Poblaciones microbianas y su contribución en la generación de suelos supresivos - Covarrubias, Sergio Abraham; Barrera-Galicia, Guadalupe C.; Martínez-Acuña, Mónica Imelda; Cardoso-Ortiz, Jaime; Flores de la Torre, Juan Armando (ECOAgropecuaria. Revista Científica Ecológica Agropecuaria, 2024)
En los agroecosistemas, el suelo es esencial para todos los cultivos, siendo el principal soporte de las raíces y la fuent-e de nutrientes para las plantas. El suelo es además el hábitat de microorganismos que pueden llegar a tener efectos tanto benéficos como perjudiciales para las plantas. Los suelos supresivos (SS) son quizás el mejor ejemplo para describir la compleja interacción entre las plantas y su microbioma. En un SS la incidencia y severidad de las infecciones permanecen bajas aun en las condiciones adecuadas para su desarrollo. Existen dos tipos de supresión en los SS: general, donde toda la comunidad microbiana actúa en conjunto, y específica, donde ciertos taxones microbianos o grupos antagonistas dirigen la supresión. El efecto antagónico de los SS se debe a los diversos mecanismos como: la competencia por nutrientes, producción de compuestos antimicrobianos, compuestos orgánicos volátiles (VOCs) e inducción de resistencia sistémica. En las últimas décadas, gracias a las tecnologías ómicas, la naturaleza microbiana de la supresión ha sido ampliamente demostrada. Sin embargo, potenciar la formación de suelos supresivos sigue representando un reto en términos del manejo sustentable de dicho recurso natural. Por ello, en la presente revisión se busca brindar un panorama actual sobre el papel de las comunidades microbianas en la formación de suelos supresivos. Referencias Abd-Elmonsef Mahmoud, G. (2021). Biotic stress to legumes: fungal diseases as major biotic stress factor. En Sustainable Agriculture Reviews 51: Legume Agriculture and Biotechnology (Vol. 51, pp. 181-212). Springer Nature Switzerland AG. https://doi.org/10.1007/978-3-030-68828-8_7 Alabouvette, C., Couteaudier, Y., Louvet, J., Bremeersch, P., Richard, P., and Soulas, M. L. (1985). Recherches sur la resistance des sols aux maladies. XI. Etude comparative du comportement des Fusarium spp. dans un sol résistant et un sol sensible aux fusarioses vasculaires enrichis en glucose. Agronomie, 5, 63-68. http://doi: 10.1051/ agro:19850109 Alfano, G., Lustrato, G., Lima, G., Vitullo, D., Ranalli G. (2011). Characterization of composted olive mill wastes to predict potential plant disease suppressiveness. Biological control, 58(3), 199-207 Arseneault, T., and Filion, M. (2017). Biocontrol through antibiosis: Exploring the role played by subinhibitory concentrations of antibiotics in soil and their impact on plant pathogens. Canadian Journal of Plant Pathology, 39(3), 267-274. https://doi.org/10.1080/07060661.2017.1354335 Arseneault, T., Goyer, C., and Filion, M. (2013). Phenazine production by Pseudomonas sp. LBUM223 contributes to the biological control of potato common Scab. Phytopathology®, 103(10), 995-1000. https://doi.org/10.1094/PHYTO-01-13-0022-R Akhter, A., Hage-Ahmed, K., Soja, G., and Steinkellner, S. (2015). Compost and biochar alter mycorrhization, tomato root exudation and development of Fusarium oxysporum f. sp. lycopersici. Frontiers in Plant Science, 6(529), 1-13. http//doi:10.3389/fpls.2015.00529 Bakker, P. A. H. M., Doornbos, R. F., Zamioudis, C., Berendsen, R. L., and Pieterse, C. M. J. (2013). Induced systemic resistance and the rhizosphere microbiome. The Plant Pathology Journal, 29(2), 136-143. https://doi.org/10.5423/PPJ.SI.07.2012.0111 Bongiorno, G., Postma, J., Bünemann E. K., Brussaard, L., de Goede