Abstract
Background and aims
Drought is one of the main causes of global crop decline. Plant growth-promoting rhizobacteria enhance plant tolerance to adverse environmental conditions. This study aimed to determine whether the rhizobacteria Microvirga vignae (BR 3296 and BR 3299) and Bradyrhizobium sp. (BR 3301) can maintain cowpea growth under drought stress.
Methods
We analyzed biomass, nodulation, nitrogen accumulation, and physiological traits of the inoculated plants. Rhizobacterial strains were assessed for exopolysaccharide (EPS) and indole acetic acid (IAA) production, growth, and biofilm formation in a water-stress medium induced by polyethylene glycol (PEG)-6000. The expression of genes associated with abscisic acid (ABA) biosynthesis in root nodules was also investigated.
Results
All evaluated strains were grown in a culture medium supplemented with PEG. M. vignae strains exhibited increased biofilm formation and EPS production, while Bradyrhizobium showed high IAA production. Cowpea plants inoculated with Bradyrhizobium exhibit higher levels of nodulation, biomass, and nitrogen accumulation. Conversely, M. vignae strains were more efficient at alleviating drought stress and maintaining nodulation, biomass, nitrogen accumulation, and stomatal conductance similar to well-watered plants. Drought-inducible genes were more strongly upregulated in the nodules of plants inoculated with Bradyrhizobium than in those inoculated with M. vignae.
Conclusion
Our results suggest that M. vignae strains, isolated from a semi-arid region, help plants withstand water-stress, whereas the strain of Bradyrhizobium sp. isolated from a wet region did not effectively alleviate drought stress. However, Bradyrhizobium sp. conferred growth and nitrogen accumulation to cowpea superior to M. vignae and like plants supplied with nitrogen fertilizer.
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References
Álvarez-Aragón R, Manuel Palacios JM, Ramirez-Parra E (2023) Rhizobial symbiosis promotes drought tolerance in Vicia sativa and Pisum sativum. Environ Exp Bot 208:105268. https://doi.org/10.1016/j.envexpbot.2023.105268
Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252:1–9. https://doi.org/10.1023/A:1024191913296
Ardley JK, Parker MA, De Meyer SE, Trengove RD, O’Hara GW, Reeve WG, Yates RJ, Dilworth MJ, Willems A, Howieson JG (2012) Microvirga lupini sp. nov., Microvirga lotononidis sp. nov. and Microvirga zambiensis sp. nov. are alphaproteobacterial rootnodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int J Syst Evol Microbiol 62:2579–2588. https://doi.org/10.1099/ijs.0.035097-0
Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27(2):197–205. https://doi.org/10.1007/s11274-010-0444-1
Ashwin R, Bagyaraj DJ, Raju BM (2023) Dual inoculation with Bradyrhizobium liaoningense and Ambispora leptoticha improves drought stress tolerance and productivity in soybean cultivars, MAUS 2 and DSR 12. Biologia 78(2):331–348. https://doi.org/10.1007/s11756-022-01196-3
Ayalew T, Yoseph T (2022) Cowpea (Vigna unguiculata L. Walp.): a choice crop for sustainability during the climate change periods. J Appl Biol Biotechnol 10:154–162. https://doi.org/10.7324/JABB.2022.100320
Barbosa DD, Brito SL, Fernandes PD, Fernandes-Júnior PI, Lima LM (2018) Can Bradyrhizobium strains inoculation reduce water deficit effects on peanuts? World J Microb Biotech 34(7):87. https://doi.org/10.1007/s11274-018-2474-z
