Skip to main content
SpringerLink
Log in

Evolutionary Divergence of TNL Disease-Resistant Proteins in Soybean (Glycine max) and Common Bean (Phaseolus vulgaris)

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Disease-resistant genes (R genes) encode proteins that are involved in protecting plants from their pathogens and pests. Availability of complete genome sequences from soybean and common bean allowed us to perform a genome-wide identification and analysis of the Toll interleukin-1 receptor-like nucleotide-binding site leucine-rich repeat (TNL) proteins. Hidden Markov model (HMM) profiling of all protein sequences resulted in the identification of 117 and 77 regular TNL genes in soybean and common bean, respectively. We also identified TNL gene homologs with unique domains, and signal peptides as well as nuclear localization signals. The TNL genes in soybean formed 28 clusters located on 10 of the 20 chromosomes, with the majority found on chromosome 3, 6 and 16. Similarly, the TNL genes in common bean formed 14 clusters located on five of the 11 chromosomes, with the majority found on chromosome 10. Phylogenetic analyses of the TNL genes from Arabidopsis, soybean and common bean revealed less divergence within legumes relative to the divergence between legumes and Arabidopsis. Syntenic blocks were found between chromosomes Pv10 and Gm03, Pv07 and Gm10, as well as Pv01 and Gm14. The gene expression data revealed basal level expression and tissue specificity, while analysis of available microRNA data showed 37 predicted microRNA families involved in targeting the identified TNL genes in soybean and common bean.

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

Similar content being viewed by others

References

  • Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol. https://doi.org/10.1104/pp.107.104588

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersen EJ, Nepal MP (2017) Genetic diversity of disease resistance genes in foxtail millet (Setaria italica L.). Plant Gene 10:8–16

    Article  CAS  Google Scholar 

  • Andersen EJ, Ali S, Reese RN, Yen Y, Neupane S, Nepal MP (2016) Diversity and evolution of disease resistance genes in Barley (Hordeum vulgare L.). Evol Bioinfor Online 12:99

    Article  CAS  Google Scholar 

  • Anderson PA, Lawrence GJ, Morrish BC, Ayliffe MA, Finnegan EJ, Ellis JG (1997) Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell 9:641–651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987

    Article  PubMed  PubMed Central  Google Scholar 

  • Andolfo G, Sanseverino W, Aversano R, Frusciante L, Ercolano M (2014) Genome-wide identification and analysis of candidate genes for disease resistance in tomato. Mol Breed 33:227–233

    Article  CAS  Google Scholar 

  • Arumuganathan K, Earle E (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218

    Article  CAS  Google Scholar 

  • Arya P, Kumar G, Acharya V, Singh AK (2014) Genome-wide identification and expression analysis of NBS-encoding genes in Malus x domestica and expansion of NBS genes family in Rosaceae. PLoS ONE 9:e107987. https://doi.org/10.1371/journal.pone.0107987

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983. https://doi.org/10.1038/415977a

    Article  PubMed  CAS  Google Scholar 

  • Ashfield T, Egan AN, Pfeil BE, Chen NW, Podicheti R, Ratnaparkhe MB, Ameline-Torregrosa C, Denny R, Cannon S, Doyle JJ (2012) Evolution of a complex disease resistance gene cluster in diploid Phaseolus and tetraploid Glycine. Plant Physiol 159:336–354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159

    Article  PubMed  CAS  Google Scholar 

  • Ba ANN, Pogoutse A, Provart N, Moses AM (2009) NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:1

    Google Scholar 

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proc Int Syst Mol Biol 2:28–36

  • Bales C, Zhang G, Liu M, Mensah C, Gu C, Song Q, Hyten D, Cregan P, Wang D (2013) Mapping soybean aphid resistance genes in PI 567598B. Theor Appl Genet 126:2081–2091

    Article  PubMed  CAS  Google Scholar 

  • Bennett MD, Smith J (1976) Nuclear DNA amounts in angiosperms. Phil Trans Soc B 274:227–274

    Article  CAS  Google Scholar 

  • Benson B (2014) Disease resistance genes and their evolutionary history in six plant species. South Dakota State University, Brookings, SD

    Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103

    PubMed  PubMed Central  CAS  Google Scholar 

  • Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, Daniels MJ, Holub EB, Jones JD (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10:1847–1860

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caicedo AL, Purugganan MD (2005) Comparative plant genomics. Frontiers and prospects. Plant Physiol 138:545–547

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN (2014) A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front Plant Sci 5(10):3389

