Metabolitos Sintetizados en la Simbiosis Micorrícica: De la Raíz a las Partes Aéreas

Palabras clave: hongos micorrícicos arbusculares, estrés, metabolitos

Resumen

Los hongos micorrícicos arbusculares (HMA) forman la asociación simbiótica más frecuente (80%) con las raíces de las plantas terrestres. Esta relación se establece mediante un diálogo de señalización que comienza en el suelo, induciendo cambios fisiológicos en toda la planta. Tras el contacto físico entre las hifas fúngicas y la raíz, los HMA desarrollan estructuras especializadas dentro de las células corticales. Posteriormente, la colonización interna del hongo facilita el intercambio de nutrientes entre ambos organismos. Hace tres décadas, se descubrió que la inoculación con HMA aumenta los niveles de ciertos aminoácidos y proteínas solubles, lo que demuestra que esta asociación simbiótica altera significativamente el metabolismo de la planta. Durante la simbiosis, los compuestos sintetizados como respuesta defensiva a la presencia del hongo pueden inducir cambios en los metabolitos secundarios y los compuestos bioactivos en diversos tejidos vegetales. Esta revisión describe cómo se activan los metabolitos en respuesta a los HMA, así como su función ante estímulos adicionales como el estrés abiótico y biótico.

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Aliferis, K. A., Chamoun, R. and Jabaji, S. (2015). Metabolic responses of willow (Salix purpurea L.) leaves to mycorrhization as revealed by mass spectrometry and 1H NMR spectroscopy metabolite profiling. Frontiers Plant Science, 6(344), doi: 10.3389/fpls.2015.00344

Asensio, D., Rapparini, F. and Peñuelas, J. (2012). AM fungi root colonization increases the production of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77: 149-161. http://dx.doi.org/10.1016/j.phytochem.2011.12.012.

Brundrett, M. C. (2009). Mycorrhizal associations and other means of nutrition of vascular plants: Understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil, 320(1-2), 37-77. https://doi.org/10.1007/s11104-008-9877-9.

Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R. and Bécard, G. (2000). The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Molecular Plant Microbe Interactions, 13(6), 693-698. https://doi:10.1094/MPMI.2000.13.6.693 )

Ceccarelli, N., Curadi, M., Martelloni, L., Sbrana, C., Picciarelli, P. and Giovannetti, M. (2010). Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant and Soil, 335(1), 311-323. https://doi.org/10.1007/s11104-010-0417-z.

Charest, C., Dalpé, Y. and Brown, A. (1993). The effect of vesicular-arbuscular mycorrhizae and chilling on two hybrids of Zea mays L. Mycorrhiz,. 4(1), 89-92. https://doi.org/10.1007/BF00204064.

Chen, X., Song, F., Liu, F., Tian, C., Liu, S., Xu, H. and Zhu, X. (2014). Effect of different arbuscular mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes. The Scientific World Journal, 2014(956141), 1-7. http://dx.doi.org/10.1155/2014/956141.

De Deyn, G. B., Biere, A., van der Putten, W. H., Wagenaar, R. and Klironomos, J. N. (2009). Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia, 160(3), 433-442. https://doi.org/10.1007/s00442-009-1312-2.

Dhawi, F., Datta, R. and Ramakrishna, W. (2016). Mycorrhiza and heavy metal resistant bacteria enhance growth, nutrient uptake and alter metabolic profile of sorghum grown in marginal soil. Chemosphere, 157, 33-41. https://doi.org/10.1016/j.chemosphere.2016.04.11.2

Duhamel, M., Pel, R., Ooms, A., Bücking, H., Jansa, J., Ellers, J., van Straalen, N. M., Wouda, T., Vandenkoornhuyse, P. and Kiers, E. T. (2013). Do fungivores trigger the transfer of protective metabolites from host plants to arbuscular mycorrhizal hyphae? Ecology, 94(9), 2019-2029. http://www.jstor.org/stable/23597324

Dumas, E., Gianinazzi-Pearson, V. and Gianinazzi, S. (1990). Production of new soluble proteins during VA endomycorrhiza formation. Agriculture, Ecosystems & Environment, 29(1-4): 111-114. https://doi.org/10.1016/0167-8809(90)90264-E.

