Skip to main content

Advertisement

Springer Nature Link
Log in

Molecular characterization of NBS–LRR genes in the soybean Rsv3 locus reveals several divergent alleles that likely confer resistance to the soybean mosaic virus

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The divergence patterns of NBS – LRR genes in soybean Rsv3 locus were deciphered and several divergent alleles ( NBS_C, NBS_D and Columbia NBS_E ) were identified as the likely functional candidates of Rsv3.

Abstract

The soybean Rsv3 locus, which confers resistance to the soybean mosaic virus (SMV), has been previously mapped to a region containing five nucleotide binding site–leucine-rich repeats (NBS–LRR) genes (referred to as nbs_A–E) in Williams 82. In resistant cultivars, however, the number of NBS–LRR genes in this region and their divergence from susceptible alleles remain unclear. In the present study, we constructed and screened a bacterial artificial chromosome (BAC) library for an Rsv3-possessing cultivar, Zaoshu 18. Sequencing two positive BAC inserts on the Rsv3 locus revealed that Zaoshu 18 possesses the same gene content and order as Williams 82, but two of the NBS–LRR genes, NBS_C and NBS_D, exhibit distinct features that were not observed in the Williams 82 alleles. Obtaining these NBS-LRR genes from eight additional cultivars demonstrated that the NBS_A–D genes diverged into two different alleles: the nbs_A–D alleles were associated with the rsv3-type cultivars, whereas the NBS_A–D alleles were associated with the Rsv3-possessing cultivars. For the NBS_E gene, the cultivar Columbia possesses an allele (NBS_E) that differed from that in Zaoshu 18 and rsv3-type cultivars (nbs_E). Exchanged fragments were further detected on alleles of the NBS_C–E genes, suggesting that recombination is a major force responsible for allele divergence. Also, the LRR domains of the NBS_C–E genes exhibited extremely strong signals of positive selection. Overall, the divergence patterns of the NBS–LRR genes in Rsv3 locus elucidated by this study indicate that not only NBS_C but also NBS_D and Columbia NBS_E are likely functional alleles that confer resistance to SMV.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bernard RL, Nelson RL, Cremeens CR (1991) USDA soybean genetic collection: isoline collection. Soybean Genet Newsl 18:27–57

    Google Scholar 

  • Bouzidi MF, Franchel J, Tao QZ, Stormo K, Mraz A, Nicolas P, Mouzeyar S (2006) A sunflower BAC library suitable for PCR screening and physical mapping of targeted genomic regions. Theor Appl Genet 113:81–89

    Article  CAS  PubMed  Google Scholar 

  • Buss GR, Ma G, Chen P, Tolin SA (1997) Registration of V94-5152 soybean germplasm resistant to soybean mosaic potyvirus. Crop Sci 37:1987–1988

    Article  Google Scholar 

  • Buzzell RI, Tu JC (1989) Inheritance of a soybean stem-tip necrosis reaction to soybean mosaic-virus. J Hered 80:400–401

    Article  Google Scholar 

  • Cervantes-Martinez I, Chen P, Orazaly M, Klepadlo M (2015) Identification of a new allele at the Rsv3 locus for resistance to soybean mosaic virus in PI 61944 soybean accession. Crop Sci 55:999–1005

    Article  Google Scholar 

  • Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569

    Article  CAS  PubMed  Google Scholar 

  • Eitas TK, Dangl JL (2010) NB-LRR proteins: pair, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunduz I, Buss GR, Ma G, Chen P, Tolin SA (2001) Genetic analysis of resistance to soybean mosaic virus in OX670 and Harosoy soybean. Crop Sci 41:1785–1791

    Article  Google Scholar 

  • Gunduz I, Buss GR, Chen P, Tolin SA (2002) Characterization of SMV resistance genes in Tousan 140 and Hourei soybean. Crop Sci 42:90–95

    Article  PubMed  Google Scholar 

  • Hill JH, Bailey TB, Benner HI, Tachibana H, Durand DP (1987) Soybean mosaic virus: effects of primary disease incidence on yield and seed quality. Plant Dis 71:237–239

