Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-18T05:06:48.044Z Has data issue: false hasContentIssue false
  • English
  • Français

Indigenous rhizobial strains SEMIA 4108 and SEMIA 4107 for common bean inoculation: A biotechnological tool for cleaner and more sustainable agriculture

Published online by Cambridge University Press:  16 April 2021

Bruno Britto Lisboa ,
Thomas Müller Schmidt ,
Arthur Henrique Ely Thomé ,
Raul Antonio Sperotto ,
Camila Gazolla Volpiano ,
Jackson Freitas Brilhante de São Jose ,
Luciano Kayser Vargas  and
Camille Eichelberger Granada Open the ORCID record for Camille Eichelberger Granada [Opens in a new window]
Bruno Britto Lisboa
Affiliation:
Department of Agricultural Research and Diagnosis, Agriculture, Livestock and Irrigation, Secretary of Rio Grande do Sul, Porto Alegre, RS, Brazil
Thomas Müller Schmidt
Affiliation:
University of Taquari Valley – Univates, Graduate Program in Biotechnology, Lajeado, RS, Brazil
Arthur Henrique Ely Thomé
Affiliation:
University of Taquari Valley – Univates, Graduate Program in Biotechnology, Lajeado, RS, Brazil
Raul Antonio Sperotto
Affiliation:
University of Taquari Valley – Univates, Graduate Program in Biotechnology, Lajeado, RS, Brazil
Camila Gazolla Volpiano
Affiliation:
Federal University of Rio Grande do Sul (UFRGS), Department of Genetics, Institute of Biosciences, Porto Alegre, RS, Brazil
Jackson Freitas Brilhante de São Jose
Affiliation:
Department of Agricultural Research and Diagnosis, Agriculture, Livestock and Irrigation, Secretary of Rio Grande do Sul, Porto Alegre, RS, Brazil
Luciano Kayser Vargas
Affiliation:
Department of Agricultural Research and Diagnosis, Agriculture, Livestock and Irrigation, Secretary of Rio Grande do Sul, Porto Alegre, RS, Brazil
Camille Eichelberger Granada*
Affiliation:
University of Taquari Valley – Univates, Graduate Program in Biotechnology, Lajeado, RS, Brazil
*
*Corresponding author. Email: cegranada@univates.br
Get access Rights & Permissions [Opens in a new window]

Summary

Inoculation of symbiotic N2-fixing rhizobacteria (rhizobia) in legumes is an alternative to reduce synthetic N fertiliser input to crops. Even though common bean benefits from the biological N2 fixation carried out by native rhizobia isolates, the low efficiency of this process highlights the importance of screening new strains for plant inoculation. Two rhizobial strains (SEMIA 4108 and SEMIA 4107) previously showed great potential to improve the growth of common beans under greenhouse conditions. Thus, this study evaluated the growth and grain yield of common bean plants inoculated with those strains in field experiments. The rhizobial identification was performed by 16S rRNA sequencing and the phylogeny showed that SEMIA 4108 and SEMIA 4107 are closely related to Rhizobium phaseoli, within a clade containing other 18 Rhizobium spp. type strains. Common bean plants inoculated with SEMIA 4107 showed similar productivity to N-fertilised (N+) plants in the first experiment (2016/17) and higher productivity in the second experiment (2018/19). The development of inoculated plants was different from that observed for N+. Nonetheless, comparing inoculated treatments with N-fertilised control, no yield or productivity losses at the end of the growing process were detected. Our results showed that inoculation of the rhizobial isolates SEMIA 4108 and SEMIA 4107 improved the growth and grain yield of common bean plants. The observed agronomical performance confirms that both strains were effective and can sustain common bean growth without nitrogen fertilisation under the edaphoclimatic conditions of this study.

Keywords

Biological nitrogen fixationIndigenous RhizobiumField experiments
Type
Research Article
Information
Experimental Agriculture , Volume 57 , Issue 1 , February 2021 , pp. 57 - 67
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

These authors contributed equally to this work.

