Skip to main content
SpringerLink
Log in

Regulation of nodule number by GmNORK is dependent on expression of GmNIC in soybean

  • Published:
Agroforestry Systems Aims and scope Submit manuscript

Abstract

Root nodules are highly organized root organs where nitrogen fixation takes place in, and its formation are the results of complicated interactions between legumes and rhizobia. Nodule number is tightly controlled by Legumes to ensure optimal growth without energy loses wasted by excessive number of nodules. One of major factors controlling of nodule number is nitrate availability in the soil. However, during symbiotic development, the details of Nod factor signaling associated with nitrate regulation of nodulation are unknown. NORK, the immediately downstream component of these Nod factor receptors is central to the Nod factor signaling. NIC1, a CLE peptide-encoding gene in soybean (Glycine max), play an important role in nitrate regulation of nodulation. In this study, specified RNAi construct of GmNORK was generated and transformed into soybean roots by agrobacterium rhizogenes-mediated hairy root transformation. We found that the nodule number decreased substantially in GmNORK knock-down soybean transgenic roots. The expression levels of GmNIC1 in the GmNORK RNAi soybean transgenic roots is substantially reduced after rhizobial inoculation compared with the control soybean transgenic roots. Our data suggest that nitrate regulation of nodulation was affected by Nod factor signaling during nodule development in soybean, providing valuable information toward understanding the functions of GmNORK and GmNIC1 in symbiotic signaling and nodule development.

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

Similar content being viewed by others

References

  • Antolin-Llovera M, Ried MK, Binder A, Parniske M (2012) Receptor kinase signaling pathways in plant–microbe interactions. Annu Rev Phytopathol 50:451–473

    Article  CAS  Google Scholar 

  • Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Gherardi M, Huguet T, Geurts R, Dénarié J, Rougé P, Gough C (2006) The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–279

    Article  CAS  Google Scholar 

  • Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182:5641–5652

    Article  CAS  Google Scholar 

  • Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M (2005) SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102:10369–10374

    Article  CAS  Google Scholar 

  • Cole MA, Elkan GH (1973) Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob Agents Chemother 4:248–253

    Article  CAS  Google Scholar 

  • Emerich DW, Krishnan HB (2014) Symbiosomes: temporary moonlighting organelles. Biochem J 460:1–11

    Article  CAS  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  Google Scholar 

  • Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16:374–381

    CAS  PubMed  Google Scholar 

  • Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441

    Article  CAS  Google Scholar 

  • Gonzalez-Guerrero M, Matthiadis A, Saez AN, Long TA (2014) Fixating on metals: new insights into the role of metals in nodulation and symbiotic nitrogen fixation. Front Plant Sci 5:45

    Article  Google Scholar 

  • Govindarajulu M, Kim SY, Libault M, Berg RH, Tanaka K, Stacey G, Taylor CG (2009) GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 149:994–1004

    Article  CAS  Google Scholar 

  • Halverson LJ, Stacey G (1986) Effect of lectin on nodulation by wild-type Bradyrhizobium japonicum and a nodulation-defective mutant. Appl Environ Microbiol 51:753–760

    Article  CAS  Google Scholar 

  • Hogg BV, Cullimore JV, Ranjeva R, Bono JJ (2006) The DMI1 and DMI2 early symbiotic genes of medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol 140:365–373

    Article  CAS  Google Scholar 

  • Indrasumunar A, Kereszt A, Searle I, Miyagi M, Li D, Nguyen CD, Men A, Carroll BJ, Gresshoff PM (2010) Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol 51:201–214

    Article  CAS  Google Scholar 

  • Indrasumunar A, Wilde J, Hayashi S, Li D, Gresshoff PM (2015) Functional analysis of duplicated Symbiosis Receptor Kinase (SymRK) genes during nodulation and mycorrhizal infection in soybean (Glycine max). J Plant Physiol 176:157–168

    Article  CAS  Google Scholar 

  • Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet EP, Duc G, Gojon A, Lepetit M, Salon C (2010) Adaptation of Medicago truncatulato nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytol 185:817–828

