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Biochemical Genetics

, Volume 56, Issue 4, pp 397–422 | Cite as

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

  • Surendra Neupane
  • Qin Ma
  • Febina M. Mathew
  • Adam J. Varenhorst
  • Ethan J. Andersen
  • Madhav P. NepalEmail author
Original Article

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.

Keywords

Legume disease-resistant genes Comparative genomics Synteny Gene duplication Purifying selection R gene targeting MicroRNAs 

Notes

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 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.

Compliance with Ethical Standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

10528_2018_9851_MOESM1_ESM.pdf (8.7 mb)
Supplementary material 1 (PDF 8864 kb)
10528_2018_9851_MOESM2_ESM.xlsx (133 kb)
Supplementary material 2 (XLSX 133 kb)
10528_2018_9851_MOESM3_ESM.pdf (998 kb)
Supplementary material 3 (PDF 997 kb)

References

  1. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andersen EJ, Nepal MP (2017) Genetic diversity of disease resistance genes in foxtail millet (Setaria italica L.). Plant Gene 10:8–16CrossRefGoogle Scholar
  3. 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 12:99CrossRefGoogle Scholar
  4. 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 9:641–651PubMedPubMedCentralCrossRefGoogle Scholar
  5. Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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 33:227–233CrossRefGoogle Scholar
  7. Arumuganathan K, Earle E (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218CrossRefGoogle Scholar
  8. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  9. 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 PubMedCrossRefGoogle Scholar
  10. 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 159:336–354PubMedPubMedCentralCrossRefGoogle Scholar
  11. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedCrossRefGoogle Scholar
  12. Ba ANN, Pogoutse A, Provart N, Moses AM (2009) NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:1Google Scholar
  13. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proc Int Syst Mol Biol 2:28–36Google Scholar
  14. 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 126:2081–2091PubMedCrossRefGoogle Scholar
  15. Bennett MD, Smith J (1976) Nuclear DNA amounts in angiosperms. Phil Trans Soc B 274:227–274CrossRefGoogle Scholar
  16. Benson B (2014) Disease resistance genes and their evolutionary history in six plant species. South Dakota State University, Brookings, SDGoogle Scholar
  17. 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 120:1095–1103PubMedPubMedCentralGoogle Scholar
  18. 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 10:1847–1860PubMedPubMedCentralCrossRefGoogle Scholar
  19. Caicedo AL, Purugganan MD (2005) Comparative plant genomics. Frontiers and prospects. Plant Physiol 138:545–547PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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):3389Google Scholar
  21. 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 187:941–956PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 101:15289–15294PubMedCrossRefGoogle Scholar
  23. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 24:918–931PubMedCrossRefGoogle Scholar
  25. 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 621:32–39PubMedCrossRefGoogle Scholar
  26. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dangl JL, Jones JD (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  28. DeYoung BJ, Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7:1243–1249PubMedPubMedCentralCrossRefGoogle Scholar
  29. 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 13:163–178PubMedPubMedCentralGoogle Scholar
  30. 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 24:21–32PubMedPubMedCentralCrossRefGoogle Scholar
  31. 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 34:381–411CrossRefGoogle Scholar
  32. 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 11:495–506PubMedPubMedCentralCrossRefGoogle Scholar
  33. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971PubMedCrossRefGoogle Scholar
  34. Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 83:451–465PubMedCrossRefGoogle Scholar
  36. 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–D231PubMedPubMedCentralCrossRefGoogle Scholar
  37. 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–W38PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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 PubMedCrossRefGoogle Scholar
  39. 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 8:29PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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 18:1035–1045PubMedCrossRefGoogle Scholar
  41. 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 20:265–277PubMedCrossRefGoogle Scholar
  42. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308PubMedCrossRefGoogle Scholar
  43. 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 PubMedCrossRefGoogle Scholar
  44. 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 296:92–100PubMedCrossRefGoogle Scholar
  45. 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 8:329–331PubMedCrossRefGoogle Scholar
  46. 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 157:757–769PubMedPubMedCentralCrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 74:33–37Google Scholar
  49. 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 106:786–793PubMedCrossRefGoogle Scholar
  50. Hill C, Chirumamilla A, Hartman G (2012) Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica 186:635–646CrossRefGoogle Scholar
  51. Howe EA, Sinha R, Schlauch D, Quackenbush J (2011) RNA-Seq analysis in MeV. Bioinformatics 27:3209–3210PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes. Annu Rev Phytopathol 39:285–312PubMedCrossRefGoogle Scholar
  53. 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:e0159338PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329.  https://doi.org/10.1038/nature05286 PubMedCrossRefGoogle Scholar
  55. 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 30:1236–1240PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jun T-H, Mian MR, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theor Appl Genet 124:13–22PubMedCrossRefGoogle Scholar
  57. 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 13:1CrossRefGoogle Scholar
  58. 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 12:1CrossRefGoogle Scholar
  59. 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 28:1647–1649PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 120:1063–1071PubMedCrossRefGoogle Scholar
  61. 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 121:599–610PubMedCrossRefGoogle Scholar
  62. 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 PubMedCrossRefGoogle Scholar
  63. Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73PubMedCrossRefGoogle Scholar
  64. 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 54:69–80PubMedCrossRefGoogle Scholar
  65. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874PubMedCrossRefPubMedCentralGoogle Scholar
  66. Kuwabara C, Arakawa K, Yoshida S (1999) Abscisic acid-induced secretory proteins in suspension-cultured cells of winter wheat. Plant Cell Physiol 40:184–191PubMedCrossRefGoogle Scholar
