Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants

Physiology and Molecular Biology of Plants

Volumn 19, Issue 1, 2013, Pages 1-9

  Joshi, Raj Kumar ^a   Nayak, Sanghamitra ^a  

^a SIKSHA O ANUSANDHAN DEEMED TO BE UNIVERSITY   (India)

Author keywords

Diversification; Duplication; Evolution; NBS LRRs; R genes

Indexed keywords

EID: 84872126333     PISSN: 09715894     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12298-012-0138-2     Document Type: Review

References (58)

1. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12: 1871-1884. doi: 10. 1101/gr. 454902.
2. Bauer E, Weyen J, Schiemann A, Graner A, Ordon F (1997) Molecular mapping of novel resistance genes against barley mild mosaic virus (BaMMV). Theor Appl Genet 95: 1263-1269. doi: 10. 1007/s001220050691.
3. Baumgarten A, Cannon S, Spangler R, May G (2003) Genome level evolution of resistance genes in Arabidopsis thaliana. Genetics 165: 309-319.
4. Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292: 2281-2285. doi: 10. 1126/science. 1061337.
5. Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I (2007) Transgenerational changes in the genome stability and methylation in pathogen-infected plants. Nucleic Acids Res 35: 1714-1725. doi: 10. 1093/nar/gkm029.
6. Budak H, Su S, Ergen N (2006) Revealing constitutively expressed resistance genes Agrostis species using PCR based motif directed RNA fingerprinting. Genet Res 88: 165-175. doi: 10. 1017/S0016672307008518.
7. Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND (2002) Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 54: 548-562. doi: 10. 1007/s0023901-0057-2.
8. Dawkins R, Krebs J (1979) Arm races between and within species. Proceedings of the royal society of London 205: 480-511.
9. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10: 1915-1925. doi: 10. 1105/tpc. 10. 11. 1915.
10. Dodds PN, Lawrence G, Catanzariti AM, Teh T, Wang CIA, Ayliffe MBK, Ellis J (2006) Direct protein interaction underlies gene-for-gene specificity and co-evolution of the flax L5/L6/L7 resistance genes and flax rust AvrL567 avirulence genes. Proc Natl Acad Sci USA 103: 8888-8893. doi: 10. 1073/pnas. 0602577103.
11. Dodds PN, Lawrence GJ, Ellis JG (2001) Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. Plant J 27: 439-453. doi: 10. 1046/j. 1365-313X. 2001. 01114. x.
12. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209. doi: 10. 1146/annurev. phyto. 42. 040803. 140421.
13. Durant WE, Wang S, Dong X (2007) Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response. Proc Natl Acad Sci USA 104: 4223-4227. doi: 10. 1073/pnas. 0609357104.
14. 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. doi: 10. 1105/tpc. 11. 3. 495.
15. Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3: 278-284. doi: 10. 1016/S1369-5266(00)00080-7.
16. Grant M (1998) Independent deletion of a pathogen resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci USA 95: 15843-15848. doi: 10. 1073/pnas. 95. 26. 15843.
17. Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168: 2197-2206. doi: 10. 1534/genetics. 104. 032193.
18. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444: 323-329. doi: 10. 1038/nature05286.
19. Joshi RK, Nayak S (2011) Functional characterization and signal transduction ability of nucleotide-binding site leucine rich repeats resistance genes in plants. Genet Mol Res 10(4): 2637-2652. doi: 10. 4238/2011. October. 25. 10.
20. Jiang SM, Hu J, Yin WB, Chen YH, Wang RRC, Hu ZM (2005) Cloning of resistance gene analogs located on the alien chromosome in an addition line of wheat-Thinopyrum intermedium. Theor Appl Genet 111: 923-931. doi: 10. 1007/s00122-005-0022-3.
21. Jupe F, Pritchard L, Etherington GJ, Mackenzie K, Cock PJA, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JDG, Ingo H (2012) Identification and localization of the NB-LRR gene family within the potato genome. BMC Genomics 13: 75. doi: 10. 1186/1471-2164-13-75.
22. Kim MG, da Cunha L, McFall AJ, Belkhadir Y, Debroy S, Dangl JL, Mackey D (2005) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121: 749-759. doi: 10. 1016/j. cell. 2005. 03. 025.
23. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelan D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66: 619-636. doi: 10. 1007/s11103-008-9293-9.
24. Korves TM, Bergelson J (2003) A developmental response to pathogen infection in Arabidopsis. Plant Physiol 133: 339-347. doi: 10. 1104/pp/103. 027094.
25. Kreitman M, Akashi H (1995) Molecular evidence for natural selection. Annu Rev Ecol Syst 26: 403-422. doi: http://www. jstor. org/stable/2097213.
26. 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. doi: 10. 1105/tpc. 104. 025502.
27. Li X, Cheng Y, Ma W, Zhao Y, Jiang H, Zhang M (2010) Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst Evol 289: 101-110. doi: 10. 1007/s00606-010-0331-0.
