Beyond the nodule: agro-biotechnological potential of the endophytic microbiota in symbiotic nodules of legumes
DOI:
https://doi.org/10.52807/qunab.v1i1.11Keywords:
nodule endophytic bacteria, bioprospection, co-inoculation, rhizobiaAbstract
Nitrogen fixation through the legume-rhizobium symbiosis is one of the most important processes on the planet Earth. Since its discovery, the symbiosis was strictly pragmatized to rhizobia, and isolates from nodules that failed to nodulate the host plant was considered contaminants. These non-rhizobia are called Non-Nodulating Endophytic Bacteria (NNEB) and constitute a polyphasic group of soil bacteria capable of sharing the nodule interior with rhizobia. Additionally, co-inoculation of NNEB and rhizobia has been shown to improve symbiotic parameters. This synergy is explained by the diversity of growth-promoting and biocontrol characteristics that they exert during the infection and colonization process inside the symbiotic nodule. The biotechnological potential of these microorganisms is still a field to be explored, ranging from agricultural to biomedical biotechnology. This review focuses on updating the concept of NNBE, their role within the nodule, and their phylogenetic diversity. Main techniques for the study of the NNEB and their potential in the Peruvian biotechnology industry are also looked for.
References
Azani, N., Babineau, M., Bailey, C. D., Banks, H., Barbosa, A., Pinto, R. B., Boatwright, J., Borges, L., Brown, G., Bruneau, A., Candido, E., Cardoso, D., Chung, K.-F., Clark, R., Conceição, A. deS., Crisp, M., Cubas, P., Delgado-Salinas, A., Dexter, K., Zimmerman, E. (2017). A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny The Legume Phylogeny Working Group (LPWG). Taxon, 66(1), 4477. https://doi.org/10.12705/661.3
Benito, P., Alonso-Vega, P., Aguado, C., Luján, R., Anzai, Y., Hirsch, A. M., & Trujillo, M. E. (2017). Monitoring the colonization and infection of legume nodules by Micromonospora in co-inoculation experiments with rhizobia. Scientific Reports, 7(1), 11051. https://doi.org/10.1038/s41598-017-11428-1
Bhatt, K., Suyal, D. C., Kumar, S., Singh, K., & Goswami, P. (2022). New insights into engineered plant-microbe interactions for pesticide removal. Chemosphere, 309, 136635. https://doi.org/10.1016/j.chemosphere.2022.136635
Brígido, C., Menéndez, E., Paço, A., Glick, B. R., Belo, A., Félix, M. R., Oliveira, S., & Carvalho, M. (2019). Mediterranean Native Leguminous Plants: A Reservoir of Endophytic Bacteria with Potential to Enhance Chickpea Growth under Stress Conditions. Microorganisms, 7(10), 392. https://doi.org/10.3390/microorganisms7100392
De Meyer, S. E., De Beuf, K., Vekeman, B., & Willems, A. (2015). A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biology and Biochemistry, 83, 111. https://doi.org/10.1016/j.soilbio.2015.01.002
Egamberdieva, D., Wirth, S. J., Shurigin, V. V., Hashem, A., & Abd_Allah, E. F. (2017). Endophytic Bacteria Improve Plant Growth, Symbiotic Performance of Chickpea (Cicer arietinum L.) and Induce Suppression of Root Rot Caused by Fusarium solani under Salt Stress. Frontiers in Microbiology, 8. https://doi.org/10.3389/fmicb.2017.01887
Etesami, H. (2022). Root nodules of legumes: A suitable ecological niche for isolating non-rhizobial bacteria with biotechnological potential in agriculture. Current Research in Biotechnology, 4, 7886. https://doi.org/10.1016/j.crbiot.2022.01.003
Etesami, H., & Adl, S. M. (2020). Can interaction between silicon and nonrhizobial bacteria help in improving nodulation and nitrogen fixation in salinitystressed legumes? A review. Rhizosphere, 15, 100229. https://doi.org/10.1016/j.rhisph.2020.100229
Fan, M., Liu, Z., Nan, L., Wang, E., Chen, W., Lin, Y., & Wei, G. (2018). Isolation, characterization, and selection of heavy metal-resistant and plant growth-promoting endophytic bacteria from root nodules of Robinia pseudoacacia in a Pb/Zn mining area. Microbiological Research, 217, 5159. https://doi.org/10.1016/j.micres.2018.09.002
Foyer, C. H., Nguyen, H., & Lam, H.-M. (2019). Legumes-The art and science of environmentally sustainable agriculture. Plant, Cell & Environment, 42(1), 15. https://doi.org/10.1111/pce.13497
Kan, F. L., Chen, Z. Y., Wang, E. T., Tian, C. F., Sui, X. H., & Chen, W. X. (2007). Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in QinghaiTibet plateau and in other zones of China. Archives of Microbiology, 188(2), 103115. https://doi.org/10.1007/s00203-007-0211-3
Lace, B., & Ott, T. (2018). Commonalities and Differences in Controlling Multipartite Intracellular Infections of Legume Roots by Symbiotic Microbes. Plant and Cell Physiology, 59(4), 666677. https://doi.org/10.1093/pcp/pcy043
