Skip to main content
SpringerLink
Log in

Rhizobia at Extremes of Acidity, Alkalinity, Salinity, and Temperature

  • Chapter
  • First Online:
Microbial Versatility in Varied Environments

Abstract

Symbiosis and nitrogen fixation are an utmost requirement in agricultural system and global nitrogen (N) cycling. However, the soil’s harsh conditions such as acidity, alkalinity, salinity, and temperature are the primary challenges to plant-microbe interaction. Because conditions altered rapidly in soil and thus associated bacteria is failed in selection and associate with compatible host. Among the soil microbiota, rhizobia are a well-known group of bacteria for their ability to fix atmospheric nitrogen via the mechanism of symbioses with leguminous plants. These are opportunistic endosymbionts as well as saprophytic bacteria. Though soil abiotic factors have altered the activity of rhizobial populations negatively, research have proven that soil pH, salinity, and temperature are the major abiotic factors in determining the rhizobial population and their symbiotic performance. Hence, the following chapter described the integrative view of adaptation mechanism and physiological responses of rhizobia in acid, alkalinity, salinity, and temperature stress.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdelmoumen H, Filaling MA, Neyra M, Belabed A, El Idrissi MM (1999) Effects of high salts concentrations on the growth of rhizobia and responses to added osmotica. J Appl Microbiol 86:889–898

    Article  CAS  Google Scholar 

  • Alexandre A, Oliveira S (2013) Response to temperature stress in rhizobia. Crit Rev Microbiol 39:219–228

    Article  CAS  PubMed  Google Scholar 

  • Athar M, Johnson DA (1997) Effects of drought on the growth and survival of Rhizobium meliloti strains from Pakistan and Nepal. J Arid Environ 35:335–340

    Article  Google Scholar 

  • Bernard T, Pocard JA, Perround B, Le Rudulier D (1986) Variations in the response of salt-stressed Rhizobium strains to betaines. Arch Microbiol 143:359–364

    Article  CAS  Google Scholar 

  • Bhattacharya I, Das HR (2003) Cell surface characteristics of two halotolerant strains of Sinorhizobium meliloti. Microbiol Res 158:187–194

    Article  CAS  PubMed  Google Scholar 

  • Bianco C, Imperlini E, Calogero R, Senatore B, Amoresano A et al (2006) Indole-3-acetic acid improves Escherichia coli’s defences to stress. Arch Microbiol 185:373–382

    Article  CAS  PubMed  Google Scholar 

  • Biswas S, Das RH, Sharma GL (2008) Isolation and characterization of a novel cross-infective rhizobial from Sesbania aculeata (Dhaincha). Curr Microbiol 56:48–54

    Article  CAS  PubMed  Google Scholar 

  • Bittner AN, Foltz A, Oke V (2007) Only one of five groEL genes is required for viability and successful symbiosis in Sinorhizobium meliloti. J Bacteriol 189:1884–1889

    Article  CAS  PubMed  Google Scholar 

  • Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49:359–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouhmouch I, Souad-Mouhsine B, Brhada F (2005) Influence of host cultivars and Rhizobium species on the growth and symbiotic performance of Phaseolus vulgaris under salt stress. J Plant Physiol 162:1103–1113

    Article  CAS  PubMed  Google Scholar 

  • Brígido C, Alexandre A, Oliveira S (2012) Transcriptional analysis of major chaperone genes in salt-tolerant and salt-sensitive mesorhizobia. Microbiol Res 167:623–629

    Article  PubMed  CAS  Google Scholar 

  • Brockwell J, Bottomly PJ, Thies JA (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility. A critical assessment. Plant Soil 174:143–180

    Article  CAS  Google Scholar 

  • Chen H, Richardson AE, Rolfe BG (1993) Studies of the physiology and genetic basis of acid tolerance in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 59:1798–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen WM, Lee TM, Lan CC, Cheng CP (2000) Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol Ecol 34:9–16

