Skip to main content

Advertisement

SpringerLink
Log in

Nodulation and Genomic Capacity of a Novel High-Latitude Bradyrhizobium japonicum HLNEAU001

  • Research Article
  • Published:
Journal of Soil Science and Plant Nutrition Aims and scope Submit manuscript

Abstract

Rhizobium species are essential symbionts of legumes, participating in nitrogen fixation and having an important impact on the protein content of soybeans. In this study, we isolated Rhizobia from the soybean cultivar Suinong14 growing in a soybean field in Harbin (45.75° N, 126.53° E), which is situated within one of the three largest black soil belts in the world. One Bradyrhizobium japonicum strain (High-Latitude Northeast Agricultural University 001, HLNEAU001) was identified. Two hundred fifteen core soybean germplasms from Northeast China were screened for nodule traits, with the nodule number ranging from 0 to 95. Phylogenetic analysis showed that B. japonicum HLNEAU001 is closely related to B. japonicum USDA6 and B. diazoefficiens USDA110. A nodulation capacity analysis showed that B. japonicum HLNEAU001 formed more nodules than B. japonicum USDA6 or B. diazoefficiens USDA110, with 30 soybean germplasms being assayed for each strain. Using a draft genome sequence of B. japonicum HLNEAU001 to compare the genomic differences between B. japonicum HLNEAU001, B. japonicum USDA6 and B. diazoefficiens USDA110 showed that the three strains contain 5790 core genes. Because B. japonicum HLNEAU001 and B. japonicum USDA6 exhibited collinearity, the genomic differences between these two strains were further analysed. In addition to type IV and type VI secreted proteins, we hypothesize that type III effectors are the key factors underlying the nodulation capacity differences between B. japonicum HLNEAU001 and B. japonicum USDA6. The results of this study indicate that B. japonicum HLNEAU001 is a distinctive cold-region, slow-growing Rhizobium strain that is capable of effective symbiotic nitrogen fixation in cold regions and black soil and may play a pivotal role in sustainable agricultural production.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bladergroen MR, Badelt K, Spaink HP (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16:53–64

    Article  CAS  PubMed  Google Scholar 

  • Büttner D, Bonas U (2003) Common infection strategies of plant and animal pathogenic bacteria. Curr Opin Plant Biol 6:312–319

    Article  CAS  PubMed  Google Scholar 

  • Cao MM, Qiao LI, Zhang LY, Gao J, Wei-Hai LI, Ding WM, Sun YK (2014) Accumulated temperature variation and accumulated temperature rezone in Heilongjiang Province. Chin J Agrometeorol

  • Dai WJ, Zeng Y, Xie ZP, Staehelin C (2008) Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J Bacteriol 190:5101–5110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dâmiany PO, Marislaine AF, Bruno LS, Otávio HST, Fábio ADM, Márcia R et al (2017) Acid tolerant Rhizobium strains contribute to increasing the yield and profitability of common bean in tropical soils. J Soil Sci Plant Nutr 17:922–934

  • Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320

    Article  CAS  PubMed  Google Scholar 

  • Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9

    Article  CAS  PubMed  Google Scholar 

  • Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol 40:770

    Article  CAS  PubMed  Google Scholar 

  • Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194

    Article  CAS  PubMed  Google Scholar 

  • Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18

    Article  CAS  Google Scholar 

  • Hongkun Z, Yumin W, Fu X, Xiaodong L, Cuiping Y, Guangxun Q et al (2018) The genetic diversity and geographic differentiation of the wild soybean in Northeast China based on nuclear microsatellite variation. Int J Genomics 2018:1–9

    Google Scholar 

  • Hubber A, Vergunst A, Sullivan J, Hooykaas PJ, Ronson C (2004) Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 54:561–574

    Article  CAS  PubMed  Google Scholar 

  • Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jabbouri S, Fellay R, Talmont F, Kamalaprija P, Burger U, Relić B, Promé JC, Broughton WJ (1995) Involvement of nodS in N-methylation and nodU in 6-O-carbamoylation of Rhizobium sp. NGR234 Nod factors. J Biol Chem 270:22968–22973

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (supplement). DNA Res 9:225–256

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Maita H, Hirakawa H, Uchiike N, Minamisawa K, Watanabe A, Sato S (2011) Complete genome sequence of the soybean symbiont Bradyrhizobium japonicum strain USDA6T. Genes 2:763–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keyser HH, Griffin RF (1987) Beltsville hizobium culture collection catalog. Ars

  • Kneen BE, Larue TA (1983) Congo red absorption by Rhizobium leguminosarum. Appl Environ Microbiol 45:340–342

    CAS  PubMed  PubMed Central  Google Scholar 

  • López-Baena FJ, Ruiz-Sainz JE, Rodríguez-Carvajal MA, Vinardell JM (2016) Bacterial molecular signals in the Sinorhizobium fredii-soybean symbiosis. Int J Mol Sci 17:755

    Article  CAS  PubMed Central  Google Scholar 

  • Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252

    Article  CAS  PubMed  Google Scholar 

  • Pádua Oliveira D, Alves de Figueiredo M, Lima Soares B, Stivanin Teixeira OH, Dias Martins FA, Rufini M, Peixoto Chain C, Pereira Reis R, Ramalho de Morais A, de Souza Moreira FM, Bastos de Andrade MJ (2017) Acid tolerant rhizobium strains contribute to increasing the yield and profitability of common bean in tropical soils. JSSPN 17(4):922–934