    Article  Google Scholar 

  • Innes RW, Ameline-Torregrosa C, Ashfield T, Cannon E, Cannon SB, Chacko B, Chen NW, Couloux A, Dalwani A, Denny R et al (2008) Differential accumulation of retroelements and diversification of NBLRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean. Plant Physiol 148:1740–1759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeong SC, Kristipati S, Hayes AJ, Maughan PJ, Noffsinger SL, Gunduz I, Buss GR, Maroof MAS (2002) Genetic and sequence analysis of markers tightly linked to the soybean mosaic virus resistance gene, Rsv3. Crop Sci 42:265–270

    CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kiihl RAS, Hartwig EE (1979) Inheritance of reaction to soybean mosaic-virus in soybeans. Crop Sci 19:372–375

    Article  Google Scholar 

  • Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuang H, Caldwell KS, Meyers BC, Michelmore RW (2008) Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J 54:69–80

    Article  CAS  PubMed  Google Scholar 

  • Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 20:116–122

    Article  CAS  PubMed  Google Scholar 

  • Li N, Yin JL, Li C, Wang DG, Yang YQ, Karthikeyan A, Luan HX, Zhi HJ (2016) NB-LRR gene family required for Rsc4-mediated resistance to Soybean mosaic virus. Crop Pasture Sci 67:541–552

    Article  CAS  Google Scholar 

  • Liao L, Chen P, Buss GR, Yang Q, Tolin SA (2002) Inheritance and allelism of resistance to soybean mosaic virus in Zao18 soybean from China. J Hered 93:447–452

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genet Genomics 34:765–776

    Article  PubMed  Google Scholar 

  • Ma G, Chen P, Buss GR, Tolin SA (2002) Complementary action of two independent dominant genes in Columbia soybean for resistance to soybean mosaic virus. J Hered 93:179–184

    Article  CAS  PubMed  Google Scholar 

  • Ma FF, Wu XY, Chen YX, Liu YN, Shao ZQ, Wu P, Wu M, Liu CC, Wu WP, Yang JY, Li DX, Chen JQ, Wang B (2016) Fine mapping of the Rsv1-h gene in the soybean cultivar Suweon 97 that confers resistance to two Chinese strains of the soybean mosaic virus. Theor Appl Genet 129:2227–2236

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1: vev003

  • McDowell JM, Simon SA (2006) Recent insights into R gene evolution. Mol Plant Pathol 7:437–448

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130

    Article  CAS  PubMed  Google Scholar 

  • Redekar NR, Clevinger EM, Laskar MA, Biyashev RM, Ashfield T, Jensen RV, Jeong SC, Tolin SA, Maroof MAS (2016) Candidate gene sequence analyses toward identifying Rsv3-Type resistance to soybean mosaic virus. Plant Genome 9:1–12

    Article  Google Scholar 

  • Ren Q, Pfeiffer TW, Ghabrial SA (1997) Soybean mosaic virus incidence level and infection time: interaction effects on soybean. Crop Sci 37:1706–1711

    Article  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  CAS  PubMed  Google Scholar 

  • Shakiba E, Chen P, Shi A, Li D, Dong D, Brye K (2012) Two novel alleles at the Rsv3 locus for resistance to soybean mosaic virus in PI 399091 and PI 61947 soybeans. Crop Sci 52:2587–2594

    Article  CAS  Google Scholar 

  • Shao ZQ, Zhang YM, Hang YY, Xue JY, Zhou GC, Wu P, Wu XY, Wu XZ, Wang Q, Wang B, Chen JQ (2014) Long-term evolution of nucleotide-binding site–leucine-rich repeat genes: understanding gained from and beyond the legume family. Plant Physiol 166:217–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Shao ZQ, Xue JY, Wu P, Zhang YM, Wu Y, Hang YY, Wang B, Chen JQ (2016) Large-scale analyses of angiosperm nucleotide-binding site–leucine-rich repeat (NBS–LRR) Genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol 170:2095–2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319