    Article  CAS  PubMed  Google Scholar 

  • Chen LS, Figueredo A, Pedrosa FO, Hungria M (2002) Genetic characterization of soybean rhizobia in Paraguay. Appl Environ Microbiol 66:5099–5103

    Article  Google Scholar 

  • Cheng HP, Walker GC (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol 180:20–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordovilla MP, Ligero F, Lluch C (1999) Effect of salinity on growth, nodulation and nitrogen assimilation in nodules of faba bean (Vicia faba L.). Appl. Soil Ecol 11:1–7

    Article  Google Scholar 

  • Cunningham SD, Munns DN (1984) The correlation of the exopolysaccharide production and acid-tolerance in Rhizobium. Soil Sci Soc Am J 48:1273–1276

    Article  CAS  Google Scholar 

  • Domínguez-Ferreras A, Soto MJ, Pérez-Arnedo R, Olivares J, Sanjuán J (2009) Importance of trehalose biosynthesis for Sinorhizobium meliloti osmotolerance and nodulation of alfalfa roots. J Bacteriol 191:7490–7499

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dowling DN, Broughton WJ (1986) Competition for nodulation of legumes. Annu Rev Microbiol 40:131–157

    Article  CAS  PubMed  Google Scholar 

  • Duzan HM, Mabood F, Souleimanov A, Smith DL (2006) Nod Bj-V (C18:1, MeFuc) production by Bradyrhizobium japonicum (USDA110, 532C) at suboptimal growth temperatures. J Plant Physiol 163:107–111

    Article  CAS  PubMed  Google Scholar 

  • Eva D, Helga A, Eva SB, Jozesf F, Fodor FB et al (2004) Aluminum toxicity, Al tolerance and oxidative stress in an Al- sensitive wheat genotype and in Al-tolerant lines developed by in-vitro microspore selection. Plant Sci 166:583–591

    Article  CAS  Google Scholar 

  • Fenner BJ, Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (2004) Sinorhizobium medicae genes whose regulation involves the ActS and/or ActR signal transduction proteins. FEMS Microbiol Lett 236:21–31. https://doi.org/10.1016/j.femsle.2004.05.016

    Article  CAS  PubMed  Google Scholar 

  • Foster JW (2000) Microbial responses to acid stress. In: Storz G, Hengge-Aronis R (eds) Bacterial stress response. ASM Press, Washington, DC, pp 9–115

    Google Scholar 

  • Frank B (1889) Ueber die Pilzsymbiose der Leguminosen. Ber Dtsch Bot Ges 7:332–346

    Google Scholar 

  • Fujihara S, Yoneyama T (1993) Effects of pH and osmotic stress on cellular polyamine contents in the soybean Rhizobia fredii P220 and Bradyrhizobium japonicum A1017. Appl Environ Microbiol 59:1104–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girvin R (2010) Effects of saline and alkaline stress on germination, seedling growth, and ion balance in wheat. Agron J 102:1252–1260. https://doi.org/10.2134/agronj2010.0022

    Article  CAS  Google Scholar 

  • Glenn AR, Dilworth MJ (1994) The life of root nodule Bacteria in the acidic underground. FEMS Microbiol Lett 123:1–10

    Article  CAS  Google Scholar 

  • Glenn AR, Reeve WG, Tiwari RP, Dilworth MJ (1999) Acid tolerance in root nodule bacteria. Novartis Found Symp 221:112–126

    CAS  PubMed  Google Scholar 

  • Graham PH (1992) Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil condition. Can J Microbiol 38:475–484

    Article  CAS  Google Scholar 

  • Gustafson AM, O’Connell KP, Thomashow MF (2002) Regulation of Sinorhizobium meliloti 1021 rrnA-reporter gene fusions in response to cold shock. Can J Microbiol 48:821–830

    Article  CAS  PubMed  Google Scholar 

  • Hashem FM, Swelim DM, Kuykendall LD, Mohamed AI, Abdel-Wahab SM et al (1998) Identification and characterization of salt- and thermo-tolerant Leucaena-nodulating Rhizobium strains. Biol Fertil Soil 27:335–341