R. G. M., Mäder, P., Tamm, L., Thuerig, B. (2019). Soil Suppressiveness to Pythium ultimum in ten European long-term field experiments and its relation with soil parameters. Soil Biology and Biochemistry, 133, 147-187. https://doi.org/10.1016/j.soilbio.2019.03.012 Carrión, V. J., Cordovez, V., Tyc, O., Etalo, D. W., de Bruijn, I., de Jager, V. C. L., Medema, M. H., Eberl, L., and Raaijmakers, J. M. (2018). Involvement of Burkholderiaceae and sulfurous volatiles in disease-suppressive soils. The ISME Journal, 12(9), 2307-2321. https://doi.org/10.1038/s41396-018-0186-x Chapelle, E., Mendes, R., Bakker, P. A. H. M., and Raaijmakers, J. M. (2016). Fungal invasion of the rhizosphere microbiome. The ISME Journal, 10(1), 265-268. https://doi.org/10.1038/ismej.2015.82 Chialva, M., Salvioli di Fossalunga, A., Daghino, S., Ghignone, S., Bagnaresi, P., Chiapello, M., Novero, M., Spadaro, D., Perotto, S., and Bonfante, P. (2018). Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytologist, 220(4), 1296-1308. https://doi.org/10.1111/nph.15014 Choudhary, D. K., and Johri, B. N. (2009). Interactions of Bacillus spp. and plants – with special reference to induced systemic resistance (ISR). Microbiological Research, 164(5), 493-513. https://doi.org/10.1016/j.micres.2008.08.007 Choudhary, D. K., Prakash, A., and Johri, B. N. (2007). Induced systemic resistance (ISR) in plants: Mechanism of action. Indian Journal of Microbiology, 47(4), 289-297. https://doi.org/10.1007/s12088-007-0054-2 Cook, R. J. (2014). Plant health management: pathogen suppressive soils. En Encyclopedia of Agriculture and Food Systems (pp. 441-455). Elsevier, London, UK. https://doi.org/10.1016/B978-0-444-52512-3.00182-0 De Coninck, B., Timmermans, P., Vos, C., Cammue, B. P. A., and Kazan, K. (2015). What lies beneath: Belowground defense strategies in plants. Trends in Plant Science, 20(2), 91-101. https://doi.org/10.1016/j.tplants.2014.09.007 De Corato, U. (2019). Use of omic approaches for characterizing microbiota from suppressive compost to control soil-borne plant pathogens. Archives of Phytopathology and Plant Protection, 52(7-8), 757-775. https://doi.org/10.1080/03235408.2018.1554199 Döring, T. F., Rosslenbroich, D., Giese, C., Athmann, M., Watson, C., Vágó, I., Kátai, J., Tállai, M., and Bruns, C. (2020). Disease suppressive soils vary in resilience to stress. Applied Soil Ecology, 149(103482), 1-7. https://doi.org/10.1016/j.apsoil.2019.103482 Du, S., Trivedi, P., Wei, Z., Feng, J., Hu, H.-W., Bi, L., Huang, Q., and Liu, Y.-R. (2022). The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils. mSystems, 7(2), e01337-21. https://doi.org/10.1128/msystems.01337-21 Fierer, N., Wood, S. A., and Bueno de Mesquita, C. P. (2021). How microbes can, and cannot, be used to assess soil health. Soil Biology and Biochemistry, 153(108111). https://doi.org/10.1016/j.soilbio.2020.108111 Garbeva, P., van Veen, J. A., and van Elsas, J. D. (2004). Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annual Review of Phytopathology, 42(1), 243-270. https://doi.org/10.1146/annurev.phyto.42.012604.135455 Gómez Expósito, R., de Bruijn, I., Postma, J., and Raaijmakers, J. M. (2017). current insights into the role of rhizosphere bacteria in disease suppressive soils. Frontiers in Microbiology, 8(2529), 1-12. https://doi.org/10.3389/fmicb.2017.02529 Gu, S., Yang, T., Shao, Z., Wang, T., Cao, K., Jousset, A., Friman, V. P., Mallon, C., Mei, X., Wei, Z., Xu, Y., Shen, Q., and Pommier, T. (2020). Siderophore-mediated interactions determine the disease suppressiveness of microbial consortia. mSystems, 5(3), e00811-19. https://doi.org/10.1128/mSystems.00811-19 