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Dynamic succession of chickpea rhizobia over years and sampling sites in Xinjiang, China

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Abstract

Aims

To investigate the succession of chickpea rhizobia over years and sampling sites.

Methods

Rhizobia were sampled four times from nodules of chickpea grown in four sites of Mulei County and Qitai County in Xinjiang, China during 2009–2016. The recA genes of rhizobia representing different populations were phylogenetically compared for their genotypic differentiation. Soil properties were examined to explore their hypothetical incidence on the rhizobial succession.

Results

The 628 isolates were all identified as Mesorhizobium muleiense, belonging to 28 genotypes distinguished by recA phylogeny. For each site, 15, 17, 10 and 7 genotypes were detected during the whole sampling period; while 4, 15, 12 and 17 genotypes were evidenced in each of the 4 sampling years (2009, 2013, 2015 and 2016) from all the four sites. Four major genotypes (T12 through T15) were found throughout the four years in the four sites at various frequencies. While the other genotypes were site and/or year specific. Both increased genetic diversity as revealed by Shannon-Weaver index and shifts in the population composition as revealed by genotyping were detected in the chickpea rhizobial populations during the study period. Nitrogen content, available phosphorus and potassium, and pH were the main factors correlated to the genotype distribution of chickpea rhizobia in the soil over years.

Conclusions

The genetic diversity of M. muleiense increased and the population composition shifted over years and at different sampling sites. The recA gene is an adequate molecular marker to estimate the intraspecific variation and succession of M. muleiense genotypes. The rhizobial genotype succession/evolution in the fields might be driven by the fluctuations of soil characteristics like nitrogen content, available phosphorus and potassium, and pH.

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References

  • Alexandre A, Brigido C, Laranjo M, Rodrigues S, Oliveira S (2009) Survey of chickpea rhizobia diversity in Portugal reveals the predominance of species distinct from Mesorhizobium ciceri and Mesorhizobium mediterraneum. Microb Ecol 58:930–941

    Article  PubMed  Google Scholar 

  • Armas-Capote N, Perez-Yepez J, Martinez-Hidalgo P, Garzon-Machado V, Del Arco-Aguilar M, Velazquez E, Leon-Barrios M (2014) Core and symbiotic genes reveal nine Mesorhizobium genospecies and three symbiotic lineages among the rhizobia nodulating Cicer canariense in its natural habitat (La Palma, Canary Islands). Syst Appl Microbiol 37:140–148

    Article  CAS  PubMed  Google Scholar 

  • Atlas RM, Bartha R (2001) Ecologıa Microbiana y Microbiologıa Ambiental (Spanish version of the 4th edn). Addison Wesley, Madrid, p 696

    Google Scholar 

  • Braak C, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: sofware for canonical community ordination (version 4.5). Section on permutation methods microcomputer power, Ithaca, Newyork

  • Cao Y, Wang ET, Zhao L, Chen WM, Wei GH (2014) Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem 78:128e137

    Article  Google Scholar 

  • Diaz Caballero J, Clark ST, Coburn B, Zhang Y, Wang PW, Donaldson SL, Tullis DE, Yau YC, Waters VJ, Hwang DM, Guttman DS (2015) Selective sweeps and parallel Pathoadaptation drive Pseudomonas aeruginosa evolution in the cystic fibrosis lung. mBio 6:e00981–e00915. https://doi.org/10.1128/mBio.00981-15

  • Duodu S, Nsiah EK, Bhuvaneswari TV, Svenning MM (2006) Genetic diversity of a natural population of Rhizobium leguminosarum biovar trifolii analysed from field nodules and by a plant infection technique. Soil Biol Biochem 38(5):1162–1165

    Article  CAS  Google Scholar 

  • Duodu S, Carlsson G, Huss-Danell K, Svenning MM (2007) Large genotypic variation but small variation in N2 fixation among rhizobia nodulating red clover in soils of northern Scandinavia. J Appl Microbiol 102:1625–1635

    Article  CAS  PubMed  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han L, Wang E, Han T, Liu J, Sui X, Chen W (2009) Unique community structure and biogeography of soybean rhizobia in the saline-alkaline soils of Xinjiang, China. Plant Soil 324:291–305

    Article  CAS  Google Scholar 

  • Harrison S, Young JPW, Jones DG (1987) Rhizobium population genetics: effect of clover variety and inoculum dilution on the genetic diversity sampled from natural populations. Plant Soil 103:147–150

