Abstract
Seventeen morphological groups of Non-Nodulating Endophytic Bacteria (NNEB) were isolated from the interior of healthy cowpea root nodules (Vigna unguiculata L. Walp.) growing in seven soils from three regions of Peru. The amplification and partial sequencing of the 16S rRNA ribosomal gene for representatives of each morphological group showed that they were closely related to members of genera Rhizobium, Agrobacterium, Phyllobacterium, Mesorhizobium, Bosea, Ochrobactrum, Bradyrhizobium, Labrys, Ensifer, Starkeya and Nordella (Proteobacteria), and of Mycobacterium (Actinobacteria). The plant growth promotion capacity of representative NNEB strains was examined. Agrobacterium radiobacter 5620I and 5722H isolates showed high IAA production (> 400 μg ml−1). Ochrobactrum haematophilum 5410F and Starkeya novella 5740O were the best isolates solubilizing tricalcium phosphate (> 300%). Agrobacterium radiobacter 5722H was the best isolate for production of siderophores (272.59%), whereas A. radiobacter 5620I showed the greatest antagonistic activity against Fusarium oxysporum (88.52%). The NNEB strains identified in this study showed that cowpea root nodules are a potential source of Plant Growth Promoting Bacteria (PGPB) which may be used for the development of new inoculants.
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References
Beghalem, H., Aliliche, K., Chriki, A., et al. (2017). Molecular and phenotypic characterization of endophytic bacteria isolated from Sulla nodules. Microbial Pathogenesis, 111, 225–231.
Boukhatem, Z. F., Merabet, C., Bekki, A., et al. (2016). Nodular bacterial endophyte diversity associated with native Acacia spp. in desert region of Algeria. African Journal of Microbiology Research, 10, 634–645.
Carvalho, M., Muñoz-Amatriaín, M., Castro, I., et al. (2017). Genetic diversity and structure of Iberian Peninsula cowpeas compared to world-wide cowpea accessions using high density SNP markers. BMC Genomics, 18, 891.
Castellano-Hinojosa, A., & Bedmar, E. J. (2017). Methods for evaluating plant growth-promoting rhizobacteria traits. In H. B. Singh, B. K. Sarma, & C. Keswani (Eds.), Advances in PGPR research (pp. 255–274). Oxford: CABI international.
Chou, Y. J., Elliott, G. N., James, E. K., et al. (2007). Labrys neptuniae sp. nov., isolated from root nodules of the aquatic legume Neptunia oleracea. International Journal of Systematic and Evolutionary Microbiology, 57, 577–581.
Da Costa, E. M., Nóbrega, R. S. A., de Carvalho, F., et al. (2013). Promoção do crescimento vegetal e diversidade genética de bactérias isoladas de nódulos de feijão-caupi. Pesquisa Agropecuária Brasileira, 48, 1275–1284.
Da Costa, E. M. D., Carvalho, F. D., Nóbrega, R. S. A., et al. (2016). Bacterial strains from floodplain soils perform different plant-growth promoting processes and enhance cowpea growth. Scientia Agricola, 73, 301–310.
De Meyer, S. E., & Willems, A. (2012). Multilocus sequence analysis of Bosea species and description of Bosea lupini sp. nov., Bosea lathyri sp. nov. and Bosea robiniae sp. nov., isolated from legumes. International Journal of Systematic and Evolutionary Microbiology, 62, 2505–2510.
De Meyer, S. E., de Beuf, K., Vekeman, B., et al. (2015). A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biology and Biochemistry, 83, 1–11.
Egamberdieva, D., Wirth, S. J., Shurigin, V. V., et al. (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, 1887.
FAOSTAT. (2017). Agricultural database. Available in: http://faostat.fao.org/site/567/default.aspx#ancor
Flores-Félix, J. D., Carro, L., Velázquez, E., et al. (2013). Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. International Journal of Systematic and Evolutionary Microbiology, 63, 821–826.
Imran, A., Hafeez, F. Y., Frühling, A., et al. (2010). Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. International Journal of Systematic and Evolutionary Microbiology, 60, 1548–1553.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Legume Phylogeny Working Group. (2013). Towards a new classification system for legumes: Progress report from the 6th international legume conference. South African Journal of Botany, 89, 3–9.
Leite, J., Seido, S. L., & Passos, S. R. (2009). Biodiversity of rhizobia associated with cowpea cultivars in soils of the lower half of the São Francisco River valley. Revista Brasileira de Ciência do Solo, 33, 1215–1226.
Leite, J., Fischer, D., & Rouws, L. F. (2017). Cowpea nodules harbor non-rhizobial bacterial communities that are shaped by soil type rather than plant genotype. Frontiers in Plant Science, 7, 2064.
Martínez-Hidalgo, P., & Hirsch, A. M. (2017). The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes, 1, 70–82.