    Google Scholar 

  • Chen NW, Sévignac M, Thareau V, Magdelenat G, David P, Ashfield T, Innes RW, Geffroy V (2010) Specific resistances against Pseudomonas syringae effectors AvrB and AvrRpm1 have evolved differently in common bean (Phaseolus vulgaris), soybean (Glycine max), and Arabidopsis thaliana. New Phytol 187:941–956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi H-K, Mun J-H, Kim D-J, Zhu H, Baek J-M, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Christie N, Tobias PA, Naidoo S, Külheim C (2016) The Eucalyptus grandis NBS-LRR gene family: physical clustering and expression hotspots. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01238

    Article  PubMed  PubMed Central  Google Scholar 

  • Collier SM, Hamel L-P, Moffett P (2011) Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant Microbe Interact 24:918–931

    Article  PubMed  CAS  Google Scholar 

  • Cui X, Yan Q, Gan S, Xue D, Dou D, Guo N, Xing H (2017) Overexpression of gma-miR1510a/b suppresses the expression of a NB-LRR domain gene and reduces resistance to Phytophthora sojae. Gene 621:32–39

    Article  PubMed  CAS  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dangl JL, Jones JD (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dodds PN, Lawrence GJ, Ellis JG (2001) Six amino acid changes confined to the leucine-rich repeat β-strand/β-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 13:163–178

    PubMed  PubMed Central  CAS  Google Scholar 

  • Du J, Tian Z, Sui Y, Zhao M, Song Q, Cannon SB, Cregan P, Ma J (2012) Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. Plant Cell 24:21–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duc G, Agrama H, Bao S, Berger J, Bourion V, De Ron AM, Gowda CL, Mikic A, Millot D, Singh KB (2015) Breeding annual grain legumes for sustainable agriculture: new methods to approach complex traits and target new cultivar ideotypes. Crit Rev Plant Sci 34:381–411

    Article  Google Scholar 

  • Ellis JG, Lawrence GJ, Luck JE, Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant cell 11:495–506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971

    Article  PubMed  CAS  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fei Q, Li P, Teng C, Meyers BC (2015) Secondary siRNAs from Medicago NB-LRRs modulated via miRNA–target interactions and their abundances. Plant J 83:451–465

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J (2013) Pfam: the protein families database. Nucleic Acids Res 42:D222–D231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR (2015) HMMER web server: 2015 update. Nucleic Acids Res 43:W30–W38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Friedman AR, Baker BJ (2007) The evolution of resistance genes in multi-protein plant resistance systems. Curr Opin Genet Dev. https://doi.org/10.1016/j.gde.2007.08.014

    Article  PubMed  Google Scholar 

  • Gao H, Bhattacharyya MK (2008) The soybean-Phytophthora resistance locus Rps1-k encompasses coiled coil-nucleotide binding-leucine rich repeat-like genes and repetitive sequences. BMC Plant Biol 8:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gao H, Narayanan NN, Ellison L, Bhattacharyya MK (2005) Two classes of highly similar coiled coil-nucleotide binding-leucine rich repeat genes isolated from the Rps1-k locus encode Phytophthora resistance in soybean. Mol Plant Microbe Interact 18:1035–1045

    Article  PubMed  CAS  Google Scholar 

  • Gassmann W, Hinsch ME, Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20:265–277

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308

    Article  PubMed  CAS  Google Scholar 

  • Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11:169–177. https://doi.org/10.1111/j.1364-3703.2009.00589.x

    Article  PubMed  CAS  Google Scholar 

  • Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • González VM, Müller S, Baulcombe D, Puigdomènech P (2015) Evolution of NBS-LRR gene copies among dicot plants and its regulation by members of the miR482/2118 superfamily of miRNAs. Mol Plant 8:329–331

    Article  PubMed  CAS  Google Scholar 

  • Guo Y-L, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157:757–769

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65. https://doi.org/10.1016/j.pmpp.2012.01.002

    Article  CAS  Google Scholar 

  • Hartman G, Domier L, Wax L, Helm C, Onstad D, Shaw J, Solter L, Voegtlin D, d’Arcy C, Gray M (2001) Occurrence and distribution of Aphis glycines on soybeans in Illinois in 2000 and its potential control. Plant Health Progr 74:33–37

  • He C-Y, Tian A-G, Zhang J-S, Zhang Z-Y, Gai J-Y, Chen S-Y (2003) Isolation and characterization of a full-length resistance gene homolog from soybean. Theor Appl Genet 106:786–793