Eftekhari, M., Alizadeh, M. and Ebrahimi, P. (2012). Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetin yield. Industrial Crops and Products, 38(1), 160-165. https://doi.org/10.1016/j.indcrop.2012.01.022.

Engel, R., Szabó, K., Abrankó, L., Rendes, K., Füzy, A. and Takács, T. (2016). Effect of arbuscular mycorrhizal fungi on the growth and polyphenol profile of marjoram, lemon balm, and marigold. Journal of Agricultural and Food Chemistry, 64(19), 3733-3742. http://dx.doi.org/10.1021/acs.jafc.6b00408.

Evelin, H. and Kapoor, R. (2014). Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza, 24(3), 197-208. https://doi.org/10.1007/s00572-013-0529-4.

Fester, T., Fetzer, I., Buchert, S., Lucas, R., Rillig, M. C. and Härtig, C. (2011). Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction. Oecologia, 167(4): 913-924. DOI 10.1007/s00442-011-2037-6.

Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J. and Unsicker, S. B. (2009). The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. Journal of Chemical Ecology, 35(7), 833–843. DOI 10.1007/s10886-009-9654-0.

Gange, A. C. (2001). Species-specific responses of a root and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytologist, 150(3), 611–618. https://doi.org/10.1046/j.1469-8137.2001.00137.x.

Garg, N. and Manchanda, G. (2009). Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea). Journal of Agronomy and Crop Science, 195(2), 110-123. https://doi.org/10.1111/j.1439-037X.2008.00349.x

Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Bécard, G., Bonfante, P. and Barker, D. G. (2013). Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytologist, 198(1), 190-202. https://doi:10.1111/nph.12146.

Gerlach, N., Schmitz, J., Polatajko, A., Schlüter, U., Fahnenstich, H., Witt, S., Fernie, A. R., Uroic, K., Scholz, U., Sonnewald, U. and Bucher, M. (2015). An integrated functional approach to dissect systemic responses in maize to arbuscular mycorrhizal symbiosis. Plant, Cell and Environment, 38(8), 1591-1612. https://doi.org/10.1111/pce.12508.

Gough, C. and Cullimore, J. (2011). Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Molecular plant-microbe interactions : MPMI, 24(8), 867-878. https://doi.org/10.1094/mpmi-01-11-0019.

Hajiboland, R., Aliasgharzadeh, N., Laiegh, S. F. and Poschenrieder, C. (2010). Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant and Soil, 331(1), 313–327. https://doi.org/10.1007/s11104-009-0255-z.

Hodge, A. and A.H. Fitter. (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences of the United States of America, 107(31), 13754-13759. https://doi.org/10.1073/pnas.1005874107.

Hubberten, H. M., Sieh, D., Zöller, D., Hoefgen, R. and Krajinski, F. (2015). Medicago truncatula Mtha1-2n mutants loose metabolic responses to mycorrhizal colonization. Plant Signaling & Behavior, 10(6), e989025. https://doi.org/10.4161/15592324.2014.989025.

Jurkiewicz, A., Ryszka, P., Anielska, T., Waligórski, P., Białońska, D., Góralska, K., Tsimilli-Michael, M. and Turnau, K. (2010). Optimization of culture conditions of Arnica montana L.: Effects of mycorrhizal fungi and competing plants. Mycorrhiza, 20(5), 293-306. https://doi.org/10.1007/s00572-009-0280-z

Kapoor, R., Chaudhary, V. and Bhatnagar, A. K. (2007). Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza, 17(7), 581–587. https://doi.org/10.1007/s00572-007-0135-4.

Kee, Y. J., Ogawa, S., Ichihashi, Y., Shirasu, K. and Yoshida, S. (2023). Strigolactones in rhizosphere communication: multiple molecules with diverse functions. Plant and Cell Physiology, 64(9), 955-966. https://doi:10.1093/pcp/pcad055.

Kempel, A., Schmidt, A. K., Brandl, R. and Schädler, M. (2010). Support from the underground: Induced plant resistance depends on arbuscular mycorrhizal fungi. Functional Ecology, 24(2), 293–300. https://doi.org/10.1111/j.1365-2435.2009.01647.x.