Belko N, Zaman-Allah M, Diop NN, Cisse N, Zombre G, Ehlers JD, Vadez V (2013) Restriction of transpiration rate under high vapour pressure deficit and non-limiting water conditions is important for terminal drought tolerance in cowpea. Plant Biol 15:304–316. https://doi.org/10.1111/j.1438-8677.2012.00642.x
Bittencourt PP, Alves AF, Ferreira MB, da Silva Irineu LES, Pinto VB, Olivares FL (2023) Mechanisms and applications of bacterial inoculants in plant drought stress tolerance. Microorganisms 11:502. https://doi.org/10.3390/microorganisms11020502
Bouremani N, Cherif-Silini H, Silini A, Bouket AC, Luptakova L, Alenezi FN, Baranov O, Belbahri L (2023) Plant growth-promoting rhizobacteria (PGPR): a rampart against the adverse effects of drought stress. Water 15:418. https://doi.org/10.3390/w15030418
Braga APA, Cruz JM, de Melo IS (2022) Rhizobacteria from Brazilian semiarid biome as growth promoters of soybean (Glycine max L.) under low water availability. Braz J Microbiol 53:873–883. https://doi.org/10.1007/s42770-022-00711-7
Brasil (2011) Instrução normativa n° 13 de 24 de março de 2011. Ministério da Agricultura Pecuária e Abastecimento. Diário Oficial [da] República Federativa do Brasil, 25 março de 2011. Seção 1, p.3–7. Available at: http://www.agricultura.gov.br/assuntos/insumos-agropecuarios/insumos-agricolas/fertilizantes/legislacao/in-sda-13-de-24-03-2011-inoculantes.pdf/view. Accessed 15 Jun 2023
Cao M, Narayanan M, Shi X, Chen X, Li Z, Ma Y (2023) Optimistic contributions of plant growth-promoting bacteria for sustainable agriculture and climate stress alleviation. Environ Res 217:114924. https://doi.org/10.1016/j.envres.2022.114924
Cerezini P, Kuwano BH, Grunvald AK, Hungria M, Nogueira MA (2020) Soybean tolerance to drought depends on the associated Bradyrhizobium strain. Braz J Microbiol 51:1977–1986. https://doi.org/10.1007/s42770-020-00375-1
Cesari AB, Paulucci NS, López-Gómez M, Hidalgo-Castellanos J, Lluch Plá C, Dardanelli MS (2019) Performance of Bradyrhizobium and Bradyrhizobium–Azospirillum in alleviating the effects of water-restrictive conditions during the early stages of Arachis hypogaea growth. J Plant Growth Regul 38:1362–1374. https://doi.org/10.1007/s00344-019-09939-4
Chaudhry S, Sidhu GPS (2022) Climate change regulated abiotic stress mechanisms in plants: a comprehensive review. Plant Cell Rep 41(1):1–31. https://doi.org/10.1007/s00299-021-02759-5
CONAB, Companhia Nacional de Abastecimento (2022) Monitoring the Brazilian grain harvest, Brasília, DF, v. 9, 2021/22 harvest, n.12 - twelfth survey, September 2022, p 88. file:///C:/Users/rspacheco/Downloads/E-book_Boletim-de-Safras-12o-levantamento.pdf. https://www.conab.gov.br/info-agro/safras/graos/boletim-da-safra-de-graos?start=10
da Silva HAP, Galisa PDS, Oliveira RSDS, Vidal MS, Simões-Araújo JL (2012) Gene expression induced by abiotic stress in cowpea nodules. Pesq Agropec bras 47:797-807. [in Portuguese, with English abstract]
da Silva HAP, Nardeli SM, Alves-Ferreira M, Simões-Araújo JL (2015) Evaluation of reference genes for RT-qPCR normalization in cowpea under drought stress during biological nitrogen fixation. Crop Sci 55:1660–1672. https://doi.org/10.2135/cropsci2014.10.0738
de Andrade WL, de Melo AS, Melo YL, Sá FVS, Rocha MM, Oliveira APS, Fernandes-Júnior PI (2021) Bradyrhizobium inoculation plus foliar application of salicylic acid mitigates water deficit effects on cowpea. J Plant Growth Regul 40:656–667. https://doi.org/10.1007/s00344-020-10130-3
Decagon Devices (2006) Leaf porometer. Operator’s manual. Version 1.0. Decagon Devices. Inc. Pullman, WA, US