    Article  CAS  Google Scholar 

  • Hawkins JP, Geddes BA, Oresnik IJ (2017) Succinoglycan production contributes to acidic pH tolerance in Sinorhizobium meliloti Rm1021. Mol Plant-Microbe Interact 30(12):1009–1019. https://doi.org/10.1094/MPMI-07-17-0176-R

    Article  CAS  PubMed  Google Scholar 

  • Hellweg C, Pühler A, Weidner S (2009) The time course of the transcriptomic response of Sinorhizobium meliloti 1021 following a shift to acidic pH. BMC Microbiol 9:37. https://doi.org/10.1186/1471-2180-9-37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

    Article  CAS  Google Scholar 

  • Hirsch AM (1992) Developmental biology of legume nodulation. New Phytol 122:211–237

    Article  Google Scholar 

  • Howieson J, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem 36:1261–1273

    Article  CAS  Google Scholar 

  • Howieson JG, Ewing MA, D’Antuono MF (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105(2):179–188

    Google Scholar 

  • Howieson JG, Robson AD, Abbott LK (1992) Acid-tolerant species of Medicago produce root exudates at low pH which induce the expression of nodulation genes in Rhizobium meliloti. Aust J Plant Physiol 19:287–296

    CAS  Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164

    Article  Google Scholar 

  • Idrissi MME, Aujjar N, Dessaux Y, FilalingMaltouf A (1996) Characterization of rhizobia isolated from Carob tree (Ceratonia siliqua). J Appl Biotechnol 80:165–173

    Google Scholar 

  • Islam R, Ghoulam W (1981) Screening of several strains of faba bean Rhizobium for tolerance to salinity. FABIS-Newslett (ICARDA) 3:34

    Google Scholar 

  • Jenkins MB (2003) Rhizobial and bradyrhizobial symbionts of mesquite from the Sonoran Desert: salt tolerance, facultative halophily and nitrate respiration. Soil Biol Biochem 35:1675–1682

    Article  CAS  Google Scholar 

  • Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169(1):83–98

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Bacteriol 272:196–202

    CAS  Google Scholar 

  • Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: tolerance of high temperature and antibiotic resistance. Plant Soil 112:115–122

    Google Scholar 

  • Kiss E, Huguet T, Poinsot V, Batut J (2004) The typA is required for stress adaptation as well as for Symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Mol Plant-Microbe Interact 17:235–244

    Article  CAS  PubMed  Google Scholar 

  • Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR et al (2015) Rhizobial symbiosis effect on the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress. Environ Sci Pollut Res 22:12479–12489

    Article  CAS  Google Scholar 

  • Kosanke JW, Osburn RM, Smith RS, LiphaTech Inc (1999) Process for preparation of bacterial agricultural products. Canadian patent 2,073:507

    Google Scholar 

  • Kulkarni S, Nautiyal CS (2000) Crossing the limits of Rhizobium existence in extreme conditions. Curr Microbiol 41:402–409

    Article  CAS  PubMed  Google Scholar 

  • Kurchak ON, Provorov NA, Simarov BV (2001) Plasmid pSym1-32 of Rhizobium leguminosarum bv. viceae controlling nitrogen fixation activity, effectiveness of Symbiosis, competitiveness and acid tolerance. Russian J Genet 37:1025–1031

    Article  CAS  Google Scholar 

  • Laranjo M, Oliveira S (2011) Tolerance of Mesorhizobium type strains to different environmental stresses. Anton Leeuw 99:651–662

    Article  CAS  Google Scholar 

  • Li Z, Zu C, Wang C, Yang J, Yu H et al (2016) Different responses of rhizosphere and non-rhizosphere soil microbial communities to consecutive Piper nigrum L. monoculture. Sci Rep 6(1):35825. https://doi.org/10.1038/srep35825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lilienfein J, Qualls RG, Uselman SM, Bridgham SD (2003) Soil formation and organic matter accretion in a young andesitic chronosequence at Mt. Shasta, California. Geoderma 116:249–264