    Article  Google Scholar 

  • Javaid AM, Muhammad K, Amer J (2011) Screening of Mesorhizobium ciceri isolates from rainfed area for improvement in growth and nodulation of chickpea seedlings under controlled conditions. Soil and. Environment 30:160–165

    Google Scholar 

  • Jukanti AK, Gaur PM, Gowda CL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutr 108(Suppl 1):S11–S26

    Article  CAS  PubMed  Google Scholar 

  • Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Li QQ, Wang ET, Zhang YZ, Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX (2011) Diversity and biogeography of rhizobia isolated from root nodules of glycine max grown in Hebei Province, China. Microb Ecol 61:917–931

    Article  PubMed  Google Scholar 

  • L'Taief B, Sifi B, Gtari M, Zaman-Allah M, Lachaal M (2007) Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Tunisia. Can J Microbiol 53:427–434

    Article  PubMed  Google Scholar 

  • Nandwani R, Dudeja SS (2009) Molecular diversity of a native mesorhizobial population of nodulating chickpea (Cicer arietinum L.) in Indian soils. J Basic Microbiol 49:463–470

    Article  CAS  PubMed  Google Scholar 

  • Nour SM, Cleyet-Marel JC, Beck D, Effosse A, Fernandez MP (1994) Genotypic and phenotypic diversity of Rhizobium isolated from chickpea (Cicer arietinum L.) Can J Microbiol 40:345–354

    Article  CAS  PubMed  Google Scholar 

  • Nour SM, Cleyet-Marel JC, Normand P, Fernandez MP (1995) Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int J Syst Bacteriol 45:640–648

    Article  CAS  PubMed  Google Scholar 

  • Odair A, Glaciela K, Mariangela H (2006) Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem 38(6):1298–1307

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL https://www.R-project.org/

    Google Scholar 

  • Rai R, Dash PK, Mohapatra T, Singh A (2012) Phenotypic and molecular characterization of indigenous rhizobia nodulating chickpea in India. Indian J Exp Biol 50:340–350

    CAS  PubMed  Google Scholar 

  • Rivas R, Laranjo M, Mateos PF, Oliveira S, Martinez-Molina E, Velazquez E (2007) Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett Appl Microbiol 44:412–418

    Article  CAS  PubMed  Google Scholar 

  • Romdhane BS, Tajini F, Trabelsi M, Aouani ME, Mhamdi R (2007) Competition for nodule formation between introduced strains of Mesorhizobium ciceri and the native populations of rhizobia nodulating chickpea (Cicer arietinum L.) in Tunisia. World J Microbiol Biotechnol 23:1195–1201

    Article  Google Scholar 

  • Rupela OP, Sudarshana MR (1990) Displacement of native rhizobia nodulating chickpea (Cicer arietinum L.) by an inoculant strain through soil solarization. Biol Fertil Soils 10:207–212

    Google Scholar 

  • Scholz HC, Witte A, Tomaso H, Dahouk SA, Neubauer H (2005) Genotyping of Chromobacterium violaceum isolates by recA PCR-RFLP analysis. FEMS Microbiol Lett 244:347–352

    Article  CAS  PubMed  Google Scholar 

  • Scholz HC, Tomaso H, Dahouk SA, Witte A, Schloter M, Kampfer P, Falsen E, Neubauer H (2006) Genotyping of Ochrobactrum anthropi by recA-based comparative sequence, PCR-RFLP, and 16S rRNA gene analysis. FEMS Microbiol Lett 257:7–16

    Article  CAS  PubMed  Google Scholar 

  • Singh F, Diwakar B (eds) (1995) Chickpea botany and production practices. ICRISAT Training andFellowships Program Patancheru 502 324, Andhra Pradesh, India

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Somasegaran P, Bohlool BB (1990) Single-strain versus multistrain inoculation: effect of soil mineral N availability on rhizobial strain effectiveness and competition for nodulation on chickpea, soybean, and dry bean. Appl Environ Microbiol 56:3298–3303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suleiman AKA, Manoeli L, Boldo JT, Pereira MG, Roesch LFW (2013) Shifts in soil bacterial community after eight years of land-use change. Syst Appl Microbiol 36:137–144

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tena W, Wolde-Meskel E, Degefu T, Walley F (2017) Genetic and phenotypic diversity of rhizobia nodulating chickpea (Cicer arietinum L.) in soils from southern and central Ethiopia. Can J Microbiol 63:690–707