    Article  CAS  Google Scholar 

  • Kevei Z, Lougnon G, Mergaert P, Horvath GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, Ane JM (2007) 3-Hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:3974–3989

    Article  CAS  Google Scholar 

  • Libault M, Zhang XC, Govindarajulu M, Qiu J, Ong YT, Brechenmacher L, Berg RH, Hurley-Sommer A, Taylor CG, Stacey G (2010) A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis. Plant J 62:852–864

    Article  CAS  Google Scholar 

  • Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102:10375–10380

    Article  CAS  Google Scholar 

  • Loh JT, Yuen-Tsai JP, Stacey MG, Lohar D, Welborn A, Stacey G (2001) Population density-dependent regulation of the Bradyrhizobium japonicum nodulation genes. Mol Microbiol 42:37–46

    Article  CAS  Google Scholar 

  • Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640

    Article  CAS  Google Scholar 

  • Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:10

    Article  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    Article  CAS  Google Scholar 

  • Oldroyd GE, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144

    Article  CAS  Google Scholar 

  • Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24:606–618

    Article  CAS  Google Scholar 

  • Riely BK, Ane JM, Penmetsa RV, Cook DR (2004) Genetic and genomic analysis in model legumes bring Nod-factor signaling to center stage. Curr Opin Plant Biol 7:408–413

    Article  CAS  Google Scholar 

  • Samaddar S, Dutta A, Sinharoy S, Paul A, Bhattacharya A, Saha S, Chien KY, Goshe MB, DasGupta M (2013) Autophosphorylation of gatekeeper tyrosine by symbiosis receptor kinase. FEBS Lett 587:2972–2979

    Article  CAS  Google Scholar 

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962

    Article  CAS  Google Scholar 

  • Toth K, Stratil TF, Madsen EB, Ye J, Popp C, Antolin-Llovera M, Grossmann C, Jensen ON, Schussler A, Parniske M, Ott T (2012) Functional domain analysis of the Remorin protein LjSYMREM1 in Lotus japonicus. PLoS ONE 7:e30817

    Article  CAS  Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805

    Article  CAS  Google Scholar 

  • Yoshida S, Parniske M (2005) Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J Biol Chem 280:9203–9209

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the PhD Start-up Fund of Natural Science Foundation under Grant No. 801100010121; Open fund project of State Key laboratory of Crop Genetics and Germplasm Enhancement under Grant No. ZW201706; Open fund project of oil crops biology and genetics and breeding key laboratory of Ministry of Agriculture under Grant No. 2016006. Open funds of State Key Laboratory of Agricultural Microbiology under Grant No. AMLKF201608.

Author information

Authors and Affiliations

  1. The College of Life Science, Yangtze University, Jingzhou, 434025, China

    Lijun Wang

  2. Tillage Institute, Heilongjiang Academic of Agriculture Sciences, Harbin, 150086, China

    Lingwei Deng

  3. Jingzhou No.1 People’s Hospital and First Affiliated Hospital of Yangtze University, Jingzhou, 434000, China

    Xue Bai

  4. Oil Crops Research Institute of Chinese Academic of Agriculture Sciences, Wuhan, 430062, China

    Yongqing Jiao

  5. The College of Life Science, Huazhong Agricultural University, Wuhan, 430070, China

    Yangrong Cao

  6. The State Key Laboratory of Crop Genetics and Germplasm Enhancement, Bioinformatics Center, Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, 210095, China

    Yufeng Wu

Authors
  1. Lijun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lingwei Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xue Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongqing Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yangrong Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yufeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LW, YW, YJ, YC, LD, and XB contributed equally to this work.

Corresponding authors

Correspondence to Lijun Wang, Yongqing Jiao, Yangrong Cao or Yufeng Wu.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Deng, L., Bai, X. et al. Regulation of nodule number by GmNORK is dependent on expression of GmNIC in soybean. Agroforest Syst 94, 221–230 (2020). https://doi.org/10.1007/s10457-019-00382-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10457-019-00382-8

Keywords

Search

Navigation