Performance of different Bradyrhizobium strains in root nodule symbiosis under drought stress

Abdelhamid MT, Kamel HA, Dawood MG (2011) Response of non-nodulating, nodulating, and super-nodulating soybean genotypes to potassium fertilizer under water stress. J Plant Nutr 34:1675–1689. https://doi.org/10.1080/01904167.2011.592563 Almagro L, Gomez-Ros LV, Bekchi-Navarro S, Bru R, Barcelo AR, Predeno MA (2009) Class III peroxidases in plant defense reactions. J Exp Bot 60:377–390. https://doi.org/10.1093/jxb/ern277 Appunu C, Sen D, Singh M, Dhar B (2008) Variation in symbiotic performance of Bradyrhizobium japonicum strains and soybean cultivars under field conditions. J Cent Eur Agric 9:169–174 Arasimowicz M, Floryszak-Wieczorek J, Milczarek G, Jelonek T (2009) Nitric oxide, induced by wounding, mediates redox regulation in pelargonium leaves. Plant Biol (Stuttg) 11:650–663. https://doi.org/10.1111/j.1438-8677.2008.00164.x Athar M, Johnson DA (1996) Nodulation, biomass production, and nitrogen fixation in Alfalfa under drought. J Plant Nutr 19:185–199. https://doi.org/10.1080/01904169609365116 Barbosa MAM, Lobato AKS, Tan DKY, Viana GDM, Coelho KNN, Barbosa JRS, Moraes MCH, Costa RCL, Santos Filho BG, Oliveira Neto CF (2013) Bradyrhizobium improves nitrogen assimilation, osmotic adjustment and growth in contrasting cowpea cultivars under drought. Aust J Crop Sci 7:1983–1989 Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000) Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381. https://doi.org/10.1034/j.1399-3054.2000.100402.x Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107. https://doi.org/10.1093/jxb/erp140 Bohm V, Puspitasari-Nienaber NL, Ferruzzi MG, Schwartz SJ (2002) Trolox equivalent antioxidant capacity of different geometrical isomers of α-carotene, β-carotene, lycopene and zeaxanthin. J Agric Food Chem 50:221–226. https://doi.org/10.1021/jf010888q Cytryn EJ, Sangurdekar DP, Streeter JG, Franck WL, Chang W, Stacey G, Emerich DW, Joshi T, Xu D, Sadowsky MJ (2007) Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J Bacteriol 189:6751–6762. https://doi.org/10.1128/JB.00533-07 Daryanto S, Wang L, Jacinthe P-A (2015) Global synthesis of drought effects on food legume production. Plos One 10:1–16. https://doi.org/10.1371/journal.pone.0127401 dos Santos WD, Ferrarese MLL, Finger A, Teixeira ACN, Ferrarese-Filho O (2004) Lignification and related enzymes in Glycine max root growth-inhibition by ferulic acid. J Chem Ecol 30:1203–1212. https://doi.org/10.1023/B:JOEC.0000030272.83794.f0 Esfahani MN, Mostajeran A (2011) Rhizobial strain involvement in symbiosis efficiency of chickpea–rhizobia under drought stress: plant growth, nitrogen fixation and antioxidant enzyme activities. Acta Physiol Plant 33:1075–1083. https://doi.org/10.1007/s11738-010-0635-2 Evett SR (2008) Gravimetric and volumetric direct measurements of soil water content. In: Evett SR (ed) Field estimation of soil water content: a practical guide to methods, instrumentation, and sensor technology IAEA-TCS-30 International Atomic Energy Agency, Vienna, Austria, pp 23–37 Fenta BA, Beebe SE, Kunert KJ, Burridge JD, Barlow KM, Lynch PJ, Foyer CH (2014) Field phenotyping of soybean roots for drought stress tolerance. Agronomy 4:418–435. https://doi.org/10.3390/agronomy4030418 Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21. https://doi.org/10.1016/j.phytochem.2014.07.020 Germano MG, Menna P, Mostasso FL, Hungria M (2006) RFLP analysis of the rRNA operon of a Brazilian collection of bradyrhizobial strains from 33 legume species. Int J Syst Evol Micr 56:217–229. https://doi.org/10.1099/ijs.0.02917-0 Gil-Quintana E, Lyon D, Staudinger C, Wienkoop S, Gonzalez EM (2015) Medicago truncatula and Glycine max: different drought tolerance and similar local response of the root nodule proteome. J Proteome Res 14:5240–5251. https://doi.org/10.1021/acs.jproteome.5b00617 Hossain Z, Khatoon A, Komatsu S (2013) Soybean proteomics for unraveling abiotic stress response mechanism. J Proteome Res 12:4670–4684. https://doi.org/10.1021/pr400604b Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856. https://doi.org/10.1021/jf030723c IUSS Working Group WRB (2014) World reference