Kogel, K. H., Voll, L.M., Schäfer, P., Jansen, C., Wu, Y., Langen, G., Imani, J., Hofmann, J., Schmiedl, A., Sonnewald, S., von Wettstein, D., Cook, R. J. and Sonnewald, U. (2010). Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific variances. Proceedings of the National Academy of Sciences of the United States of America, 107(14), 6198–6203. https://doi.org/10.1073/pnas.1001945107.

Laparre, J., Malbreil, M., Letisse, F., Portais, J. C., Roux, C., Bécard, G. and Puech-Pagès, V. (2014). Combining metabolomics and gene expression analysis reveals that propionyl- and butyryl-carnitines are involved in late stages of arbuscular mycorrhizal symbiosis. Molecular Plant, 7(3), 554–566. https://doi.org/10.1093/mp/sst136.

Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C. D. and Harrison, M. J. (2007). Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. The Plant Journal 50(3), 529–544. https://doi.org/10.1111/j.1365-313X.2007.03069.x.

Lohse, S., Schliemann, W., Ammer, C., Kopka, J., Strack, D. and Fester, T. (2005). Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant physiology, 139(1), 329-340. https://doi.org/10.1104/pp.105.061457.

López-Ráez, J. A., Verhage, A., Fernández, I., García, J. M., Azcón-Aguilar, C., Flors, V. and Pozo M. J. (2010). Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. Journal of Experimental Botany, 61(10), 2589–2601. https://doi.org/10.1093/jxb/erq089.

Mechri, B., Attia, F., Tekaya, M., Cheheb, H. and Hammami, M. (2014). Colonization of olive trees (Olea europaea L.) with the arbuscular mycorrhizal fungus Glomus sp. modified the glycolipids biosynthesis and resulted in accumulation of unsaturated fatty acids. Journal of Plant Physiology, 171(14), 1217–1220. https://doi.org/10.1016/j.jplph.2014.04.005.

Nair, A., Kolet, S. P., Thulasiram, H. V. and Bhargava, S. (2015). Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biology, 17(3), 625-631. https://doi.org/10.1111/plb.12277.

Nell, M., Wawrosch, C., Steinkellner, S., Vierheilig, H., Kopp, B., Lössl, A., Franz, C., Novak, J., Zitterl-Eglseer, K. (2010). Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Medica, 76(4), 393-398. https://doi.org/10.1055/s-0029-1186180.

Oldroyd, G.E.D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature reviews Microbiology, 11(4), 252-263. https://doi.org/10.1038/nrmicro2990.

Pacovsky, R. S. (1989). Carbohydrate, protein and amino acid status of Glycine-Glomus-Bradyrhizobium symbioses. Physiologia Plantarum, 75(3), 346–354. https://doi.org/10.1111/j.1399-3054.1989.tb04637.x.

Pandey D. K., Malik T., Dey, A., Singh J, and Banik R. M. (2014). Improved growth and colchicine concentration in Gloriosa superba on mycorrhizal inoculation supplemented with phosphorus-fertilizer. African Journal of Traditional, Complementary and Alternative Medicines, 11(2), 439-446. https://doi.org/10.4314/ajtcam.v11i2.30.

Pedone-Bonfim, M.V.L., Lins, M. A., Coelho, I. R., Santana, A. S., Silva, F. S. B. and Maiaa, L. C. (2012). Mycorrhizal technology and phosphorus in the production of primary and secondary metabolites in cebil (Anadenanthera colubrina ( Vell .) Brenan ) seedlings. Journal of the Science of Food Agriculture, 93(6), 1479-1484. https://doi.org/10.1002/jsfa.5919.

Rasouli-Sadaghiani, M., Hassani, A., Barin, M., Danesh, Y. R. and Sefidkon, F. (2010). Effects of arbuscular mycorrhizal (AM) fungi on growth, essential oil production and nutrients uptake in basil. Journal of Medicinal Plants Research, 4(21), 2222–2228. https://doi.org/10.5897/JMPR10.337

Redecker, D., Kodner, R. and Graham, L. E. (2000). Glomalean fungi from the Ordovician. Science, 289(5486), 1920-1921. https://doi.org/10.1126/science.289.5486.1920.

