Symbiosis. In: Podila, G.K.; Douds, D.D. eds, Current Advances in Mycorrhizae Research. APS Press, St. Paul, MN, pp. 61-68.
Shinshi, H.; Mohnen, D.; Meins, F. (1987). Regulation of a Plant Pathogenesisrelated Enzyme: Inhibition of Chitinase and Chitinase mRNA Accumulation in Cultured Tobacco Tissues by Auxin and Cytokinin. Proceedings of the National Academy of Sciences, USA. 84: 89-93. https://doi.org/10.1073/pnas.84.1.89
Siqueira, J.O.; Nair, M.G.; Hammerschmidt, R.; Safir, G.R. (1991). Significance of Phenolic Compounds in Plant Soil Microbial Systems. Crit Rev Plant Science. 10: 63-121. https://doi.org/10.1080/07352689109382307
Smith, S.E. and Gianinazzi-Pearson, V. (1988). Physiological Interactions Between Symbionts in Vesicular-arbuscular Mycorhiza Plants. Ann Rev. Plant Physiol. Plant Mol. Biol. 39: 221-244. https://doi.org/10.1146/annurev.pp.39.060188.001253
Smith, S.D. and Read, D.J. (2008). Mycorrhizal Symbiosis. (Ed 3). Academic Press. Somssich, I.
Hahlbrock, K. (1998) Pathogen Defense in Plants: a Paradigm of Biological Complexity. Trends in Plant Sci. 3: 86-90. https://doi.org/10.1016/S1360-1385(98)01199-6
Spanu, P.; Bonfante-Fasolo, P. (1988). Cell Wall-bound Peroxidase Activity in Roots of Mycorrhizal Allium porrum. New Phytologist. 109: 119-124. https://doi.org/10.1111/j.1469-8137.1988.tb00226.x
Van der Heijden and Sanders, I. (2002). Mycorrhizal Ecology. Ecologycal Studies 157. Springer Ed. 469 p. https://doi.org/10.1007/978-3-540-38364-2_17
Vierheilig, H.; Alt, M.; Mohr, U.; Boller, T.; Wiemken, A. (1994). Ethylene Biosynthesis and Activities of Chitinase and ß-1,3-Glucanase in the Roots of Host and Non-host Plants of Vesicular-arbuscular Mycorrhizal Fungi After Inoculation with Glomus mosseae. J. of Plant Physiology. 143: 337-343. https://doi.org/10.1016/S0176-1617(11)81641-X
Vierheilig, H.; Piché, Y. (2002). Signaling in Arbuscular Mycorrhiza: Facts and Hypotheses. In: Manthey, J.; Buslig, B. eds. Flavonoids in the Living System. New York: Plenum Press. https://doi.org/10.1007/978-1-4757-5235-9_3
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