    Article  CAS  Google Scholar 

  • Lloret J, Bolanos L, Mercedes LM, Peart JM, Brewin NJ et al (1995) Ionic stress and osmotic pressure induce different alterations in the lipopolysaccharide of a Rhizobium meliloti strain. Appl Environ Microbiol 61:3701–3704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloret J, Wulff B, Rubio JM, Downie JA, Bonilla I et al (1998) Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl Environ Microbiol 64:1024–1028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowendorf HS, Baya AM, Alexander M (1981) Survival of Rhizobium in acid soils. Appl Environ Microbiol 42:951–957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567

    Article  CAS  PubMed  Google Scholar 

  • Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169:609–615

    Article  CAS  PubMed  Google Scholar 

  • Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean-nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Münchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in rhizobia. J Bacteriol 181:83–90

    Article  PubMed  PubMed Central  Google Scholar 

  • Natera SHA, Guerreiro N, Djordjevic MA (2000) Proteome analysis of differentially displayed proteins as a tool for the investigation of Symbiosis. Mol Plant Microbe Interact 13:995–1009

    Article  CAS  PubMed  Google Scholar 

  • Netzer WJ, Hartl FU (1998) Protein folding in the cytosol: chaperonin- Dependent and independent mechanisms. Trends Biochem Sci 23:68–73

    Article  CAS  PubMed  Google Scholar 

  • O’Hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl Environ Microbiol 55:1870–1876

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogutcu H, Algur ÖF, Elkoca E, Kantar F (2008) The determination of symbiotic effectiveness of rhizobium strains isolated from wild chickpea collected from high altitudes in Erzurum. Turk J Agric For 32:241–248

    CAS  Google Scholar 

  • OsangAlfiana LO, Alexander M (1982) Differences among cowpea Rhizobium in tolerance to high temperature and desiccation in soil. Appl Environ Microbiol 43:435–439

    Article  Google Scholar 

  • Panoff JM, Corroler D, Thammavongs B, Boutibonnes P (1997) Differentiation between cold shock proteins and cold acclimation proteins in a mesophilic gram-positive bacterium, Enterococcus faecalis JH2-2. J Bacteriol 179:4451–4454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peoples MB (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agriculture production. Plant Soil 174:3–28

    Article  CAS  Google Scholar 

  • Phadtare S, Yamanaka K, Inouye M (2000) The cold shock response. In: Storz G, Hengge-Aronis R (eds) Bacterial stress response. ASM Press, Washington, DC, pp 33–45

    Google Scholar 

  • Prajakta BM, Suvarna PP, Singh RP, Rai AR (2019) Potential biocontrol and superlative plant growth promoting activity of indigenous Bacillus mojavensis PB-35(R11) of soybean (Glycine max) rhizosphere. SN Appl Sci 1:1143. https://doi.org/10.1007/s42452-019-1149-1

    Article  CAS  Google Scholar 

  • Rao DLN, Sharma PC (1995) Alleviation of salinity stress in chickpea by Rhizobium inoculation or nitrate supply. Biol Plant 37:405–410

    Article  Google Scholar 

  • Reeve WG, Tiwari RP, Wong CM, Dilworth MJ, Glenn AR (1998) The transcriptional regulator gene phrR in Sinorhizobium meliloti WSM419 is regulated by low pH and other stresses. Microbiology 144:3335–3342

    Google Scholar 

  • Reeve WG, Bräu L, Castelli J, Garau G, Sohlenkamp C et al (2006) The Sinorhizobium medicae WSM419 lpiA gene is transcriptionally activated by FsrR and required to enhance survival in lethal acid conditions. Microbiology 152:3049–3059

    Article  CAS  PubMed  Google Scholar 

  • Rehman A, Nautiyal CS (2002) Effect of drought on the growth and survival of the stress-tolerant bacterium Rhizobium sp. NBRI2505 sesbania and its drought-sensitive transposon Tn5 mutant. Curr Microbiol 45(5):368–377