Li, J. H., Wang, E. T., Chen, W. F., & Chen, W. X. (2008). Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biology and Biochemistry, 40(1), 238246. https://doi.org/10.1016/j.soilbio.2007.08.014
Liu, J., Wang, E. T., Ren, D. W., & Chen, W. X. (2010). Mixture of endophytic Agrobacterium and Sinorhizobium meliloti strains could induce nonspecific nodulation on some woody legumes. Archives of Microbiology, 192(3), 229234. https://doi.org/10.1007/s00203-010-0543-2
Magadlela, A., Pérez-Fernández, M. A., Kleinert, A., Dreyer, L. L., & Valentine, A. J. (2016). Source of inorganic N affects the cost of growth in a legume tree species ( Virgilia divaricata ) from the Mediterrean-type Fynbos ecosystem. Journal of Plant Ecology, 9(6), 752761. https://doi.org/10.1093/jpe/rtw015
Martínez-Hidalgo, P., & Hirsch, A. M. (2017). The Nodule Microbiome: N 2 -Fixing Rhizobia Do Not Live Alone. Phytobiomes Journal, 1(2), 7082. https://doi.org/10.1094/PBIOMES-12-16-0019-RVW
Mehrasa, H., Farnia, A., Kenarsari, M. J., & Nakhjavan, S. (2022). Correction to: Endophytic Bacteria and SA Application Improve Growth, Biochemical Properties, and Nutrient Uptake in White Beans Under Drought Stress. Journal of Soil Science and Plant Nutrition, 22(3), 34473447. https://doi.org/10.1007/s42729-022-00898-6
Pandya, M., Naresh Kumar, G., & Rajkumar, S. (2013). Invasion of rhizobial infection thread by non-rhizobia for colonization of Vigna radiata root nodules. FEMS Microbiology Letters, 348(1), 5865. https://doi.org/10.1111/1574-6968.12245
Ríos-Ruiz, W. F., Valdez-Nuñez, R. A., Bedmar, E. J., & Castellano-Hinojosa, A. (2019). Utilization of Endophytic Bacteria Isolated from Legume Root Nodules for Plant Growth Promotion (pp. 145176). https://doi.org/10.1007/978-3-030-30926-8_6
Safronova, V. I., Kuznetsova, I. G., Sazanova, A. L., Kimeklis, A. K., Belimov, A. A., Andronov, E. E., Pinaev, A. G., Pukhaev, A. R., Popov, K. P., Akopian, J. A., Willems, A., & Tikhonovich, I. A. (2015). Extra-slow-growing Tardiphaga strains isolated from nodules of Vavilovia formosa (Stev.) Fed. Archives of Microbiology, 197(7), 889898. https://doi.org/10.1007/s00203-015-1122-3
Saini, R., Dudeja, S. S., Giri, R., & Kumar, V. (2015). Isolation, characterization, and evaluation of bacterial root and nodule endophytes from chickpea cultivated in Northern India. Journal of Basic Microbiology, 55(1), 7481. https://doi.org/10.1002/jobm.201300173
Somasegaran, P., & Hoben, H. J. (1994). Handbook for Rhizobia. Springer New York. https://doi.org/10.1007/978-1-4613-8375-8
Sturz, A. V., Christie, B. R., Matheson, B. G., & Nowak, J. (1997). Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biology and Fertility of Soils, 25(1), 1319. https://doi.org/10.1007/s003740050273
Tokgöz, S., Lakshman, D. K., Ghozlan, M. H., Pinar, H., Roberts, D. P., & Mitra, A. (2020). Soybean Nodule-Associated Non-Rhizobial Bacteria Inhibit Plant Pathogens and Induce Growth Promotion in Tomato. Plants, 9(11), 1494. https://doi.org/10.3390/plants9111494
Valdez-Nuñez, R. A., Castro-Tuanama, R., Castellano-Hinojosa, A., Bedmar, E. J., & Ríos-Ruiz, W. F. (2019). PGPR Characterization of Non-Nodulating Bacterial Endophytes from Root Nodules of Vigna unguiculata (L.) Walp. (pp. 111126). https://doi.org/10.1007/978-3-030-17597-9_7
Velázquez, E., Carro, L., Flores-Félix, J. D., Martínez-Hidalgo, P., Menéndez, E., Ramírez-Bahena, M.-H., Mulas, R., González-Andrés, F., Martínez-Molina, E., & Peix, A. (2017). The Legume Nodule Microbiome: A Source of Plant Growth-Promoting Bacteria. In Probiotics and Plant Health (pp. 4170). Springer Singapore. https://doi.org/10.1007/978-981-10-3473-2_3
Wigley, K., Moot, D., Wakelin, S. A., Laugraud, A., Blond, C., Seth, K., & Ridgway, H. (2017). Diverse bacterial taxa inhabit root nodules of lucerne (Medicago sativa L.) in New Zealand pastoral soils. Plant and Soil, 420(12), 253262. https://doi.org/10.1007/s11104-017-3395-6
Zhao, L., Xu, Y., & Lai, X. (2018). Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Brazilian Journal of Microbiology, 49(2), 269278. https://doi.org/10.1016/j.bjm.2017.06.007
Zineb, F. B., Chahinez, M., Abdelkader, B., Sonia, S., Odile, D., Robin, D., & Antoine, G. (2016). Nodular bacterial endophyte diversity associated with native Acacia spp. in desert region of Algeria. African Journal of Microbiology Research, 10(18), 634645. https://doi.org/10.5897/AJMR2015.7678

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Copyright (c) 2022 Renzo Alfredo Valdez-Nuñez, Winston Franz Ríos-Ruiz, Eulogio J. Bedmar

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