    Article  CAS  PubMed  Google Scholar 

  • Terefework Z, Kaijalainen S, Lindstrom K (2001) AFLP fingerprinting as a tool to study the genetic diversity of Rhizobium galegae isolated from Galega orientalis and Galega officinalis. J Biotechnol 91:169–180

    Article  CAS  PubMed  Google Scholar 

  • Van Cauwenberghe J, Lemaire B, Stefan A, Efrose R, Michiels J, Honnay O (2016) Symbiont abundance is more important than pre-infection partner choice in a Rhizobium-legume mutualism. Syst Appl Microbiol 39(5):345–349

    Article  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of rootnodule bacteria. International Biological Programme, Blackwell, Oxford

  • Wei G, Chen W, Zhu W, Chen C, Young JPW, Bontemps C (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol Ecol 68:320–328

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Liu TY, Chen WF, Wang ET, Sui XH, Zhang XX, Li Y, Li Y, Chen WX (2012a) Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int J Syst Evol Microbiol 62:2737–2742

    Article  CAS  PubMed  Google Scholar 

  • Zhang JJ, Lou K, Jin X, Mao PH, Wang ET, Tian CF, Sui XH, Chen WF, Chen WX (2012b) Distinctive Mesorhizobium populations associated with Cicer arietinum L. in alkaline soils of Xinjiang, China. Plant Soil 353:123–134

    Article  CAS  Google Scholar 

  • Zhang YM, Li Y, Chen WF, Wang ET, Tian CF, Li QQ, Zhang YZ, Sui XH, Chen WX (2011) Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl Environ Microbiol 77:6331–6342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JJ, Yu T, Lou K, Mao PH, Wang ET, Chen WF, Chen WX (2014) Genotypic alteration and competitive nodulation of Mesorhizobium muleiense against exotic chickpea rhizobia in alkaline soils. Syst Appl Microbiol 37:520–524

    Article  PubMed  Google Scholar 

  • Zhang JJ, Yang X, Guo C, de Lajudie P, Singh RP, Wang ET, Chen WF (2017) 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 

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Acknowledgements

This work was financed by the National Natural Science Foundation of China (Project No. 31400008, 11575149 and 31571778), National human and social security ministry of science and technology for overseas returnees (Project No. 21104000005) and the Scientific Research Funds of Zhengzhou University of Light Industry (Project No. 2014bsjj006). Entao Wang is financially supported by grants SIP20171259 authorized by Instituto Politécnico Nacional, Mexico. Wenfeng Chen was supported financially from State Key Laboratory of Agrobiotechnology (2017SKLAB7-1).

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Authors and Affiliations

  1. College of Food and Bioengineering, Zhengzhou University of Light Industry, Zhengzhou, Henan province, 450000, People’s Republic of China

    Junjie Zhang, Chen Guo, Yimin Shang, Xu Yang & Jianqiang Zheng

  2. Collaborative Innovation Center for Food Production and Safety of Henan province, Zhengzhou, 450002, Henan Province, People’s Republic of China

    Junjie Zhang

  3. Collaborative Innovation Center of Environmental Pollution Control and Ecological Restoration, Zhengzhou, 450002, Henan Province, People’s Republic of China

    Junjie Zhang

  4. State Key Laboratory of Agrobiotechnology, Beijing, 100193, China

    Wenfeng Chen

  5. College of Biological Sciences and Rhizobium Research Center, China Agricultural University, Beijing, 100193, People’s Republic of China

    Wenfeng Chen

  6. IRD, LSTM, Campus de Baillarguet TA-A-82/J, 34398, Montpellier Cedex 5, France

    Philippe de Lajudie

  7. Institute of Ion Beam Biotechnology, College of Physics Science and Technology, Xinjiang University, Urumqi, Xinjiang, 830046, People’s Republic of China

    Peihong Mao

  8. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, D. F, 11340, México, Mexico

    En Tao Wang

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  1. Junjie Zhang
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  2. Chen Guo
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  6. Xu Yang
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  8. Jianqiang Zheng
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  9. En Tao Wang
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Correspondence to Junjie Zhang, Philippe de Lajudie or En Tao Wang.

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Zhang, J., Guo, C., Chen, W. et al. Dynamic succession of chickpea rhizobia over years and sampling sites in Xinjiang, China. Plant Soil 425, 241–251 (2018). https://doi.org/10.1007/s11104-018-3586-9

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