do Nascimento TR, Sena PTS, Oliveira GS, da Silva TR, Dias MAM, de Freitas ADS, Martins LMV, Fernandes-Júnior PI (2021) Co-inoculation of two symbiotically efficient Bradyrhizobium strains improves cowpea development better than a single bacterium application. 3 Biotech 11:1–12. https://doi.org/10.1007/s13205-020-02534-5
Du X, Ran Q, Wang J, Jiang H, Wang J, Li YZ (2022) Microvirga roseola sp. nov and Microvirga lenta sp. nov., isolated from Taklamakan desert soil. Int J Syst Evol Microbiol 72:5409. https://doi.org/10.1099/ijsem.0.005409
DuBois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017
Egamberdieva D, Reckling M, Wirth S (2017) Biochar-based Bradyrhizobium inoculum improves growth of lupin (Lupinus angustifolius L.) under drought stress. Eur J Soil Biol 78:38–42. https://doi.org/10.1016/j.ejsobi.2016.11.007
Embrapa (2021) AleloMicro Consultas, Empresa Brasileira de Pesquisa Agropecuária. Section: “Linhagem”. Available at https://am.cenargen.embrapa.br/amconsulta/linhagem?id=33699. Accessed 05 Jun 2023
Falker (2008) Manual do medidor eletrônico de teor clorofila (ClorofiLOG / CFL 1030). Falker Automação Agrícola Ltda. Porto Alegre, Brasil: 33p. Available at: http://www.falker.com.br/produto_download.php?id=4
Fierro-Coronado RA, Quiroz-Figueroa FR, García-Pérez LM, Ramírez-Chávez E, Molina-Torres J, Maldonado-Mendoza IE (2014) IAA-producing rhizobacteria from chickpea (Cicer arietinum L.) induce changes in root architecture and increase root biomass. Can J Microbiol 60:639–648. https://doi.org/10.1139/cjm-2014-0399
Figueiredo MVB, Villar HA, Burity HA, de França FP (1999) Alleviation of water stress effects in cowpea by Bradyrhizobium spp. inoculation. Plant Soil 207:67–75
Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and rhizobium tropici. Appl Soil Ecol 40:182–188. https://doi.org/10.1016/j.apsoil.2008.04.005
Gang S, Sharma S, Saraf M, Buck M, Schumacher J (2021) Bacterial indole-3-acetic acid influences soil nitrogen acquisition in barley and chickpea. Plants 10:780. https://doi.org/10.3390/plants10040780
Grover M, Bodhankar S, Sharma A, Sharma P, Singh J, Nain L (2021) PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst 4:618230. https://doi.org/10.3389/fsufs.2020.618230
Guimarães AA, Florentino LA, Almeida KA, Lebbe L, Silva KB, Willems A, Moreira FMS (2015) High diversity of Bradyrhizobium strains isolated from several legume species and land uses in Brazilian tropical ecosystems. Syst Appl Microbiol 38(6):433–441. https://doi.org/10.1016/j.syapm.2015.06.006
Hall AE, Schulze E-D (1980) Stomatal response to environment and a possible interrelation between stomatal effects on transpiration and CO2 assimilation. Plant Cell Environ 3:467–474. https://doi.org/10.1111/1365-3040.ep11587040
Hellemans J, Mortier G, de Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. https://doi.org/10.1186/gb-2007-8-2-r19
Iuchi S, Yamaguchi-Shinozaki K, Urao T, Shinozaki K (1996a) Characterization of two cDNAs for novel drought-inducible genes in the highly drought-tolerant cowpea. J Plant Res 109(4):415–424
Iuchi S, Yamaguchi-Shinozaki K, Urao T, Terao T, Shinozaki K (1996b) Novel drought-inducible genes in the highly drought-tolerant cowpea: cloning of cDNAs and analysis of the expression of the corresponding genes. Plant Cell Physiol 37(8):1073–1082
Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123(2):553–562
Jordan DC (1982) Transfer of rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. Nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int J Syst Bacteriol 32:136–139