    Article  CAS  PubMed  Google Scholar 

  • Rhijn PV, Vanderleyden J (1995) The rhizobium -plant Symbiosis. Microbiol Rev 59(1):124–142

    Article  PubMed  PubMed Central  Google Scholar 

  • Riccillo PM, Muglia CJ, de Bruijn FJ, Roe AJ, Booth IR (2000) Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J Bacteriol 182:1748–1753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruberg S, Tian ZX, Krol E, Linke B, Meyer F (2003) Construction and validation of a Sinorhizobium meliloti whole genome DNA microarray: genome-wide profiling of osmoadaptive gene expression. J Biotechnol 106:255–268

    Article  CAS  PubMed  Google Scholar 

  • Salema MP, Parker CA, Kirby DK, Chatel DL (1982) Death of rhizobia on inoculated seed. Soil Biol Biochem 14:13–14

    Article  Google Scholar 

  • Sanja K, Hulak N, Sikora S (2016) Environmental stress response and adaptation mechanisms in rhizobia. Agric Conspec Sci 81(1):15–19

    Google Scholar 

  • Santos H, da Costa MS (2002) Compatible solutes of organisms that live in hot saline environments. Environ Microbiol 20024:501–509

    Article  Google Scholar 

  • Santos R, Herouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in rhizobium-legume symbiosis. Mol Microbiol 38:750–759

    Google Scholar 

  • Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50(1):11–16

    Google Scholar 

  • Shamseldin A, Nyalwidhe J, Werner DA (2006) Proteomic approach towards the analysis of salt tolerance in Rhizobium etli and Sinorhizobium meliloti strains. Curr Microbiol 52:333–339

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Singh RN, Srivastava AK, Kumar S, Dubey RC et al (2011) Structural analysis and 3D-modelling of fur protein from Bradyrhizobium japonicum. J Appl Sci Environ Sanit 6(3):357–366

    CAS  Google Scholar 

  • Singh RP, Manchanda G, Singh RN, Srivastava AK, Dubey RC (2016) Selection of alkalotolerant and symbiotically efficient chickpea nodulating rhizobia from North-West Indo Gangetic Plains. J Basic Microbiol 56:14–25. https://doi.org/10.1002/jobm.201500267

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Manchanda G, Anwar MN, Zhang JJ, Li YZ (2017a) Mycorrhiza – helping plants to navigate environmental stresses. In: Kashyap PL, Srivastava AK, Tiwari SP, Kumar S (eds) Microbes for climate resilient agriculture. https://doi.org/10.1002/9781119276050.ch10

    Chapter  Google Scholar 

  • Singh RP, Manchanda G, Li ZF, Rai AR (2017b) Insight of proteomics and genomics in environmental bioremediation. In: Bhakta JN (ed) Handbook of research on inventive bioremediation techniques. IGI Global, Hershey. https://doi.org/10.4018/978-1-5225-2325-3

    Chapter  Google Scholar 

  • Singh RP, Manchanda G, Maurya IK, Maheshwari NK, Tiwari PK et al (2019) Streptomyces from rotten wheat straw endowed the high plant growth potential traits and agro-active compounds. Biocatal Agric Biotechnol 17:507–513. https://doi.org/10.1016/j.bcab.2019.01.014

    Article  Google Scholar 

  • Singh RP, Manchanda G, Yang Y, Singh D, Srivastava AK et al (2020) Deciphering the factors for nodulation and Symbiosis of Mesorhizobium associated with Cicer arietinum in Northwest India. Sustainability 12:1–17

    Article  CAS  Google Scholar 

  • Singleton PW, Elswaify SA, Bohlool BB (1982) Effect of salinity on rhizobium growth and survival. Appl Environ Microbiol 44:884–890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith RS (1992) Legume inoculant formulation and application. Can J Microbiol 38:485–492

    Article  Google Scholar 

  • Soussi M, Ocana A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J Exp Bot 49:1329–1337