base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome Kaur K, Kaur K (2018) Nitric oxide improves thermotolerance in spring maize by inducing varied genotypic defense mechanisms. Acta Physiol Plant 40:55. https://doi.org/10.1007/s11738-018-2632-9 Ladrera R, Marino D, Larrainzar E, Gonzalez EM, Arrese-Igor C (2007) Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol 145:539–546. https://doi.org/10.1104/pp.107.102491 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275 Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276. https://doi.org/10.1093/pcp/pcp082 Marinkovic J, Djordjevic V, Balesevic-Tubic S, Bjelic D, Vucelic-Radovic B, Josic D (2013) Osmotic stress tolerance, PGP traits and RAPD analysis of Bradyrhizobium japonicum strains. Genetika-Belgrade 45:75–86. https://doi.org/10.2298/GENSR1301075M Marquez-Garcia B, Shaw D, Cooper JW, Karpinska B, Quain MD, Makgopa EM, Kunert K, Foyeret CH (2015) Redox markers for drought-induced nodule senescence, a process occurring after drought-induced senescence of the lowest leaves in soybean (Glycine max). Ann Bot Lond 116:497–510. https://doi.org/10.1093/aob/mcv030 Matamoros MA, Dalton DA, Ramos J, Clemen MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:499–509. https://doi.org/10.1104/pp.103.025619 Matamoros MA, Loscos J, Coronado MJ, Ramos J, Sato S, Testillano PS, Tabata S, Becana M (2006) Biosynthesis of ascorbic acid in legume root nodules. Plant Physiol 141:1068–1077. https://doi.org/10.1104/pp.106.081463 Melchiorre M, de Luca MJ, Anta GG, Suarez P, Lopez C, Lascano R, Racca RW (2011) Evaluation of bradyrhizobia strains isolated from field-grown soybean plants in Argentina as improved inoculants. Biol Fert Soils 47:81–89. https://doi.org/10.1007/s00374-010-0503-7 Mhadhbi H, Jebara M, Zitoun A, Limam F, Aouani ME (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea-rhizobia associations. World J Microb Biot 24:1027–1035. https://doi.org/10.1007/s11274-007-9571-8 Mhadhbi H, Fotopoulos V, Djebali N, Polidoros AN, Aouani ME (2009) Behaviours of Medicago truncatula—Sinorhizobium meliloti symbioses under osmotic stress in relation with the symbiotic partner input: effects on nodule functioning and protection. J Agron Crop Sci 195:225–231. https://doi.org/10.1111/j.1439-037X.2009.00361.X Mhadhbi H, Djebali N, Chihaoui S, Jebara M, Mhamdi R (2011) Nodule senescence in Medicago truncatula—Sinorhizobium symbiosis under abiotic constraints: biochemical and structural processes involved in maintaining nitrogen-fixing capacity. J Plant Growth Reg 30:480–489. https://doi.org/10.1007/s00344-011-9210-3 Mhamdi R, Nouairi I, ben Hammouda T, Mhamdi R, Mhadhbi H (2015) Growth capacity and biochemical mechanisms involved in rhizobia tolerance to salinity and water deficit. J Basic Microb 55:451–461. https://doi.org/10.1002/jobm.201400451 Miller NJ, Sampson J, Candeias LP, Bramley PM, Rice-Evans CA (1996) Antioxidant activities of carotenes and xanthophylls. FEBS Lett 384:240–242. https://doi.org/10.1016/0014-5793(96)00323-7 Mnasri B, Aouani ME, Mhamdi R (2007) Nodulation and growth of common bean (Phaseolus vulgaris) under water deficiency. Soil Biol Biochem 39:1744–1750. https://doi.org/10.1016/j.soilbio.2007.01.030 Munoz V, Ibanez F, Tonelli ML, Valetti L, Anzuay MS, Fabra A (2011) Phenotypic and phylogenetic characterization of native peanut Bradyrhizobium isolates obtained from Córdoba, Argentina. Syst Appl Microbiol 34:446–452. https://doi.org/10.1016/j.syapm.2011.04.007 Mutava RN, Prince SJK, Syed NH, Song L, Valliyodan B, Chen W, Nguyen HT (2015) Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol Bioch 86:109–120. https://doi.org/10.1016/j.plaphy.2014.11.010 Neto ADA, Prisco JT, Gomes-Filho E (2009) Changes in soluble amino-N, soluble proteins and free amino acids in leaves and roots of salt-stressed maize genotypes. J Plant Interact 4:137–144. https://doi.org/10.1080/17429140902866954 Neves GYS, Marchiosi R, Ferrarese MLL, Siqueira-Soares RC, Ferrarese-Filho O (2010) Root growth inhibition and lignification induced by salt stress in soybean. J Agron Crop Sci 196:467–473. https://doi.org/10.1111/j.1439-037X.2010.00432.x Nouri MZ, Toorchi M, Komatsu S (2011) Proteomics approach for identifying abiotic