Kavamura VN, Santos SN, da Silva JL, Parma MM, Ávila LA, Visconti A, Zucchi TD, Taketani RG, Andreote FD, de Melo IS (2013) Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res 168:183–191. https://doi.org/10.1016/j.micres.2012.12.002
Lumactud RA, Dollete D, Liyanage DK, Szczyglowski K, Hill B, Thilakarathna MS (2022) The effect of drought stress on nodulation, plant growth, and nitrogen fixation in soybean during early plant growth. J Agro Crop Sci. https://doi.org/10.1111/jac.12627
Marengo JA, Souza CM Jr, Thonicke K, Burton C, Halladay K, Betts RA, Alves LM, Soares WR (2018) Changes in climate and land use over the Amazon region: current and future variability and trends. Front Earth Sci 6:228. https://doi.org/10.3389/feart.2018.00228
Marinho RCN, Nóbrega RSA, Zilli JE, Xavier GR, Santos CAF, Aidar ST, Martins LMV, Fernandes-Júnior PI (2014) Field performance of new cowpea cultivars inoculated with efficient nitrogen-fixing rhizobial strains in the Brazilian semiarid. Pesq Agropec Bras 49:395–402. https://doi.org/10.1590/S0100-204X2014000500009
Marinković J, Bjelić D, Đorđević V, Balešević-Tubić S, Jošić D, Vucelić-Radović B (2019) Performance of different Bradyrhizobium strains in root nodule symbiosis under drought stress. Acta Physiol Plant 41:37. https://doi.org/10.1007/s11738-019-2826-9
Martins LMV, Neves MCP, Rumjanek NG (1997) Growth characteristics and symbiotic efficiency of rhizobia isolated from cowpea nodules of the north-east region of Brazil. Soil Biol Biochem 29:1005–1010
Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. https://doi.org/10.1007/s00344-009-9079-6
Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51(5):914–916
Mouad L, Hanane L, Omar B, Meryeme B, Hanaa A, Bedma EJ, El Idrissi MM (2020) Nodulation of Retama species by members of the genus Microvirga in Morocco. Symbiosis 82:249–258. https://doi.org/10.1007/s13199-020-00725-5
Msaddak A, Rejili M, Durán D, Rey L, Imperial J, Palacios JM, Ruiz-Argüeso T, Mars M (2017) Members of Microvirga and Bradyrhizobium genera are native endosymbiotic bacteria nodulating Lupinus luteus in northern Tunisian soils. FEMS Microbiol Ecol 93:28505340. https://doi.org/10.1093/femsec/fix068
Msaddak A, Rejili M, Durán D, Mars M, Palacios JM, Ruiz-Argüeso T, Imperial J (2019) Microvirga tunisiensis sp. nov., a root nodule symbiotic bacterium isolated from Lupinus micranthus and L. luteus grown in northern Tunisia. Syst Appl Microbiol 42(6):126015. https://doi.org/10.1016/j.syapm.2019.126015
Munjonji L, Ayisi KK, Haesaert G, Boeckx P (2018) Screening cowpea genotypes for high biological nitrogen fixation and grain yield under drought conditions. Agron J 110:1925–1935. https://doi.org/10.2134/agronj2017.01.0037
Naseem H, Ahsan M, Shahid MA, Khan N (2018) Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J Basic Microbiol 58(12):1009–1022
Nelson DW, Sommers LE (1973) Determination of Total nitrogen in plant material. Agron J 65:109–112. https://doi.org/10.2134/agronj1973.00021962006500010033x
Nonato JJ, da Silva TJA, Bonfim-Silva EM (2022) Cowpea root growth under water availability and co-inoculation with growth promoting rhizobacteria. Commun Soil Sci Plant Anal 53(14):1756–1766. https://doi.org/10.1080/00103624.2022.2063320
Nunes GFO, Menezes KAS, Sampaio AA, Leite J, Fernandes-Júnior PI, Seido SL, Zilli JÉ, Martins LMV (2018) Polyphasic characterization of forage legumes root nodule bacteria isolated from semiarid region in Brazil. Rev Ciênc Agrár 41:612–624. https://doi.org/10.19084/RCA17339
Oosthuizen MC, Steyn B, Lindsay D, Brözel VS, von Holy A (2001) Novel method for the proteomic investigation of a dairy-associated Bacillus cereus biofilm. FEMS Microbiol Lett 194(1):47–51. https://doi.org/10.1111/j.1574-6968.2001.tb09444.x