References

Bhattacharyya, P.N. and Jha, D.K. (2012). Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World Journal of Microbiology and Biotechnology 28, 1327–1350.CrossRefGoogle ScholarPubMed
BRASIL (2011). Ministério da Agricultura Pecuária e Abastecimento. Secretaria da Defesa Agropecuária. Instrução Normativa nº 13, de 24 de março de 2011. Brasília.Google Scholar
Chibeba, A.M., Kyei-Boahen, S., Guimarães, M.F., Nogueira, M.A. and Hungria, M. (2018). Feasibility of transference of inoculation-related technologies: a case study of evaluation of soybean rhizobial strains under the agro-climatic conditions of Brazil and Mozambique. Agriculture Ecosystems and Environment 261, 230–240.CrossRefGoogle ScholarPubMed
de Souza, E.M., Bassani, V.L., Sperotto, R.A. and Granada, C.E. (2016). Inoculation of new rhizobial isolates improve nutrient uptake and growth of bean (Phaseolus vulgaris) and arugula (Eruca sativa). Journal of the Science of Food and Agriculture 96, 3446–3453.CrossRefGoogle Scholar
Fageria, N.K., Melo, L.C., Ferreira, E.P.B., Oliveira, J.P. and Knupp, A.M. (2014). Dry matter, grain yield, and yield components of dry bean as influenced by nitrogen fertilization and rhizobia. Communications in Soil Science and Plant Analysis 45, 111–125.CrossRefGoogle Scholar
FAO (2018). Food and Agriculture Organization of the United Nations. Statistical databases. Available at http://www.fao.org/faostat/en/#data/QC (accessed 27 October 2020).Google Scholar
Figueiredo, M.V.B., Martinez, C.R., Burity, H.A. and Chanway, C.P. (2008). Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World Journal of Microbiology and Biotechnology 24, 1187–1193.CrossRefGoogle Scholar
Gourion, B., Berrabah, F., Ratet, P. and Stacey, G. (2015). Rhizobium-legume symbioses: the crucial role of plant immunity. Trends in Plant Science 20, 186–194.CrossRefGoogle ScholarPubMed
Graham, P.H., Sadowsky, M.J., Keyser, H.H., Barnet, Y.M., Bradley, R.S., Cooper, J.E. and Young, J.P.W. (1991). Proposed minimal standards for the description of new genera and species of root-and stem-nodulating bacteria. International Journal of Systematic and Evolutionary Microbiology 41, 582–587.Google Scholar
Granada, C.E., Beneduzi, A., Lisboa, B.B., Turchetto-Zolet, A.C., Vargas, L.K. and Passaglia, L.M. (2015). Multilocus sequence analysis reveals taxonomic differences among Bradyrhizobium sp. symbionts of Lupinus albescens plants growing in arenized and non-arenized areas. Systematic and Applied Microbiology 38(5), 323–329.CrossRefGoogle ScholarPubMed
Hahn, M.W., Jezberová, J., Koll, U., Saueressig-Beck, T. and Schmidt, J. (2016). Complete ecological isolation and cryptic diversity in Polynucleobacter bacteria not resolved by 16S rRNA gene sequences. The ISME Journal 10, 1642–1655.CrossRefGoogle Scholar
Hungria, M., Campo, R.J. and Mendes, I.C. (2003). Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils 39(2), 88–93.CrossRefGoogle Scholar
Kaschuk, G., Hungria, M., Andrade, D.S. and Campo, R.J. (2006). Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Applied Soil Ecology 32, 210–220.CrossRefGoogle Scholar
Kolbert, C.P. and Persing, D.H. (1999). Ribosomal DNA sequencing as a tool for identification of bacterial pathogens. Current Opinion in Microbiology 2, 299–305.CrossRefGoogle ScholarPubMed
Korir, H., Mungai, N.W., Thuita, M., Hamba, Y. and Masso, C. (2017). Co-inoculation effect of rhizobia and Plant Growth Promoting Rhizobacteria on common bean growth in a low phosphorus soil. Frontiers in Plant Science 8, 141. https://doi.org/10.3389/fpls.2017.00141 CrossRefGoogle Scholar
Koskey, G., Mburu, S.W., Njeru, E.M., Kimiti, J.M., Ombori, O. and Maingi, J.M. (2017). Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of eastern Kenya. Frontiers in Plant Science 8, 443. https://doi.org/10.3389/fpls.2017.00443 CrossRefGoogle ScholarPubMed
