Abstract
We evaluated the effect of three different Bradyrhizobium strains inoculated in two soybean genotypes (R01-581F, drought-tolerant, and NA5858RR, drought-sensitive) submitted to drought in two trials conducted simultaneously under greenhouse. The strains (SEMIA 587, SEMIA 5019 (both B. elkanii), and SEMIA 5080 (B. diazoefficiens)) were inoculated individually in each genotype and then submitted to water restriction (or kept well-watered, control) between 45 and 62 days after emergence. No deep changes in plant physiological variables were observed under the moderate water restriction imposed during the first 10 days. Nevertheless, photosynthesis and transpiration decreased after the severe water restriction imposed for further 7 days. Water restriction reduced growth (− 30%) and the number of nodules (− 47% and − 58% for R01-581F and NA5858RR, respectively) of both genotypes, with a negative effect on N-metabolism. The genotype R01-581F inoculated with SEMIA 5019 strain had higher photosynthetic rates compared with NA5858RR, regardless of the Bradyrhizobium strain. On average, R01-581F showed better performance under drought than NA5858RR, with higher number of nodules (51 vs. 38 nodules per plant, respectively) and less accumulation of ureides in petioles (15 μmol g−1 vs. 34 μmol g−1, respectively). Moreover, plants inoculated with SEMIA 5080 had higher glutamine synthetase activity under severe water restriction, especially in the drought-tolerant R01-518F, suggesting maintenance of N metabolism under drought. The Bradyrhizobium strain affects the host plant responses to drought in which the strain SEMIA 5080 improves the drought tolerance of R01-518F genotype.
Similar content being viewed by others
References
IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Denmark. https://www.ipcc.ch/site/assets/uploads/2018/05/SYR_AR5_FINAL_full_wcover.pdf. Accessed 12 Jan 2020
Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB, Venkateswarlu B (2014) Drought stress responses in crops. Funct Integr Genom 14:11–22. https://doi.org/10.1007/s10142-013-0356-x
Sinclair TR, Purcell LC, King A, Sneller CH, Chen P, Vadez V (2007) Drought tolerance and yield increase of soybean resulting from improved symbiotic N2 fixation. Field Crop Res 101:68–71. https://doi.org/10.1016/j.fcr.2006.09.010
Cerezini P, Kuwano BH, Neiverth W, Grunvald AK, Pípolo AE, Hungria M, Nogueira MA (2019) Physiological and N2-fixation-related traits for tolerance to drought in soybean progenies. Pesq Agropec Bras 54:e00839. https://doi.org/10.1590/S1678-3921.pab2019.v54.00839
Chen P, Sneller CH, Purcell LC, Sinclair TR, King CA, Ishibashi T (2007) Registration of soybean germplasm lines R01-416F and R01-581F for improved yield and nitrogen fixation under drought stress. J Plant Register 1:166–167. https://doi.org/10.3198/jpr2007.01.0046crg
Serraj R, Sinclair TR, Purcell LC (1999) Symbiotic N2 fixation response to drought. J Exp Bot 50:143–155. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC32231/. Accessed 12 Jan 2020
Bizarro MJ, Giongo A, Vargas LK, Roesch LFW, Gano KA, Saccol de Sá EL, Passaglia LMP, Selbach PA (2011) Genetic variability of soybean bradyrhizobia populations under different soil managements. Biol Fertil Soils 47:357–362. https://doi.org/10.1007/s00374-010-0512-6
Kibido T, Karl Kunert K, Makgopa M, Greve M, Vorster J (2019) Improvement of rhizobium-soybean symbiosis and nitrogen fixation under drought. Food Energy Secur 9. https://doi.org/10.1002/fes3.177
Boddey LH, Hungria M (1997) Phenotypic grouping of Brazilian Bradyrhizobium strains which nodulate soybean. Biol Fertil Soils 25:407–415. https://doi.org/10.1007/s003740050333
Batista JSS, Hungria M, Barcellos FG, Ferreira MC, Mendes IC (2007) Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a Cerrados soil. Microb Ecol 53:270–284. https://doi.org/10.1007/s00248-006-9149-2
Loureiro MD, Kaschuk G, Alberton O, Hungria M (2007) Soybean [Glycine max (L.) Merrill] rhizobial diversity in Brazilian oxisols under various soil, cropping, and inoculation managements. Biol Fertil Soils 43:665–674. https://doi.org/10.1007/s00374-006-0146-x
Kaschuk G, Yin X, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2012) Photosynthetic adaptation of soybean due to varying effectiveness of N2 fixation by two distinct Bradyrhizobium japonicum strains. Environ Exp Bot 76:1–6. https://doi.org/10.1016/j.envexpbot.2011.10.002