Pacheco RS, Boddey RM, Alves BJR, Straliotto R, Araújo AP (2017) Growth patterns of common bean cultivars affect the ‘B’ value required to quantify biological N2 fixation using the 15N natural abundance technique. Plant Soil 419(1):293–304. https://doi.org/10.1007/s11104-017-3331-9
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36
Qin XQ, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci U S A 96:15354–15361
Radl V, Simões-Araújo JL, Leite J, Passos SR, Martins LM, Xavier GR, Rumjanek NG, Baldani JI, Zilli JE (2014) Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int J Syst Evol Microbiol 64:725–7230. https://doi.org/10.1099/ijs.0.053082-0
Rejili M, Msaddak A, Filali I, Benabderrahim MA, Mars M, Marín M (2019) New chromosomal lineages within Microvirga and Bradyrhizobium genera nodulate Lupinus angustifolius growing on different Tunisian soils. FEMS Microbial Ecol 95(9):fiz118. https://doi.org/10.1093/femsec/fiz118
Rivas R, Falcão HM, Ribeiro RV, Machado EC, Pimentel C, Santos MG (2016) Drought tolerance in cowpea species is driven by less sensitivity of leaf gas exchange to water deficit and rapid recovery of photosynthesis after rehydration. S Afr J Bot 103:101–107. https://doi.org/10.1016/j.sajb.2015.08.008
Sarwar M, Kremer RJ (1995) Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol 20:282–285. https://doi.org/10.1111/j.1472-765X.1995.tb00446.x
Sauer DB, Burroughs R (1986) Disinfection of seed surfaces with sodium hypochlorite. Phytopathology 76:745–749. https://doi.org/10.1094/Phyto-76-745
Sena PTS, do Nascimento TR, Lino J, Oliveria GS, Neto RAF, de Freitas ADS, Fernandes PI Jr, Martins LMV (2020) Molecular, physiological, and symbiotic characterization of cowpea rhizobia from soils under different agricultural systems in the semiarid region of Brazil. J Soil Sci Plant Nutr 20(3):1178–1192. https://doi.org/10.1007/s42729-020-00203-3
Shet SA, Garg S (2022) Plant growth promotion of Vigna unguiculata in arid sandy soil using bacterial species from coastal sand dune. Agric Res 1–12. https://doi.org/10.1007/s40003-022-00613-y
Shirinbayan S, Khosravi H, Malakouti MJ (2019) Alleviation of drought stress in maize (Zea mays) by inoculation with Azotobacter strains isolated from semi-arid regions. Appl Soil Ecol 133:138–145. https://doi.org/10.1016/j.apsoil.2018.09.015
Silva ER, Zoz J, Oliveira CES, Zuffo AM, Steiner F, Zoz T, Vendruscolo EP (2019) Can co-inoculation of Bradyrhizobium and Azospirillum alleviate adverse effects of drought stress on soybean (Glycine max L. Merrill.)? Arch Microbiol 201(3):325–335. https://doi.org/10.1007/s00203-018-01617-5
Soares ALL, Pereira JPAR, Ferreira PAA, Vale HMM, Lima AS, Andrade MJB, Moreira FMS (2006) Agronomic efficiency of selected rhizobia strains and diversity of native nodulating populations in Perdões (MG - Brazil). I - cowpea. Rev Bras Ciênc Solo 30:795–802. [in Portuguese, with English abstract]
Sprent JI (1994) Evolution and diversity in the legume-rhizobium symbiosis: chaos theory? Plant Soil 161:1–10
StatSoft, Inc. (2011) STATISTICA (Data analysis software system), Version 10. http://www.statsoft.com
Telles TS, Nogueira MA, Hungria M (2023) Economic value of biological nitrogen fixation in soybean crops in Brazil. Environ Technol Innov 31:103158. https://doi.org/10.1016/j.eti.2023.103158
UN (2015) Transforming our world: the 2030 agenda for sustainable development. A/RES/70/1. United Nations General Assembly, New York, p 25. Available at: https://sustainabledevelopment.un.org/post2015/transformingourworld. Accessed 10 Jul 2023