    Google Scholar 

  • Soussi M, Khadri M, Lluch C, Ocana A (2001) Carbon metabolism and bacteroid respiration in nodules of chick-pea (Cicer arietinum L.) plants grown under saline conditions. Plant Biosyst 135:157–164

    Article  Google Scholar 

  • Subhashini DV, Singh RP, Manchanda G (2017) OMICS approaches: tools to unravel microbial systems. Directorate of Knowledge Management in Agriculture, Indian Council of Agricultural Research. ISBN: 9788171641703. https://books.google.co.in/books?id=vSaLtAEACAAJ

  • Surange S, Wollum AG, Kumar N, Nautiyal CS (1997) Characterisation of Rhizobium from root nodules of leguminous trees growing in alkaline soils. Can J Microbiol 43:891–894

    Article  CAS  Google Scholar 

  • Thorne SH, Williams HD (1997) Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance and changes in macromolecular synthesis during entry to and exit from stationary phase. J Bacteriol 179:6894–6901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (1996a) An essential role for actA in acid tolerance of Rhizobium meliloti. Microbiology 142:601–610

    Article  CAS  PubMed  Google Scholar 

  • Tiwari RP, Reeve WG, Dilworth MJ, Glenn AR (1996b) Acid tolerance in Rhizobium meliloti strain WSM419 involves a two- component sensor-regulator system. Microbiology 142:1693–1704

    Article  CAS  PubMed  Google Scholar 

  • Trotman AP, Weaver RW (1995) Tolerance of clover rhizobia to heat and desiccation stresses in soil. Soil Sci Soc Am J 59:466–470

    Article  CAS  Google Scholar 

  • Tu JC (1981) Effect of salinity on rhizobium-root hair interaction, nodulation and growth of soybean. Can J Plant Sci 61:231–239

    Article  Google Scholar 

  • Vincent JM, Thompson JA, Donovan KO (1962) Death of root- nodule bacteria on drying. Aust J Agric Res 13:258–270

    Article  Google Scholar 

  • Vinuesa P, Neumann-Silkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E et al (2003) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol Plant-Microbe Interact 16:159–168. https://doi.org/10.1094/MPMI.2003.16.2.159

    Article  CAS  PubMed  Google Scholar 

  • Vivas-Marfisi A, Tiwari R, Dilworth M, Glenn A (2002) In nitrogen fixation: from molecules to crop productivity. In: Pedrosa FO, Hungria MY, Geoffrey N, William E (eds) Current plant science and biotechnology in agriculture. Ch. 272, vol 38. Kluwer Academic, New York, pp 487–487

    Google Scholar 

  • Vriezen JAC, De Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73(11):3451–3459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallington EJ, Lund PA (1994) Rhizobium leguminosarum Contains Multiple Chaperonin (cpn60) Genes. Microbiology 140:113–122

    Article  CAS  PubMed  Google Scholar 

  • Wang XP, Chen WC, Ying Z, Han JY, Jing Y et al (2012) Comparison of adaptive strategies of alfalfa (Medicago sativa L.) to salt and alkali stresses. Aust J Crop Sci 6:309–315

    CAS  Google Scholar 

  • Watkin ELJ, O’Hara GW, Glenn AR (2003) Physiological responses to acid stress of an acid-soil tolerant and an acid-soil sensitive strain of Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 35:621–624

    Article  CAS  Google Scholar 

  • Wdowiak-Wróbel S, Leszcz A, Małek W (2013) Salt tolerance in Astragalus cicer microsymbionts: the role of glycine betaine in osmoprotection. Curr Microbiol 66:428–436

    Article  PubMed  CAS  Google Scholar 

  • Yang CW, Wang P, Li CY, Shi DC, Wang DL (2008) Comparison of effects of salt and alkali stresses on the growth and photosynthesis of wheat. Photosynthetica 46:107–114. https://doi.org/10.1007/s11099-008-0018-8

    Article  CAS  Google Scholar 

  • Yelton MM, Yang SS, Edie SA, Lim ST (1983) Characterization of an effective salt-tolerant, fast-growing strain of Rhizobium japonicum. Microbiology 129:1537–1547