  67. 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 7:425–427PubMedCrossRefGoogle Scholar
  68. 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 23:2947–2948PubMedCrossRefGoogle Scholar
  69. Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54:575–594PubMedCrossRefGoogle Scholar
  70. 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 7:1195–1206PubMedPubMedCentralCrossRefGoogle Scholar
  71. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122PubMedCrossRefGoogle Scholar
  72. 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 PubMedCrossRefGoogle Scholar
  73. 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 PubMedCrossRefGoogle Scholar
  74. 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:e34775PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 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–D226PubMedCrossRefGoogle Scholar
  78. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  79. 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 11:184PubMedPubMedCentralCrossRefGoogle Scholar
  80. 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 32:77–92PubMedCrossRefGoogle Scholar
  81. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130PubMedCrossRefGoogle Scholar
  83. 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 CrossRefGoogle Scholar
  84. 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 282:617–631PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 151:361–369CrossRefGoogle Scholar
  86. 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 162:1459–1472PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  88. 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 11:2099–2111PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 15:866PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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 176:2317–2333PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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 155:309–322PubMedPubMedCentralGoogle Scholar
  92. 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 15:968–973PubMedCrossRefGoogle Scholar
  93. 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 14:1CrossRefGoogle Scholar
  94. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786PubMedCrossRefGoogle Scholar
  95. 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 54:441–454CrossRefGoogle Scholar
  96. 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 31:153–163PubMedCrossRefGoogle Scholar
  97. 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 101:18240–18245PubMedCrossRefGoogle Scholar
  98. Rathi D, Gayen D, Gayali S, Chakraborty S, Chakraborty N (2016) Legume proteomics: progress, prospects, and challenges. Proteomics 16:310–327PubMedCrossRefGoogle Scholar
  99. 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 192:164–178PubMedCrossRefGoogle Scholar
  100. Reams AB, Neidle EL (2004) Selection for gene clustering by tandem duplication. Annu Rev Microbiol 58:119–142PubMedCrossRefGoogle Scholar
  101. Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Bioinformatics for DNA sequence analysis. Mehods Mol Biol 537:337–350Google Scholar
  102. 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 25:637–642Google Scholar
  103. 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 CrossRefPubMedGoogle Scholar
  104. Schatz MC, Witkowski J, McCombie WR (2012) Current challenges in de novo plant genome sequencing and assembly. Genome Biol 13:243PubMedPubMedCentralCrossRefGoogle Scholar
  105. 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 47:868–876PubMedCrossRefGoogle Scholar
  106. 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 463:178–183PubMedCrossRefGoogle Scholar
  107. 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 46:707–713PubMedCrossRefGoogle Scholar
  108. Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–125PubMedCrossRefGoogle Scholar
  109. 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 10:160PubMedPubMedCentralCrossRefGoogle Scholar
  110. 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 166:217–234PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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 170:15Google Scholar
  112. 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 24:859–874PubMedPubMedCentralCrossRefGoogle Scholar
  113. Soderlund C, Bomhoff M, Nelson WM (2011) SyMAP v3. 4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39:e68–e76Google Scholar
  114. 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 38:361–374CrossRefGoogle Scholar
  115. Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25PubMedCrossRefGoogle Scholar
  116. Stokes TL, Kunkel BN, Richards EJ (2002) Epigenetic variation in Arabidopsis disease resistance. Genes Dev 16:171–182PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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 25:379–392PubMedCrossRefGoogle Scholar
  118. Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643PubMedCrossRefGoogle Scholar
  119. Tian D, Traw M, Chen J, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77PubMedCrossRefGoogle Scholar
  120. 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 58:40–53PubMedCrossRefGoogle Scholar
  121. 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 29:439–451PubMedCrossRefGoogle Scholar
  122. 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 14:1CrossRefGoogle Scholar
  123. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 78:1101–1115PubMedCrossRefGoogle Scholar
  125. Whitkus R, Doebley J, Lee M (1992) Comparative genome mapping of Sorghum and maize. Genetics 132:1119–1130PubMedPubMedCentralGoogle Scholar
  126. 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 280:187–198PubMedCrossRefGoogle Scholar
  127. 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 107:18735–18740PubMedCrossRefGoogle Scholar
  128. 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 13:1CrossRefGoogle Scholar
  129. 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 CrossRefGoogle Scholar
  130. 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 193:1049–1063PubMedCrossRefGoogle Scholar
  131. 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 25:2540–2553PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zhang G, Gu C, Wang D (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theor Appl Genet 118:473–482PubMedCrossRefGoogle Scholar
  133. Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theor Appl Genet 120:1183–1191PubMedCrossRefGoogle Scholar
  134. 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 33:2692–2705PubMedPubMedCentralCrossRefGoogle Scholar
  135. 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 58:165–177PubMedCrossRefGoogle Scholar
  136. 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 17:1PubMedPubMedCentralCrossRefGoogle Scholar
  137. Zhu H, Choi H-K, Cook DR, Shoemaker RC (2005) Bridging model and crop legumes through comparative genomics. Plant Physiol 137:1189–1196PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Biology and MicrobiologySouth Dakota State UniversityBrookingsUSA
  2. 2.Department of Agronomy, Horticulture and Plant ScienceSouth Dakota State UniversityBrookingsUSA

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