Uzma M, Iqbal A, Hasnain S (2022) Drought tolerance induction and growth promotion by indole acetic acid producing Pseudomonas aeruginosa in Vigna radiata. PLoS One 17(2):e0262932. https://doi.org/10.1371/journal.pone.0262932
Veyisoglu A, Tatar D, Saygin H, Inan K, Cetin D, Guven K, Tuncer M, Sahin N (2016) Microvirga makkahensis sp. nov., and Microvirga arabica sp. nov., isolated from sandy arid soil. Antonie Van Leeuwenhoek 109:287–296. https://doi.org/10.1007/s10482-015-0631-z
Vilarinho AA (2007) BRS Guariba: cultivar de feijão-caupi de alto desempenho em Roraima. Available at: http://www.infobibos.com/Artigos/2007_4/Guariba/index.htm. Accessed 14 Mai 2023
Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14:2535–2554. https://doi.org/10.3390/molecules14072535
Xavier GR, Runjanek NG, de Rosalia e Silva Santos CE, de Freitas ADS, da Silva VSG, da Silva AF, de Alcantara RMCM (2017) Agronomic effectiveness of rhizobia strains on cowpea in two consecutive years. Aust J Crop Sci 11:1154–1160. https://doi.org/10.21475/ajcs.17.11.09.pne715
Xiong H, Shi A, Mou B, Qin J, Motes D, Lu W, Wu D (2016) Genetic diversity and population structure of cowpea (Vigna unguiculata L. Walp). PLoS one 11:8e.160941. https://doi.org/10.1371/journal.pone.0160941
Zegaoui Z, Planchais S, Cabassa C, Djebbar R, Belbachir OA, Carol P (2017) variation in relative water content, proline accumulation and stress gene expression in two cowpea landraces under drought. J Plant Physiol 218:26–34. https://doi.org/10.1016/j.jplph.2017.07.009
Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064. https://doi.org/10.1089/cmb.2005.12.1047
Zilli JE, Passos SR, Leite J, Xavier GR, Rumjaneck NG, Simoes-Araujo JL (2015) Draft genome sequence of Microvirga vignae strain BR 3299T, a novel symbiotic nitrogen-fixing Alphaproteobacterium isolated from a Brazilian semiarid region. Genome Announc 3(4):e00700–e00715. https://doi.org/10.1128/genomeA.00700-15
Acknowledgements
We would like to thank Dr. Jerri Zilli (curator of the Johanna Döbereiner Biological Resource Center of Embrapa Agrobiologia) and Drª. Fátima Moreira (professor of Universidade Federal de Lavras) for information on the nomenclature of Bradyrhizobium BR 3301 strain. We also thank Dr. Leonardo Medice (professor of Universidade Federal Rural do Rio de Janeiro) for providing the chlorophyllometer and porometer devices.
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Research grants from the CAPES (Coordination for the Improvement of Higher Education Personnel - Finance Code 001) and CNPq (Brazilian National Council for Scientific and Technological Development); and financial support from EMBRAPA (Brazilian Agricultural Research Corporation).
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JLSA, RSP, GRX conceptualization the study and supervised the research; SSC, RSP, GC performed the experiments, collected the samples and analyzing the data; MSV assisted in the qPCR analyzes; SSC and RSP wrote the preliminary draft; JLSA reviewed the final manuscript. All authors wrote the manuscript and agreed with the submitting.
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Correa, S.S., Pacheco, R.S., Viana, G.C. et al. Ability of nitrogen-fixing bacteria to alleviate drought stress in cowpea varies depending on the origin of the inoculated strain. Plant Soil 498, 391–408 (2024). https://doi.org/10.1007/s11104-023-06443-3
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DOI: https://doi.org/10.1007/s11104-023-06443-3