Cerezini P, Fagotti DSL, Pipolo AE, Hungria M, Nogueira MA (2017) Water restriction and physiological traits in soybean genotypes contrasting for nitrogen fixation drought tolerance. Sci Agric 74:110–117. https://doi.org/10.1590/1678-992X-2016-0462
Ferguson AR, Sims AP (1971) Inactivation in vivo of glutamine synthetase and NAD specific glutamate dehydrogenase: its role in the regulation of glutamine synthesis in yeasts. J Gen Microbiol 69:423–427. https://doi.org/10.1099/00221287-69-3-423
Hungria M (1994) Metabolismo do carbono e do nitrogênio nos nódulos. In: Hungria M, Araújo RS (eds) Manual de métodos empregados em estudos de microbiologia agrícola. EMBRAPA, Brasília, pp 247–283
Searle PL (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. Analyst 109:549–568. https://pubs.rsc.org/en/content/articlelanding/1984/an/an9840900549/unauth#!divAbstract. Accessed 12 Jan 2020
Vogels GD, Van Der Drift C (1970) Differential analysis of glyoxylate derivatives. Anal Biochem 33:143–157. https://doi.org/10.1016/0003-2697(70)90448-3
Scholles D, Mobrdiecks FG, Vargas LK, Saccol de Sás EL (2004) Efeitos da aplicação de herbicidas sobre a nodulação e desenvolvimento de soja inoculada com estirpes de Bradyrhizobium sp. Pesq Agrop Gaúcha 10:11–22 http://www.fepagro.rs.gov.br/upload/1398798140_art_02.pdf
Sinclair TR, Nogueira MA (2018) The next step to increase grain legume N2 fixation activity: selection of host-plant genotype. J Exp Bot 69:3523–3530. https://doi.org/10.1093/jxb/ery115
Gilbert ME, Zwieniecki MA, Holbrook NM (2011) Independent variation in photosynthetic capacity and stomatal conductance leads to differences in intrinsic water use efficiency in 11 soybean genotypes before and during mild drought. J Exp Bot 62:2875–2887. https://doi.org/10.1093/jxb/erq461
Souza GM, Catuchi TA, Bertolli SC, Soratto RP (2013) Soybean under water deficit: physiological and yield responses. In: Board JE (ed) A comprehensive survey of international soybean research - genetics, physiology, agronomy and nitrogen relationships. Chapter 13, InTech
Sinclair TR, Messina CD, Beatty A, Samples M (2010) Assessment across the United States of the benefits of altered soybean drought traits. Agric J 102:475–482. https://doi.org/10.2134/agronj2009.0195
Guan X, Gu S (2009) Photorespiration and photoprotection of grapevine (Vitisvinifera L. cv. Cabernet sauvignon) under water stress. Photosynthetic 47:437–444. https://doi.org/10.1007/s11099-009-0067-7
Delamuta JRM, Ribeiro RA, Ormenõ-Orrillo E, Melo IS, Martinéz-Romero E, Hungria M (2013) Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol 63:3342–3351. https://doi.org/10.1099/ijs.0.049130-0
Torres AR, Kaschuk G, Saridakis GP, Hungria M (2012) Genetic variability in Bradyrhizobium japonicum strains nodulating soybean [Glycine max (L.) Merrill]. World J Microbiol Biotechnol 28:1831–1835. https://doi.org/10.1007/s11274-011-0964-3
Collier R, Tegeder M (2012) Soybean ureide transporters play a critical role in nodule development, function and nitrogen export. Plant J 72:355–367. https://doi.org/10.1111/j.1365-313X.2012.05086.x
Brychkova G, Alikulov Z, Fluhr R, Sagi M (2008) A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant J 54:496–509. https://doi.org/10.1111/j.1365-313X.2008.03440.x
Baral B, Izaguirre-Mayoral ML (2017) Purine-derived ureides under drought and salinity. Adv Agron 146:167–204. https://doi.org/10.1016/bs.agron.2017.07.001
Hungria M, Kaschuk G (2013) Regulation of N2 fixation and NO3−/NH4+ assimilation in nodulated and N-fertilized Phaseolus vulgaris L. exposed to high temperature stress. Environ Exp Bot 98:32–39. https://doi.org/10.1016/j.envexpbot.2013.10.010
Acknowledgments
P. Cerezini thanks a PhD fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior); M.A. Nogueira and M. Hungria are CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) research fellows. Financed by Embrapa (02.13.08.003.00.00). The group belongs to the INCT-Plant-Growth Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (465133/2014-2)—Fundação Araucária.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Acacio Aparecido Navarrete
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cerezini, P., Kuwano, B.H., Grunvald, A.K. et al. Soybean tolerance to drought depends on the associated Bradyrhizobium strain. Braz J Microbiol 51, 1977–1986 (2020). https://doi.org/10.1007/s42770-020-00375-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-020-00375-1