    Article  PubMed  CAS  Google Scholar 

  • Hill C, Chirumamilla A, Hartman G (2012) Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica 186:635–646

    Article  CAS  Google Scholar 

  • Howe EA, Sinha R, Schlauch D, Quackenbush J (2011) RNA-Seq analysis in MeV. Bioinformatics 27:3209–3210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes. Annu Rev Phytopathol 39:285–312

    Article  PubMed  CAS  Google Scholar 

  • Jain S, Chittem K, Brueggeman R, Osorno JM, Richards J, Nelson BD Jr (2016) Comparative transcriptome analysis of resistant and susceptible common bean genotypes in response to soybean cyst nematode infection. PLoS ONE 11:e0159338

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286

    Article  PubMed  CAS  Google Scholar 

  • Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jun T-H, Mian MR, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22

    Article  PubMed  CAS  Google Scholar 

  • Jupe F, Pritchard L, Etherington GJ, MacKenzie K, Cock PJ, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JD (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics 13:1

    Article  CAS  Google Scholar 

  • Kang YJ, Kim KH, Shim S, Yoon MY, Sun S, Kim MY, Van K, Lee S-H (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:1

    Article  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim K-S, Bellendir S, Hudson KA, Hill CB, Hartman GL, Hyten DL, Hudson ME, Diers BW (2010a) Fine mapping the soybean aphid resistance gene Rag1 in soybean. Theor Appl Genet 120:1063–1071

    Article  PubMed  CAS  Google Scholar 

  • Kim K-S, Hill CB, Hartman GL, Hyten DL, Hudson ME, Diers BW (2010b) Fine mapping of the soybean aphid-resistance gene Rag2 in soybean PI 200538. Theor Appl Genet 121:599–610

    Article  PubMed  CAS  Google Scholar 

  • Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol. https://doi.org/10.1007/s11103-008-9293-9

    Article  PubMed  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kuwabara C, Arakawa K, Yoshida S (1999) Abscisic acid-induced secretory proteins in suspension-cultured cells of winter wheat. Plant Cell Physiol 40:184–191

    Article  PubMed  CAS  Google Scholar 

  • Lahaye T (2002) The Arabidopsis RRS1-R disease resistance gene–uncovering the plant’s nucleus as the new battlefield of plant defense? Trends Plant Sci 7:425–427

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54:575–594

    Article  PubMed  Google Scholar 

  • Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7:1195–1206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen JQ, Tian D, Yang S (2010) Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Genet Genomics 283:427–438. https://doi.org/10.1007/s00438-010-0527-6

    Article  PubMed  CAS  Google Scholar 

  • Li X, Kapos P, Zhang Y (2015) NLRs in plants. Curr Opin Immunol 32:114–121. https://doi.org/10.1016/j.coi.2015.01.014

    Article  PubMed  CAS  Google Scholar 

  • Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS ONE 7:e34775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lozano R, Hamblin MT, Prochnik S, Jannink JL (2015) Identification and distribution of the NBS-LRR gene family in the Cassava genome. BMC Genomics 16:360. https://doi.org/10.1186/s12864-015-1554-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo S, Zhang Y, Hu Q, Chen J, Li K, Lu C, Liu H, Wang W, Kuang H (2012) Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 159:197–210. https://doi.org/10.1104/pp.111.192062

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marchler-bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226

    Article  PubMed  CAS  Google Scholar 

  • Marone D, Russo MA, Laido G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326. https://doi.org/10.3390/ijms14047302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genomics 11:184

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92

    Article  PubMed  CAS  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. https://doi.org/10.1105/tpc.009308

    Article  PubMed  PubMed Central  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  PubMed  CAS  Google Scholar 

  • Milos V, Vuk D, Kristina P, Jegor M (2013) Review of soybean resistance to pathogens. Ratarstvo i povrtarstvo 50:52–61. https://doi.org/10.5937/ratpov50-4038

    Article  Google Scholar 

  • Mun J-H, Yu H-J, Park S, Park B-S (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Mol Genet Genomics 282:617–631

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Namayanja A, Buruchara R, Mahuku G, Rubaihayo P, Kimani P, Mayanja S, Eyedu H (2006) Inheritance of resistance to angular leaf spot in common bean and validation of the utility of resistance linked markers for marker assisted selection out side the mapping population. Euphytica 151:361–369