28. 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 Genom 34(9): 765-776. doi: 10. 1016/S1673-8527(07)60087-3.
29. 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(4): e34775. doi: 10. 1371/journal. pone. 0034775.
30. Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, Hohn B (2002) Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet 30: 311-314. doi: 10. 1038/ng846.
31. Luo S, Peng J, Li K, Wang M, Kuang H (2011) Contrasting evolutionary patterns of the Rp1 resistance gene family in different species of Poaceae. Mol Biol Evol 28(1): 313-325. doi: 10. 1093/molbev/msq216.
32. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54: 23-61. doi: 10. 1146/annurev. arplant. 54. 031902. 135035.
33. McDowell JM, Simon SA (2006) Recent insights into R gene evolution. Mol Plant Pathol 7: 437-448. doi: 10. 1111/j. 1364-3703. 2006. 00342. x.
34. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834. doi: 10. 1105/tpc. 009308.
35. 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. doi: 10. 1046/j. 1365-313X. 2002. 01404. x.
36. 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. doi: 10. 1101/gr. 8. 11. 1113.
37. Molinier J, Ries G, Zipfel C, Hohn B (2006) Tran generation memory of stress in plants. Nature 442: 1046-1049. doi: 10. 1038/nature05022.
38. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152. doi: 10. 1146/annurev. genet. 39. 073003. 112240.
39. Noel L, Moores TL, van Der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JDG (1999) Pronounced intraspecific haplotypes divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 11: 2099-2112. doi: 10. 1105/tpc. 11. 11. 2099.
40. Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50: 203-213. doi: 10. 1007/s002399910023.
41. Parker JE, Coleman MJ, Szabo V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JDG (1997) The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9: 879-894. doi: 10. 1105/tpc. 9. 6. 879.
42. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91: 821-832. doi: 10. 1016/S0092-8674(00)80470-5.
43. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465: 1033-1038. doi: 10. 1038/nature09144.
44. Ribas AF, Cenci A, Combes MC, Etienne H, Lashermes P (2011) Organization and molecular evolution of a disease resistance gene cluster in coffee trees. BMC Genomics 12: 240. doi: 10. 1186/1471-2164-12-240.
45. Rose LE, Bittner-Eddy PD, Langley CH, Holub EB, Michelmore RW, Beynon JL (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166: 1517-1527. doi: 10. 1534/genetics. 166. 3. 1517.
46. Sinapidou E, Williams K, Nott L, Bahkt S, Tor M, Crute I, Bittner-Eddy P, Beynon J (2004) Two TIR-NB-LRR genes are required to specify resistance to Perenospora parasitica isolate cala2 in Arabidopsis. Plant J 38: 898-909. doi: 10. 1111/j. 1365-313X. 2004. 02099. x.
47. Smith SM, Pryor AJ, Hulbert SH (2004) Allelic and haplotypic diversity at the rp1 rust resistance locus of maize. Genetics 167: 1939-1947. doi: 10. 1534/genetics. 104. 029371.
48. Stahl EA, Bishop JG (2000) Plant-pathogen arms races at the molecular level. Curr Opin Plant Biol 3: 299-304. doi: 10. 1016/S1369-5266(00)00083-2.
49. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671. doi: 10. 1038/23260.
50. Tarr DEK, Alexander HM (2009) TIR-NBS genes are rare in monocots: evidence from diverse monocot orders. BMC Res Notes 2: 197. doi: 10. 1186/1756-0500-2-197.
51. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999) Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 96: 14153-14158. doi: 10. 1073/pnas. 96. 24. 14153.
52. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JDG (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9: 2209-2224. doi: 10. 1105/tpc. 9. 12. 2209.
53. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77. doi: 10. 1038/nature01588.
54. Wang GL, Ruan DL, Song WY, Sideris S, Chen LL, Pi LY, Zhang S, Zhang Z, Fauquet C, Gaut B, Ronald P (1998) Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race specific recognition and is subject to adaptive evolution. Plant Cell 10: 765-779. doi: 10. 1105/tpc. 10. 5. 765.
55. 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(4): 1049-1063. doi: 10. 1111/j. 1469-8137. 2011. 04006. x.
56. Zhang M, Wu YH, Lee MK, Liu YH, Rong Y, Santos TS, Wu C, Xie F, Nelson RL, Zhang HB (2010) Number of genes in NBS and RLK families vary by more than four fold within a plant species and are regulated by multiple factors. Nucleic Acids Res 30: 1-13. doi: 10. 1093/nar/gkq524.
57. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genom 271: 402-415. doi: 10. 1007/s00438-004-0990-z.
58. Zhu HY, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and non-TIR NBSLRR resistance gene family in Medicago truncatula. Mol Plant Microbe Interact 15: 529-539. doi: 10. 1094/MPMI. 2002. 15. 6. 529.