Ribeiro da Luz, R. de C., Wu, Q-S., Albanez Bastos-Filho, C. J., Alves da Silva, F. and Barbosa da Silva, F. S. (2023) Entrophospora etunicata: A mycorrhizal biostimulant with the potential to enhance the production of bioactive health-promoting compounds in leaves of Capsicum chinense seedlings, Rhizosphere, 28, 100791, https://doi.org/10.1016/j.rhisph.2023.100791.

Rivero, J., Gamir, J., Aroca, R., Pozo, M. J. and Flors, V. (2015). Metabolic transition in mycorrhizal tomato roots. Frontiers in Microbiology, 6(598), 1-13. https://doi.org/10.3389/fmicb.2015.00598.

Rozpądek, P., Wężowicz, K., Stojakowska, A., Malarz, J., Surówka, E., Sobczyk, T., Anielska, T., Ważny, R., Miszalski, Z. and Turnau, K. (2014). Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere, 112, 217-224. https://doi.org/10.1016/j.chemosphere.2014.04.023.

Rush, T.A., Puech-Pagès, V., Bascaules, A., Jargeat, P., Maillet, F., Haouy, A., Maës, A. Q., Carrera Carriel, C., Khokhani, D., Keller-Pearson, M., Tannous, J., Cope, K. R., Garcia, K., Maeda, J., Johnson, C., Kleven, B., Choudhury, Q. J., Labbé, J., Swift, C., O’Malley, M. A., Bok, J. W., Cottaz, S., Fort, S., Poinsot, V., Sussman, M. R., Lefort, C., Nett, J., Keller, N. P., Bécard, G. and Ané, J-M.o (2020). Lipo-chitooligosaccharides as regulatory signals of fungal growth and development. Nature Communications, 11, 3897. doi:10.1038/s41467-020-17615-5.

Saia, S., Ruisi, P., Fileccia, V., Di Miceli, G., Amato, G. and Martinelli, F. (2015). Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N-Limited, P-Rich field conditions. Plos One, 10(6), e0129591. https://doi.org/10.1371/journal.pone.0129591.

Salvioli, A., Zouari, I., Chalot, M. and Bonfante, P. (2012). The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biology, 12(1), 44. http://www.biomedcentral.com/1471-2229/12/44.

Sardans, J., Peñuelas, J. and Rivas-Ubach, A. (2011). Ecological metabolomics: Overview of current developments and future challenges. Chemoecology, 21, 191–225. https://doi.org/10.1007/s00049-011-0083-5.

Schliemann, W., Ammer, C. and Strack, D. (2008). Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry, 69(1), 112–146. https://doi.org/10.1016/j.phytochem.2007.06.032.

Schweiger, R., Baier, M. C., Persicke, M. and Müller, C. (2014). High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nature communications, 5, 3886. https://doi.org/10.1038/ncomms4886.

Schweiger, R. and Müller, C. (2015). Leaf metabolome in arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology, 26, 120-126. https://doi.org/10.1016/j.pbi.2015.06.009.

Silva, F. A., Ferreira, M. R. A., Soares, L. A. L., Sampaio, E. V. S. B., Silva, F. S. B. and Maia, L. C. (2014). Arbuscular mycorrhizal fungi increase gallic acid production in leaves of field grown Libidibia ferrea. (Mart. ex Tul.) L. P. Queiroz. Journal of Medicinal Plant Research, 8(36), 1110-1115. http://dx.doi.org/10.5897/JMPR2013.5503.

Selosse, M. A. and Le Tacon, F. (1998). The land flora: A phototroph-fungus partnership?. Trends in Ecology and Evolution, 13(1), 15-20. https://doi.org/10.1016/S0169-5347(97)01230-5.

Sheng, M., Tang, M., Zhang, F. and Huang, Y. (2011). Influence of arbuscular mycorrhiza on organic solutes in maize leaves under salt stress. Mycorrhiza, 21(5), 423-430. https://doi.org/10.1007/s00572-010-0353-z.

Song, Y.Y., Cao, M., Xie, L. J., Liang, X. T., Zeng, R. S., Su, Y. J., Huang, J. H., Wang, R. L. and Luo, S. M. (2011). Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza, 21(8), 721-731. https://doi.org/10.1007/s00572-011-0380-4.