    Article  CAS  Google Scholar 

  • Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC (2013) The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol 162:1459–1472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nepal MP, Benson BV (2015) CNL disease resistance genes in soybean and their evolutionary divergence. Evol Bioinform Online 11:49–63. https://doi.org/10.4137/EBO.S21782

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Noël L, Moores TL, Van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JD (1999) Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11:2099–2111

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genomics 15:866

    Article  PubMed  PubMed Central  Google Scholar 

  • Orgil U, Araki H, Tangchaiburana S, Berkey R, Xiao S (2007) Intraspecific genetic variations, fitness cost and benefit of RPW8, a disease resistance locus in Arabidopsis thaliana. Genetics 176:2317–2333

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pan Q, Liu Y-S, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    PubMed  PubMed Central  CAS  Google Scholar 

  • Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15:968–973

    Article  PubMed  CAS  Google Scholar 

  • Peele HM, Guan N, Fogelqvist J, Dixelius C (2014) Loss and retention of resistance genes in five species of the Brassicaceae family. BMC Plant Biol 14:1

    Article  CAS  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  PubMed  CAS  Google Scholar 

  • Pfeil B, Schlueter JA, Shoemaker R, Doyle J (2005) Placing paleopolyploidy in relation to taxon divergence: a phylogenetic analysis in legumes using 39 gene families. Sys Biol 54:441–454

    Article  CAS  Google Scholar 

  • Plocik A, Layden J, Kesseli R (2004) Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 31:153–163

    Article  PubMed  CAS  Google Scholar 

  • Pontes O, Neves N, Silva M, Lewis MS, Madlung A, Comai L, Viegas W, Pikaard CS (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci USA 101:18240–18245

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rathi D, Gayen D, Gayali S, Chakraborty S, Chakraborty N (2016) Legume proteomics: progress, prospects, and challenges. Proteomics 16:310–327

    Article  PubMed  CAS  Google Scholar 

  • Ratnaparkhe MB, Wang X, Li J, Compton RO, Rainville LK, Lemke C, Kim C, Tang H, Paterson AH (2011) Comparative analysis of peanut NBS-LRR gene clusters suggests evolutionary innovation among duplicated domains and erosion of gene microsynteny. New Phytol 192:164–178

    Article  PubMed  Google Scholar 

  • Reams AB, Neidle EL (2004) Selection for gene clustering by tandem duplication. Annu Rev Microbiol 58:119–142

    Article  PubMed  CAS  Google Scholar 

  • Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Bioinformatics for DNA sequence analysis. Mehods Mol Biol 537:337–350

  • Sartorato A, Nietsche S, Barros EG, Moreira MA (2000) RAPD and SCAR markers linked to resistance gene to angular leaf spot in common beans. Fitopatol Bras 25:637–642

    CAS  Google Scholar 

  • Savard L, Li P, Strauss SH, Chase MW, Michaud M, Bousquet J (1994) Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.91.11.5163

    Article  PubMed  PubMed Central  Google Scholar 

  • Schatz MC, Witkowski J, McCombie WR (2012) Current challenges in de novo plant genome sequencing and assembly. Genome Biol 13:243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC (2004) Mining EST databases to resolve evolutionary events in major crop species. Genome 47:868–876

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–125

    Article  PubMed  CAS  Google Scholar 

  • Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shao Z-Q, Zhang Y-M, Hang Y-Y, Xue J-Y, Zhou G-C, Wu P, Wu X-Y, Wu X-Z, Wang Q, Wang B (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  CAS  Google Scholar 

  • Shao Z-Q, Xue J-Y, Wu P, Zhang Y-M, Wu Y, Hang Y-Y, Wang B, Chen J-Q (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 170:15

  • Shivaprasad PV, Chen H-M, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site–leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soderlund C, Bomhoff M, Nelson WM (2011) SyMAP v3. 4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39:e68–e76

  • Souza TLP, Faleiro FG, Dessaune SN, Paula-Junior TJd, Moreira MA, Barros EGd (2013) Breeding for common bean (Phaseolus vulgaris L.) rust resistance in Brazil. Trop Plant Pathol 38:361–374

    Article  Google Scholar 

  • Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25

    Article  PubMed  CAS  Google Scholar 

  • Stokes TL, Kunkel BN, Richards EJ (2002) Epigenetic variation in Arabidopsis disease resistance. Genes Dev 16:171–182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M, Hardham AR, Ellis JG, Dodds PN, Jones DA (2012) N-terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Mol Plant-Microbe Interact 25:379–392