Martínez-Romero, E. (2003). Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant and Soil 252, 11–23. https://doi.org/10.1023/A:1024199013926 CrossRefGoogle Scholar
Mercante, F.M., Otsubo, A.A. and Brito, O.R. (2017). New native rhizobia strains for inoculation of common bean in the Brazilian savanna. Revista Brasileira de Ciência do Solo 41, 120–150. https://doi.org/10.1590/18069657rbcs20150120 CrossRefGoogle Scholar
Mondal, T., Datta, J.K. and Mondal, N.K. (2017). Chemical fertilizer in conjunction with biofertilizer and vermicompost induced changes in morpho-physiological and bio-chemical traits of mustard crop. Journal of Saudi Society of Agricultural Science 16, 135–144. https://doi.org/10.1016/j.jssas.2015.05.001 CrossRefGoogle Scholar
Notvony, V. (1999). Diffuse pollution from agriculture – a worldwide outlook. Water Science and Technology 3, 1–13.Google Scholar
Oliveira-Longatti, S.M. de, Marra, L.M. and Moreira, F.M.D.S. (2013). Evaluation of plant growth-promoting traits of Burkholderia and Rhizobium strains isolated from Amazon soils for their co-inoculation in common bean. African Journal of Microbiology Research 7, 948–959. https://doi.org/10.5897/AJMR12.1055 CrossRefGoogle Scholar
Pastor-Bueis, R., Sánchez-Cañizares, C., James, E.K. and González-Andrés, F. (2019). Formulation of a highly effective inoculant for common bean based on an autochthonous elite strain of Rhizobium leguminosarum bv. phaseoli, and genomic-based insights into its agronomic performance. Frontiers in Microbiology 10, 2724. https://doi.org/10.3389/fmicb.2019.02724 CrossRefGoogle Scholar
Peoples, M.B., Brockwell, J., Herridge, D.F., Rochester, I.J., Alves, B.J.R., Urquiaga, S., Boddey, R.M., Dakora, F.D., Bhattarai, S., Maskey, S.L., Sampet, C., Rerkasem, B., Khan, D.F., Hauggaard-Nielsen, H. and Jensen, E.S. (2009). The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48, 1–17. https://doi.org/10.1007/BF03179980 CrossRefGoogle Scholar
Revell, L.J. (2012). Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.CrossRefGoogle Scholar
Ribeiro, R.A., Ormeño-Orrillo, E., Dall’Agnol, R.F., Graham, P.H., Martinez-Romero, E. and Hungria, M. (2013). Novel Rhizobium lineages isolated from root nodules of the common bean (Phaseolus vulgaris L.) in Andean and Mesoamerican areas. Research in Microbiology 164, 740–748. https://doi.org/10.1016/j.resmic.2013.05.002 CrossRefGoogle ScholarPubMed
Samavat, S., Mafakheri, S. and Shakouri, M.J. (2012). Promoting common bean growth and nitrogen fixation by the co-inoculation of Rhizobium and Pseudomonas fluorescens isolates. Bulgarian Journal of Agricultural Science 18, 387–395.Google Scholar
Schliep, K.P. (2011). Phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593.CrossRefGoogle ScholarPubMed
Schmidt, T.M., Thomé, A.H.E., Sperotto, R.A. and Granada, C.E. (2019). Effect of rhizobia inoculation on the development of soil-borne pathogens infecting common bean plants. European Journal of Plant Pathology 153, 687–694. https://doi.org/10.1007/s10658-018-1600-y CrossRefGoogle Scholar
Shamseldin, A. and Velázquez, E. (2020). The promiscuity of Phaseolus vulgaris L. (common bean) for nodulation with rhizobia: a review. World Journal of Microbiology and Biotechnology 36, 63. https://doi.org/10.1007/s11274-020-02839-w CrossRefGoogle ScholarPubMed
Sengupta, A. and Gunri, S.K. (2015). Microbial intervention in agriculture: an overview. African Journal of Microbiology Research 9, 1215–1226. https://doi.org/10.5897/AJMR2014.7325 Google Scholar
Skowronska, M. and Filipek, T. (2014). Life cycle assessment of fertilizers: a review. International Agrophysics 28, 101–110. https://doi.org/10.2478/intag-2013-0032 CrossRefGoogle Scholar