stress responsive proteins in soybean. In: Sudaric A (ed) Soybean molecular aspects of breeding. InTech: London, pp 187–214. https://doi.org/10.5772/15518 Papendiek F, Tartiu VE, Morone P, Venus J, Honig A (2016) Assessing the economic profitability of fodder legume production for Green Biorefineries—a cost-benefit analysis to evaluate farmers profitability. J Clean Prod 112:3643–3656. https://doi.org/10.1016/j.jclepro.2015.07.108 Parankusam S, Adimulam SS, Mathur PB, Sharma KK (2017) Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives. Front Plant Sci 8:1582. https://doi.org/10.3389/fpls.2017.01582 Parra-Colmenares A, Kahn ML (2005) Determination of nitrogen fixation effectiveness in selected Medicago truncatula isolates by measuring nitrogen isotope incorporation into pheophytin. Plant Soil 270:159–168. https://doi.org/10.1007/s11104-004-1308-y Pimratch S, Jogloy S, Vorasoot N, Toomsan B, Patanothai A, Holbrook CC (2008) Relationship between biomass production and nitrogen fixation under drought-stress conditions in peanut genotypes with different levels of drought resistance. J Agron Crop Sci 194:15–25. https://doi.org/10.1111/j.1439-037X.2007.00286.x Rao DE, Chaitanya KV (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biol Plant 60:201–218. https://doi.org/10.1007/s10535-016-0584-8 Rasanen LA, Saijets S, Jokinen K, Lindstrom K (2004) Evaluation of the roles of two compatible solutes, glycine beatine and trahalose, for the Acacia senegal-Sinorhizobium symbiosis exposed to drought stress. Plant Soil 260:237–251. https://doi.org/10.1023/B:PLSO.0000030181.03575.e1 Rodriguez-Blanco A, Sicardi M, Frioni L (2010) Competition for nodule occupancy between introduced and native strains of Rhizobium leguminosarum biovar trifolii. Biol Fert Soils 46:419–425. https://doi.org/10.1007/s00374-010-0439-y Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. https://doi.org/10.1111/1462-2920.12439 Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:06–425 Sengupta D, Reddy AR (2011) Water deficit as a regulatory switch for legume root responses. Plant Signal Behav 6:914–917. https://doi.org/10.4161/psb.6.6.15340 Serraj R, Vadez V, Denison RF, Sinclair TR (1999) Involvement of Ureides in Nitrogen fixation inhibition in soybean. Plant Physiol 119:289–296. https://doi.org/10.1104/pp.119.1.289 Silva L, Carvalho H (2013) Possible role of glutamine synthetase in the NO signaling response in root nodules by contributing to the antioxidant defenses. Front Plant Sci 4:372. https://doi.org/10.3389/fpls.2013.00372 Stroschein MRD, Eltz FLF, Antoniolli ZI, Lupatini M, Vargas LK, Giongo A, Pontelli MP (2010) Symbiotic efficiency and genetic characteristics of Bradyrhizobium sp. strain UFSM LA 1.3 isolated from Lupinus albescens (H. et Arn). Sci Agric 67:702–706. https://doi.org/10.1590/S0103-90162010000600012 Studer C, Hu Y, Schmidhalter U (2007) Evaluation of the differential osmotic adjustments between roots and leaves of maize seedlings with single or combined NPK-nutrient supply. Funct Plant Biol 34:228–236. https://doi.org/10.1071/FP06294 Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023 Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197 Torres AR, Kaschuk G, Saridakis GP, Hungria M (2012) Genetic variability in Bradyrhizobium japonicum strains nodulating soybean [Glycine max (L.) Merrill]. World J Microb Biot 28:1831–1835. https://doi.org/10.1007/s11274-011-0964-3 Versalovic J, Koeuth T, Lupski JR (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting bacterial genomes. Nucleic Acids Res 19:6823–6831. https://doi.org/10.1093/nar/19.24.6823 Vincent JM (1970) A manual for the practical study of root nodule bacteria. In I.B.P Hand book No.15. Blackwell Scientific Publications. Oxford. 73–97 Zahoor R, Zhao W, Abid M, Dong H, Zhou Z (2017) Potassium application regulates nitrogen metabolism and osmotic adjustment in cotton (Gossypium hirsutum L.) functional leaf under drought stress. J Plant Physiol 215:30–38. https://doi.org/10.1016/j.jplph.2017.05.001 Zhou K, Yu L (2006) Total phenolic contents and antioxidant properties of commonly consumed vegetables grown in Colorado. LWT Food Sci Technol 39:1155–1162. https://doi.org/10.1016/j.lwt.2005.07.015