Song, Y., Chen, D., Lu, K., Sun, Z. and Zeng, R. (2015). Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science, 6(786), 1-13. https://doi.org/10.3389/fpls.2015.00786.

Song, Y. Y., Ye, M., Li, C. Y., Wang, R. L., Wei, X. C., Luo, S. M. and Zeng, R. S. (2013). Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. Journal of Chemical Ecology, 39(7), 1036-1044. https://doi.org/10.1007/s10886-013-0312-1.

Souza, L. A., Camargos, L. S.,. Schiavinato, M. A and Andrade, S. A. L. (2014). Mycorrhization alters foliar soluble amino acid composition and influences tolerance to Pb in Calopogonium mucunoides. Theoretical and Experimental Plant Physiology, 26(3-4), 211–216. https://doi.org/10.1007/s40626-014-0019-x.

Tominaga, T., Ueno, K., Saito, H., Egusa, M., Yamaguchi, K., Shigenobu, S. and Kaminaka, H. (2023). Monoterpene glucosides in Eustoma grandiflorum roots promote hyphal branching in arbuscular mycorrhizal fungi. Plant Physiology, 193(4), 2677-2690. https://doi:10.1093/plphys/kiad482.

Toussaint, J., Smith, F. A. and Smith, S. E. (2007). Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza, 17, 291-297 https://doi.org/10.1007/s00572-006-0104-3.

Vannette, R.L., Hunter, M. D. and Rasmann, S. (2013). Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species. Frontiers in Plant Science. 4, 361. https://doi.org/10.3389/fpls.2013.00361.

Wang, B., Yeun, L. H., Xue, J. Y., Liu, Y., Ané, J. M. and Qiu, Y. L. (2010). Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytologist, 186(2), 514-525. https://doi.org/10.1111/j.1469-8137.2009.03137.x.

Wewer, V., Brands, M. and Dӧrmann, P. (2014). Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. The Plant Journal, 79(3), 398-412. https://doi.org/10.1111/tpj.12566.

Yin, B., Wang, Y., Liu, P., Hu, J. and Zhen, W. (2010). Effects of vesicular-arbuscular mycorrhiza on the protective system in strawberry leaves under drought stress. Frontiers of Agriculture in China, 4(2): 165-169. https://doi.org/10.1007/s11703-010-0109-8.

Zhu, X., Song, F. and Liu, S. (2011). Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. Journal of Food, Agriculture and Environment, 9(2), 583-587.

Zhu, X. C., Song, F. B. and Xu, H. W. (2010). Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant and Soil, 331(1), 129-137. https://doi.org/10.1007/s11104-009-0239-z.

ZhongQun, H., ChaoXing, H., ZhiBin, Z., ZhiRong, Z. and HuaiSong, W. (2007). Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids and Surfaces B: Biointerfaces, 59(2), 128–133. https://doi.org/10.1016/j.colsurfb.2007.04.023 .

Zouari, I., Salvioli, A., Chialva, M., Novero, M., Miozzi, L., Tenore, G. C., Bagnaresi, P. and Bonfante, P. (2014). From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC genomics, 15(1), 221. https://doi.org/10.1186/1471-2164-15-221.

Zubek, S., Mielcarek, S. and Turnau, K. (2012). Hypericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi. Mycorrhiza, 22(2), 149-156. https://doi.org/10.1007/s00572-011-0391-1.

Zubek, S., Stojakowska, A., Anielska, T. and Turnau, K. (2010). Arbuscular mycorrhizal fungi alter thymol derivative contents of Inula ensifolia L. Mycorrhiza, 20(7), 497-504. https://doi.org/10.1007/s00572-010-0306-6.

Publicado
2026-06-18
Cómo citar
Casarrubias Castillo, K., Plancarte de la Torre, M. M., Ramírez Briones, E., & Zañudo Hernández, J. (2026). Metabolitos Sintetizados en la Simbiosis Micorrícica: De la Raíz a las Partes Aéreas. Ciencia Latina Revista Científica Multidisciplinar, 10(3), 2981-3009. https://doi.org/10.37811/cl_rcm.v10i3.24283
Sección
Ciencias y Tecnologías