Soil Survey Staff (1999). Soil Taxonomy: A Basic System of Soil Classification for Making and Interpreting Soil Surveys, 2nd Edn. Washington, USA: Natural Resources Conservation Service. U.S. Department of Agriculture Handbook, p. 436.Google Scholar
Sparks, D.L., Page, A.L., Helmke, P.A., Loeppert, R.H. (2020) Methods of Soil Analysis, Part 3: Chemical Methods, vol. 14. Madison, USA: American Society of Agronomy.Google Scholar
Stajković, O., Delić, D., Josić, D., Kuzmanović, D., Rasulić, N. and Knezević-Vukčević, J. (2011). Improvement of common bean growth by co- inoculation with Rhizobium and plant growth- promoting bacteria. Romanian Biotechnology Letters 16, 5919–5926.Google Scholar
Stewart, W.M., Dibb, D.W., Johnston, A.E. and Smyth, T.J. (2005). The contribution of commercial fertilizer nutrients to food production. Agronomy Journal 97, 1–6. https://doi.org/10.2134/agronj2005.0001 CrossRefGoogle Scholar
Vargas, L.K., Lisboa, B.B., Schlindwein, G., Granada, C.E., Giongo, A., Beneduzi, A. and Passaglia, L.M.P. (2009). Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul state. Revista Brasileira de Ciência do Solo 33, 1227–1235.CrossRefGoogle Scholar
Vargas, M.A.T., Mendes, I.C. and Hungria, M. (2000). Response of field-grown bean (Phaseolus vulgaris L.) to Rhizobium inoculation and nitrogen fertilization in two Cerrados soils. Biology and Fertility of Soils 32, 228–233.CrossRefGoogle Scholar
Vincent, J.M. (1970). A Manual for the Practical Study of Root Nodule Bacteria IBP Handbook, n. 15. Oxford: Blackwell.Google Scholar
Vitousek, P.M., Aber, J.D., Howarth, R.H., Likens, G.E., Matson, P.A., Schindler, D.W., Schlesinger, W.H. and Tilman, D.G. (1997). Human alteration of the global nitrogen cycle: Source and consequences. Ecology Applied 7, 737–750.Google Scholar
Volpiano, C.G., Lisboa, B.B., São José, J.F.B, Oliveira, A.M.R., Beneduzi, A., Passaglia, L.M.P. and Vargas, L.K. (2018). Rhizobium strains in the biological control of the phytopathogenic fungi Sclerotium (Athelia) rolfsii on the common bean. Plant and Soil 432, 229–243.CrossRefGoogle Scholar
Wright, E.S. (2015). DECIPHER: harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics 16, 322.CrossRefGoogle ScholarPubMed
Yanni, Y., Zidan, M., Dazzo, F., Rizk, R., Mehesen, A., Abdelfattah, F. and Elsadany, A. (2016). Enhanced symbiotic performance and productivity of drought stressed common bean after inoculation with tolerant native rhizobia in extensive fields. Agriculture Ecosystems and Environment 232, 119–128.CrossRefGoogle Scholar
Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H. and Chun, J. (2017). Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology 67, 1613.CrossRefGoogle ScholarPubMed
Yu, G., Smith, D.K., Zhu, H., Guan, Y. and Lam, T.T.Y. (2017). Ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8, 28–36.CrossRefGoogle Scholar
Zaman-Allah, M., Sifi, B., L’Taief, B., El Aouni, M.H. and Drevon, J.J. (2007). Rhizobial inoculation and P fertilization response in common bean (Phaseolus vulgaris) under glasshouse and field conditions. Experimental Agriculture 43, 67–77.CrossRefGoogle Scholar
Zhang, X., Davidson, E.A., Mauzerall, D.L., Searchinger, T.D., Dumas, P. and Shen, Y. (2015). Managing nitrogen for sustainable development. Nature 528. 51–59.CrossRefGoogle ScholarPubMed
Supplementary material: File

Lisboa et al. supplementary material

Lisboa et al. supplementary material 1

Download Lisboa et al. supplementary material(File)
File 13.4 KB
Supplementary material: Image

Lisboa et al. supplementary material

Lisboa et al. supplementary material 2

Download Lisboa et al. supplementary material(Image)
Image 1.1 MB
Supplementary material: Image

Lisboa et al. supplementary material

Lisboa et al. supplementary material 3

Download Lisboa et al. supplementary material(Image)
Image 2.1 MB