Heil, M., and Bostock, R. (2002). Induced systemic resistance (ISR) against pathogens in the context of induced plant defences. Annals of Botany, 89(5), 503-512. https://doi.org/10.1093/aob/mcf076 González-Hernández A. I., Suárez-Fernández M. B., Pérez-Sánchez R., Gómez-Sánchez M. Á., Morales-Corts M. R. (2021). Compost tea induces growth and resistance against Rhizoctonia solani and Phytophthora capsici in pepper. Agronomy, 11(4), 1-12. https://doi.org/10.3390/agronomy11040781 Hu, W., Gao, Q., Hamada, M. S., Dawood, D. H., Zheng, J., Chen, Y., and Ma, Z. (2014). Potential of Pseudomonas chlororaphis subsp. aurantiaca strain pcho10 as a biocontrol agent against Fusarium graminearum. Phytopathology, 104(12), 1289-1297. https://doi.org/10.1094/PHYTO-02-14-0049-R Jayaraman, S., Naorem, A. K., Lal, R., Dalal, R. C., Sinha, N. K., Patra, A. K., and Chaudhari, S. K. (2021). Disease-suppressive soils—beyond food production: A critical review. Journal of Soil Science and Plant Nutrition, 21(2), 1437-1465. https://doi.org/10.1007/s42729-021-00451-x Kibblewhite, M. G., Ritz, K., and Swift, M. J. (2008). Soil health in agricultural systems. Philosophical Transactions of the Royal Society B: Biological Sciences, 363(1492), 685-701. https://doi.org/10.1098/rstb.2007.2178 Kopittke, P. M., Menzies, N. W., Wang, P., McKenna, B. A., and Lombi, E. (2019). Soil and the intensification of agriculture for global food security. Environment International, 132(105078), 1-8. https://doi.org/10.1016/j.envint.2019.105078 Kopecky, J., Samkova, Z., Sarikhani, E., Kyselková, M., Omelka, M., Kristufek, V., Divis. J., Grundmann, G. G., Moënne-Loccoz, Y., and Sagova-Mareckova, M. (2019). Bacterial, archaeal and micro-eukaryotic communities characterize a disease-suppressive or conducive soil and a cultivar resistant or susceptible to common scab. Sci Rep, 9(14883), 1-14. https://doi.org/10.1038/s41598-019-51570-6 Kwak, Y. S., and Weller, D. M. (2013). Take-all of wheat and natural disease suppression: A review. The Plant Pathology Journal, 29(2), 125-135. https://doi.org/10.5423/PPJ.SI.07.2012.0112 Le, K. D., Yu, N. H., Park, A. R., Park, D. J., Kim, C. J., Kim, J. C. (2022). Streptomyces sp. AN090126 as a biocontrol agent against bacterial and fungal plant diseases. Microorganisms, 10(4), 1-15. https://doi.org/10.3390/ microorganisms10040791 Liu, H., Li, J., Carvalhais, L. C., Percy, C. D., Prakash Verma, J., Schenk, P. M., and Singh, B. K. (2021). Evidence for the plant recruitment of beneficial microbes to suppress soil-borne pathogens. The New Phytologist, 229(5), 2873-2885. https://doi.org/10.1111/nph.17057 Lucas, P. (2006). Diseases caused by soil-borne pathogens. En B. M. Cooke, D. G. Jones, and B. Kaye (Eds.), The Epidemiology of Plant Diseases (2nd ed., pp. 373-386). Mazzola, M. (2002). Mechanisms of natural soil suppressiveness to soilborne diseases. Antonie van Leeuwenhoek, 8, 557-564. https://doi.org/10.1023/A:1020557523557 Mazzola, M. (2007). Manipulation of rhizosphere bacterial communities to induce suppressive soils. Journal of nematology, 39(3), 213-220 Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J. H. M., Piceno, Y. M., DeSantis, T. Z., Andersen, G. L., Bakker, P. A. H. M., and Raaijmakers, J. M. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332(6033), 1097-1100. https://doi.org/10.1126/science.1203980 Mengesha, W. K., Powelli, S. M., Evans, K. J., and Barry, K. M. (2017). Diverse microbial communities in non-aerated compost teas suppress bacterial wilt. World Journal of Microbiological Biotechnology, 33(49), 1-14. doi: 101007/s11274-017-2212-y Mitchell, A. M., Strobel, G. A., Moore, E., Robison, R., and Sears, J. (2010). Volatile antimicrobials from Muscodor crispans, a novel endophytic fungus. Microbiology, 156(1), 270-277. https://doi.org/10.1099/mic.0.032540-0 Mukherjee, P. K., Mendoza-Mendoza A., Zeilinger, S., and Horwitz B. A. (2022). Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biology Reviews, 39, 15-33. https://doi.org/10.1016/j.fbr.2021.11.004 Noble, R., Roberts, S. J. (2004). Eradication of plant pathogens and nematodes during composting: a review. Plant Pathol, 53(5), 548–568. https://doi.org/10.1111/j.0032-0862.2004.01059.x Palojärvi1, A., Kellock, M., Parikka P., Jauhiainen, L., Alakukku, L.(2020). Tillage system and crop sequence affect soil disease suppressiveness and carbon status in boreal climate. Frontier in Microbiolgy, 11, 534786. https://doi.org/10.3389/fmicb.2020.534786 Raaijmakers, J. M., and Mazzola, M. (2016). Soil immune responses. Science, 352(6292), 1392-1393. https://doi.org/10.1126/science.aaf3252 Raaijmakers, J. M., Vlami, M., and de Souza, J. T. (2002). Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81, 537-547. https://doi.org/10.1023/A:1020501420831 Rana, A., Sudakov, K., Carmeli, S., Miyara, S. B., Bucki, P., and Minz, D. (2024). Volatile organic compounds of the soil bacterium Bacillus halotolerans suppress pathogens and elicit defense-responsive genes in plants. Microbiological Research, 281(127611), 1-8. https://doi.org/10.1016/j.micres.2024.127611 Rudrappa T., Czymmek K. J., Pare P. W., and Bais H. P. (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148(3),1547–1556. https://doi.org/10.1104/pp.108.127613 Sagova-Mareckova, M., Omelka, M., and Kopecky, J. (2022). The golden goal of soil manegement: Disease-Suppresive soils. Phytopathology, 113(4), 741-752. https://doi.org/10.1094/PHYTO-09-22-0324-KD Scheuerell, S. J., Mahaffee, W. (2004). Compost tea as a container medium drench for suppressing seedling damping-off caused by Pythium ultimum. Phytopathology, 94, 1156–1163. https://doi.org/10.1094/PHYTO.2004.94.11.1156 Schlatter, D., Kinkel, L., Thomashow, L., Weller, D., and Paulitz, T. C. (2017). Disease Suppressive Soils: New Insights from the Soil Microbiome. Phytopathology, 107(11), 1284-1297. https://doi.org/10.1094/PHYTO-03-17-0111-RVW Siegel-Hertz, K., Edel-Hermann, V., Chapelle, E., Terrat, S., Raaijmakers, J. M., and Steinberg, C. (2018). comparative microbiome analysis of a Fusarium wilt suppressive soil and a Fusarium wilt conducive soil from the Châteaurenard region. Frontiers in Microbiology, 9(568), 1-16. https://doi.org/10.3389/fmicb.2018.00568 St. Martin, C. C. G. (2014). Potential of compost tea for suppressing plant diseases. CABI Reviews 3(32), 1-38. DOI: 10.1079/PAVSNNR20149032 Steinberg, C., Edel-Hermann, V., Alabouvette, C., and Lemanceau, P. (2019). Soil suppressiveness to plant diseases. En Modern Soil Microbiology (3rd ed., pp. 343-357). Taylor and Francis. https://doi.org/10.1201/9780429059186 Voroney, R. P., and Heck, R. J. (2015). Chapter 2—The Soil Habitat. En E. A. Paul (Ed.), Soil Microbiology, Ecology and Biochemistry (4th Edition pp. 15-39). Academic Press. https://doi.org/10.1016/B978-0-12-415955-6.00002-5 Weller, D. M., Raaijmakers, J. M., Gardener, B. B. M., and Thomashow, L. S. (2002). Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40(1), 309-348. https://doi.org/10.1146/annurev.phyto.40.030402.110010 Wen, T., Ding, Z., Thomashow, L. S., Hale, L., Yang, S., Xie, P., Liu, X., Wang, H., Shen, Q., and Yuan, J. (2023). Deciphering the mechanism of fungal pathogen-induced disease-suppressive soil. New Phytologist, 238(6), 2634-2650. https://doi.org/10.1111/nph.18886