    Google Scholar 

  • Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42

    Article  Google Scholar 

  • Reavy B, Bagirova S, Chichkova NV, Fedoseeva SV, Sang HK, Vartapetian AB, Taliansky ME (2007) Caspase-resistant VirD2 protein provides enhanced gene delivery and expression in plants. Plant Cell Rep 26:1215–1219

    Article  CAS  PubMed  Google Scholar 

  • Rellán-Álvarez R, Andaluz S, Rodríguez-Celma J, Wohlgemuth G, Zocchi G, Álvarez-Fernández A, Fiehn O, López-Millán AF, Abadía J (2010) Changes in the proteomic and metabolic profiles of Beta vulgaris root tips in response to iron deficiency and resupply. BMC Plant Biol 10:120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ritsema T, Wijfjes AHM, Lugtenberg BJJ, Spaink HP (1996) Rhizobium nodulation protein Noda is a host-specific determinant of the transfer of fatty acids in Nod factor biosynthesis. Mol Gen Genet MGG 251(1):44–51

    CAS  PubMed  Google Scholar 

  • Saghafi D, Ghorbanpour M, Lajayer AB (2018) Efficiency of Rhizobium strains as plant growth promoting rhizobacteria on morpho-physiological properties of Brassica napus L. under salinity stress. J Soil Sci Plant Nutr 18(1):253–268

  • Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quere A, Wollherr A et al (2009) Rhizobium sp. strain ngr234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75(12):4035–4045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzaki T, Kawaguchi M (2014) Root nodulation: a developmental program involving cell fate conversion triggered by symbiotic bacterial infection. Curr Opin Plant Biol 21:16

    Article  CAS  PubMed  Google Scholar 

  • Viprey V, Del GA, Golinowski W, Broughton WJ, Perret X (2010) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28:1381–1389

    Article  Google Scholar 

  • Wang JY, Wang R, Zhang YM, Liu HC, Chen WF, Wang ET, Sui XH, Chen WX (2013) Bradyrhizobium daqingense sp. nov. isolated from soybean nodules. Int J Syst Evol Microbiol 63(Pt 2):616–624

    Article  CAS  PubMed  Google Scholar 

  • Weisburg WG (1991) 16s ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen D, Liang W (2001) Soil fertility quality and agricultural sustainable development in the black soil region of Northeast China. Environ Dev Sustain 3(1):31–43

    Article  Google Scholar 

  • Yang FJ, Cheng LL, Zhang L, Dai WJ, Liu Z, Yao N, Xie ZP, Staehelin C (2009) Y4lO of Rhizobium sp. strain NGR234 is a symbiotic determinant required for symbiosome differentiation. J Bacteriol 191:735–746

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Li MM, Xu CJ, Yang X, Li DM, Zhao X et al (2018) Natural variation in GmGBP1 promoter affects photoperiod control of flowering time and maturity in soybean. Plant J 96:967–977

  • Zhu XC, Song FB, Xu HW (2010) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–131

Download references

Funding

The promote project for young talents of the colleges in Heilongjiang province (UNPYSCT-2016008). Financial support was received from The Ministry of Science and Technology of People’s Republic of China Project (2017YFE0111000); EUCLEG (727312); National Natural Science Foundation of China (31400074, 31271747, 31471516, 31401465, 31501332); National Key R&D Program of China (2016YFD0100500, 2016YFD0100300, 2016YFD0100201); Natural Science Foundation of Heilongjiang Province of China (Grant number ZD201213); Heilongjiang Postdoctoral Science Foundation (LBH-Q16014); Harbin Science Technology Project (2013RFQXJ005; 2014RFXXJ012) and Academic Backbon’ Project of Northeast Agricultural University (15XG02).

Author information

Author notes

  1. Yan Shi, Jianyi Li and Jinhui Wang contributed equally to this work.

Authors and Affiliations

  1. College of Agriculture, Key Laboratory of Soybean Biology in Chinese Ministry of Education, Northeast Agricultural University, College of Science, Harbin, 150030, People’s Republic of China

    Yan Shi, Jianyi Li, Jinhui Wang, Rongsheng Zhu, Shuping Li, Qingying Li, Lin Chen, Jingyi Zhu, Jianan Zou, Jieqi Wang, Huilin Chang, Chao Ma, Xueying Liu, Hongwei Jiang, Zhengong Yin, Zhenbang Hu, Xiaoxia Wu, Zhaoming Qi, Chunyan Liu, Dawei Xin & Qingshan Chen

  2. Crop Breeding Institute, Suihua branch of Heilongjiang Academy of Agricultural Sciences, Heilongjiang Academy of Agricultural Sciences, Harbin, Heilongjiang, China

    Huilin Chang & Zhengong Yin

Authors
  1. Yan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianyi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinhui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rongsheng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuping Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qingying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jingyi Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jianan Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jieqi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Huilin Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Chao Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Xueying Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Hongwei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Zhengong Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Zhenbang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Xiaoxia Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Zhaoming Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Chunyan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Dawei Xin
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Qingshan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhaoming Qi, Chunyan Liu, Dawei Xin or Qingshan Chen.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 497 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, Y., Li, J., Wang, J. et al. Nodulation and Genomic Capacity of a Novel High-Latitude Bradyrhizobium japonicum HLNEAU001. J Soil Sci Plant Nutr 19, 277–289 (2019). https://doi.org/10.1007/s42729-019-00027-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42729-019-00027-w

Keywords

Search

Navigation