    CAS  PubMed  Google Scholar 

  • Song QJ, Jia GF, Zhu YL, Grant D, Nelson RT, Hwang EY, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR_1.0) in soybean. Crop Sci 50:1950–1960

    Article  CAS  Google Scholar 

  • Suh SJ, Bowman BC, Jeong N, Yang K, Kastl C, Tolin SA, Maroof MAS, Jeong S-C (2011) The Rsv3 locus conferring resistance to soybean mosaic virus is associated with a cluster of coiled-coil nucleotide-binding leucine-rich repeat genes. Plant Genome 4:55–64

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Ma Y, Liu N, Yang Z, Zheng G, Zhi H (2011) Fine mapping and identification of the soybean Rsc4 resistance candidate gene to soybean mosaic virus. Plant Breed 130:653–659

    Article  CAS  Google Scholar 

  • Whitham SA, Qi M, Innes RW, Ma W, Lopes-Caitar V, Hewezi T (2016) Molecular soybean–pathogen interactions. Annu Rev Phytopathol 54:443–468

    Article  CAS  PubMed  Google Scholar 

  • Yang QH, Gai JY (2011) Identification, inheritance and gene mapping of resistance to a virulent soybean mosaic virus strain SC15 in soybean. Plant Breed 130:128–132

    Article  CAS  Google Scholar 

  • Yang Y, Lin J, Zheng G, Zhang M, Zhi H (2014) Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Arch Virol 159:1793–1796

    Article  CAS  PubMed  Google Scholar 

  • Zheng C, Chen P, Gergerich R (2006) Genetic analysis of resistance to soybean mosaic virus in J05 soybean. Crop Sci 97:429–437

    CAS  Google Scholar 

  • Zhou GC, Shao ZQ, Ma FF, Wu P, Wu XY, Xie ZY, Yu DY, Cheng H, Liu ZH, Jiang ZF, Chen QS, Wang B, Chen JQ (2015) The evolution of soybean mosaic virus: an updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res 208:189–198

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Many thanks are given to Dr. D. X. Li of Northwest Agriculture and Forest University for providing seeds of soybean cultivars used in this study. We thank LetPub (http://www.letpub.com) for its linguistic assistance during the preparation of this manuscript. This research was financed by National Natural Science Foundation of China (31470327 and 31570217).

Author information

Author notes

  1. Fang-Fang Ma and Mian Wu are contributed equally to this work.

Authors and Affiliations

  1. Laboratory of Plant Genetics and Molecular Evolution, School of Life Sciences, Nanjing University, 163 XianLin Avenue, Nanjing, 210023, China

    Fang-Fang Ma, Mian Wu, Ying-Na Liu, Xue-Ying Feng, Xun-Zong Wu, Jian-Qun Chen & Bin Wang

Authors
  1. Fang-Fang Ma
    View author publications

    Search author on:PubMed Google Scholar

  2. Mian Wu
    View author publications

    Search author on:PubMed Google Scholar

  3. Ying-Na Liu
    View author publications

    Search author on:PubMed Google Scholar

  4. Xue-Ying Feng
    View author publications

    Search author on:PubMed Google Scholar

  5. Xun-Zong Wu
    View author publications

    Search author on:PubMed Google Scholar

  6. Jian-Qun Chen
    View author publications

    Search author on:PubMed Google Scholar

  7. Bin Wang
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to Jian-Qun Chen or Bin Wang.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Brian Diers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 55 kb)

122_2017_2999_MOESM2_ESM.fas

Supplementary material 2 (FAS 180 kb) Table S2. The aligned coding sequences of NBS_A to NBS_E genes from ten investigated soybean cultivars. (The file is in fasta format)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, FF., Wu, M., Liu, YN. et al. Molecular characterization of NBS–LRR genes in the soybean Rsv3 locus reveals several divergent alleles that likely confer resistance to the soybean mosaic virus. Theor Appl Genet 131, 253–265 (2018). https://doi.org/10.1007/s00122-017-2999-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-017-2999-9