Martins, J. C. R., Freitas, A. D. S. D., & Menezes, R. S. C. (2015). Nitrogen symbiotically fixed by cowpea and Gliricidia in traditional and agroforestry systems under semiarid conditions. Pesquisa Agropecuaria Brasileira, 50, 178–184.
Palaniappan, P., Chauhan, P. S., & Saravanan, V. S. (2010). Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biology and Fertility of Soils, 46, 807–816.
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, 58–65.
Pandya, M., Rajput, M., & Rajkumar, S. (2015). Exploring plant growth promoting potential of non rhizobial root nodules endophytes of Vigna radiata. Microbiology, 84, 80–89.
Peix, A., Ramírez-Bahena, M. H., & Velázquez, E. (2015). Bacterial associations with legumes. Critical Reviews in Plant Sciences, 34, 17–42.
Rajendran, G., Patel, M. H., & Joshi, S. J. (2012). Isolation and characterization of nodule-associated Exiguobacterium sp. from the root nodules of fenugreek (Trigonella foenum-graecum) and their possible role in plant growth promotion. International Journal of Microbiology, 2012, 1–7.
Regensburger, B., & Hennecke, H. (1983). RNA polymerase from Rhizobium japonicum. Archives of Microbiology, 135, 103–109.
Rigaud, J., & Puppo, A. (1975). Indole-3-acetic acid catabolism by soybean bacteroids. Journal of General Microbiology, 88, 223–228.
Saitou, N., & Nei, M. A. (1987). Neighbour-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 44, 406–425.
Shamsheldin, A., Abdelkhalek, A., & Sadowsky, M. J. (2016). Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria: A review. Symbiosis, 71, 91–109.
Soares, B. L., Ferreira, P. A. A., & de Oliveira-Longatti, S. M. (2014). Cowpea symbiotic efficiency, pH and aluminum tolerance in nitrogen-fixing bacteria. Scientia Agricola (Piracicaba, Braz.), 71, 171–180.
Soil Survey Staff. (2009). Soil survey field and laboratory methods manual. Soil survey investigations Report No. 51, Version 1.0. In R. Burt (Ed.). U.S. Department of Agriculture, Natural Resources Conservation Service.
Somasegaran, P., & Hoben, H. J. (1994). Handbook for rhizobia: Methods in legume-rhizobium technology. New York: Springer.
Tariq, M., Hameed, S., & Yasmeen, T. (2014). Molecular characterization and identification of plant growth promoting endophytic bacteria isolated from the root nodules of pea (Pisum sativum L.). World Journal of Microbiology and Biotechnology, 30, 719–725.
Valdez, R. A., Soriano, B., Prado, G., et al. (2016). Symbiotic and agronomic characterization of bradyrhizobial strains nodulating cowpea in Northern Peru. In F. González-Andrés & E. James (Eds.), Biological nitrogen fixation and beneficial plant-microbe interaction (pp. 195–212). Cham: Springer.
Van Insberghe, D., Maas, K. R., Cárdenas, E., et al. (2015). Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils. Int Soc Microb Ecol, 1–7.
Velázquez, E., Martínez-Hidalgo, P., Carro, L., et al. (2013). Nodular endophytes: An untapped diversity. In M. B. Rodelas-González & J. González-López (Eds.), Beneficial plant-microbe interactions: Ecology and applications (pp. 214–236). Boca Raton: CRC Press.
Velázquez, E., Carro, L., Flores-Félix, J. D., et al. (2017). The legume nodule microbiome: A source of plant growth-promoting bacteria. In V. Kumar et al. (Eds.), Probiotics and plant health (pp. 41–70). Singapore: Springer.
Vincent, J. (1970). A manual for the practical study of the root nodule bacteria international biological programme handbook (Vol. 15). Oxford: Blackwell.
Weisburg, W. G., Barns, S. M., Pelletier, D. A., et al. (1991). 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology, 173, 697–703.
Yoon, S. H., Ha, S. M., Kwon, S., et al. (2017). Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67, 1613–1617.
Zakhia, F., Jeder, H., Willem, A., et al. (2006). Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microbiology Ecology, 51, 375–393.
Zgadzaj, R., James, E. K., Kelly, S., et al. (2015). A legume genetic framework controls infection of nodules by symbiotic and endophytic bacteria. PLoS Genetics, 1–21.
Zhao, L., Xu, Y., & Lai, X. (2017). Antagonistic endophytic bacteria associated with nodules of soybean (Glycine max L.) and plant growth-promoting properties. Brazilian Journal of Microbiology, 49, 269–278.
Acknowledgements
This study was supported by the ERDF-cofinanced grant PEAGR2012-1968 from Consejería de Economía, Innovación y Ciencia (Junta de Andalucía, Spain) and funds from the National University of San Martín-Tarapoto-Peru.
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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.. In: Zúñiga-Dávila, D., González-Andrés, F., Ormeño-Orrillo, E. (eds) Microbial Probiotics for Agricultural Systems. Sustainability in Plant and Crop Protection. Springer, Cham. https://doi.org/10.1007/978-3-030-17597-9_7
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