    Article  Google Scholar 

  • Yura T, Kanemori M, Morita MT (2000) The heat shock response: regulation and function. In: Storz G, Hengge- Aronis R (eds) Bacterial stress response. ASM Press, Washington, DC, pp 3–18

    Google Scholar 

  • Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63(4):968–989

    Google Scholar 

  • Zhang F, Lynch DH, Smith DL (1995) Impact of low root temperatures in soybean [Glycine max (L) Merr] on nodulation and nitrogen fixation. Environ Exp Bot 35:279–285

    Article  Google Scholar 

  • Zhang H, Prithiviraj B, Charles TC, Driscoll BT, Smith DL (2003) Low temperature tolerant Bradyrhizobium japonicum strains allowing improved nodulation and nitrogen fixation of soybean in a short season (cool spring) area. Eur J Agron 19:205–213

    Article  CAS  Google Scholar 

  • Zhang JJ, Jing XY, de Lajudie P, Ma C, He PX et al (2016a) Association of white clover (Trifolium repens L.) with rhizobia of sv. trifolii belonging to three genomic species in alkaline soils in North and East China. Plant Soil 407:417–427

    Article  CAS  Google Scholar 

  • Zhang JJ, Yang X, Chen G, de Lajudie P, Singh RP et al (2016b) Mesorhizobium muleiense and Mesorhizobium gsp. nov. are symbionts of Cicer arietinum L. in alkaline soils of Gansu, Northwest China. Plant Soil 410:103–112

    Article  CAS  Google Scholar 

  • Zhang JJ, Xu Y, Guo C, de Lajudie P, Singh RP, Wang E, Chen W (2017) Mesorhizobium muleienseand Mesorhizobium gsp. nov. are symbionts of Cicer arietinum L. in alkaline soils of Gansu, Northwest China. Plant Soil 410(1–2):103–112

    Google Scholar 

  • Zou N, Dart PJ, Marcar NE, Bushby HVA (1995a) Interaction of salinity and rhizobial strain on growth and nitrogen fixation by Acacia ampliceps. Soil Biol Biochem 27:409–413

    Article  CAS  Google Scholar 

  • Zou N, Dart PJ, Marcar NE, Bushby HVA (1995b) Interaction of salinity and rhizobial strain on growth and nitrogen fixation by Acacia ampliceps. Soil Biol Biochem 27:4094–4013

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Food and Bioengineering, Zhengzhou University of Light Industry, Zhengzhou, Henan Province, People’s Republic of China

    Junjie Zhang, Chen Guo, Yimin Shang & Shanshan Peng

  2. Collaborative Innovation Center for Food Production and Safety of Henan Province, Zhengzhou, Henan Province, People’s Republic of China

    Junjie Zhang

  3. Department of Microbiology, V.B.S. Purvanchal University, Jaunpur, Uttar Pradesh, India

    Dipti Singh

Authors
  1. Junjie Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dipti Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chen Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yimin Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shanshan Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Research & Development, Uttaranchal University, Dehradun, Uttarakhand, India

    Raghvendra Pratap Singh

  2. Department of Botany and Environmental Studies, DAV University, Jalandhar, Punjab, India

    Geetanjali Manchanda

  3. Department of Microbial Biotechnology, Panjab University, Chandigarh, Chandigarh, India

    Indresh Kumar Maurya

  4. Faculty of Life Science and Technology, Kunming University of Science and Technology, Xishan, Yunnan, China

    Yunlin Wei

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Zhang, J., Singh, D., Guo, C., Shang, Y., Peng, S. (2020). Rhizobia at Extremes of Acidity, Alkalinity, Salinity, and Temperature. In: Singh, R., Manchanda, G., Maurya, I., Wei, Y. (eds) Microbial Versatility in Varied Environments. Springer, Singapore. https://doi.org/10.1007/978-981-15-3028-9_4

Download citation

Publish with us

Policies and ethics

Search

Navigation