    Article  PubMed  CAS  Google Scholar 

  • Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643

    Article  PubMed  CAS  Google Scholar 

  • Tian D, Traw M, Chen J, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    Article  PubMed  CAS  Google Scholar 

  • Tian Y, Fan L, Thurau T, Jung C, Cai D (2004) The absence of TIR-type resistance gene analogues in the sugar beet (Beta vulgaris L.) genome. J Mol Evol 58:40–53

    Article  PubMed  CAS  Google Scholar 

  • Van Der Biezen EA, Freddie CT, Kahn K, Jones JD (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J 29:439–451

    Article  PubMed  Google Scholar 

  • Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J (2013) Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics 14:1

    Article  CAS  Google Scholar 

  • Wei H, Li W, Sun X, Zhu S, Zhu J (2013) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in a diploid cotton Gossypium raimondii. PLoS ONE 8:e68435. https://doi.org/10.1371/journal.pone.0068435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whitham S, Dinesh-Kumar S, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115

    Article  PubMed  CAS  Google Scholar 

  • Whitkus R, Doebley J, Lee M (1992) Comparative genome mapping of Sorghum and maize. Genetics 132:1119–1130

    PubMed  PubMed Central  CAS  Google Scholar 

  • Yang S, Zhang X, Yue J-X, Tian D, Chen J-Q (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198

    Article  PubMed  CAS  Google Scholar 

  • Yang S, Tang F, Gao M, Krishnan HB, Zhu H (2010) R gene-controlled host specificity in the legume–rhizobia symbiosis. Proc Natl Acad Sci USA 107:18735–18740

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang L, Li D, Li Y, Gu X, Huang S, Garcia-Mas J, Weng Y (2013) A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci. BMC Plant Biol 13:1

    Article  Google Scholar 

  • Yu J, Tehrim S, Zhang F, Tong C, Huang J, Cheng X, Dong C, Zhou Y, Qin R, Hua W, Liu S (2014) Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genomics 15:1–18. https://doi.org/10.1186/1471-2164-15-3

    Article  CAS  Google Scholar 

  • Yue JX, Meyers BC, Chen JQ, Tian D, Yang S (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063

    Article  PubMed  CAS  Google Scholar 

  • Zhai J, Jeong D-H, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang G, Gu C, Wang D (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor Appl Genet 118:473–482

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theor Appl Genet 120:1183–1191

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Xia R, Kuang H, Meyers BC (2016a) The diversification of plant NBS-LRR defense genes directs the evolution of microRNAs that target them. Mol Biol Evol 33:2692–2705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang YM, Shao ZQ, Wang Q, Hang YY, Xue JY, Wang B, Chen JQ (2016b) Uncovering the dynamic evolution of nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes in Brassicaceae. J Integr Plant Biol 58:165–177

    Article  PubMed  CAS  Google Scholar 

  • Zheng F, Wu H, Zhang R, Li S, He W, Wong F-L, Li G, Zhao S, Lam H-M (2016) Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics 17:1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu H, Choi H-K, Cook DR, Shoemaker RC (2005) Bridging model and crop legumes through comparative genomics. Plant Physiol 137:1189–1196

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by South Dakota Agricultural Experiment Station (SDAES) USDA-NIFA hatch Project to M. Nepal (SD00H469-13) and South Dakota Soybean Research and Promotion Council (SDSRPC-SA1800238).

Author information

Authors and Affiliations

  1. Department of Biology and Microbiology, South Dakota State University, Brookings, SD, USA

    Surendra Neupane, Ethan J. Andersen & Madhav P. Nepal

  2. Department of Agronomy, Horticulture and Plant Science, South Dakota State University, Brookings, SD, USA

    Qin Ma, Febina M. Mathew & Adam J. Varenhorst

Authors
  1. Surendra Neupane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Febina M. Mathew
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adam J. Varenhorst
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ethan J. Andersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Madhav P. Nepal
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SN conducted gene identification and analysis. MPN conceived and supervised the project as well as helped SN draft the manuscript. QM, FM, EJA and AV contributed to data analysis, interpretation and revision of the manuscript.

Corresponding author

Correspondence to Madhav P. Nepal.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Neupane, S., Ma, Q., Mathew, F.M. et al. Evolutionary Divergence of TNL Disease-Resistant Proteins in Soybean (Glycine max) and Common Bean (Phaseolus vulgaris). Biochem Genet 56, 397–422 (2018). https://doi.org/10.1007/s10528-018-9851-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-018-9851-z

Keywords

Search

Navigation