Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Lin, Xiao ^a   Zhang, Yu ^a   Kuang, Hanhui ^a   Chen, Jiongjiong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Copy number; Cucurbitaceae; Evolution; R genes; Sequence exchange

Indexed keywords

ARTICLE; CHIMERA; COMPARATIVE STUDY; CUCURBITACEAE; DATA MINING; DISEASE RESISTANCE; GENE CONVERSION; GENE DOSAGE; GENE DUPLICATION; GENE FREQUENCY; GENE LOCUS; GENE LOSS; GENE NUMBER; GENE SEQUENCE; MOLECULAR CLONING; MULTIGENE FAMILY; NATURAL POPULATION; NONHUMAN; PHYLOGENY; PLANT DISEASE; PLANT GENE; PLANT GENOME; POLYMERASE CHAIN REACTION; POPULUS; PSEUDOGENE; R GENE; SOYBEAN; TRICHOSANTHES; TRICHOSANTHES KIRILOWII;

BASE SEQUENCE; CHROMOSOME MAPPING; CUCURBITACEAE; DISEASE RESISTANCE; DNA PRIMERS; EVOLUTION, MOLECULAR; EXONS; GENE DOSAGE; GENE DUPLICATION; GENETIC LOCI; GENETIC VARIATION; GENOTYPE; INTRONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PSEUDOGENES; SPECIES SPECIFICITY;

CITRULLUS LANATUS VAR. LANATUS; CUCUMIS; CUCUMIS SATIVUS; CUCURBITACEAE; GLYCINE MAX; TRICHOSANTHES KIRILOWII;

EID: 84877840224     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-335     Document Type: Article

References (55)

1. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 1999, 20(3):317-332. 10.1046/j.1365-313X.1999.t01-1-00606.x, 10571892.
2. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15(4):809-834. 10.1105/tpc.009308, 152331, 12671079.
3. Luo S, Zhang Y, Hu Q, Chen J, Li K, Lu C, Liu H, Wang W, Kuang H. Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 2012, 159(1):197-210. 10.1104/pp.111.192062, 3375961, 22422941.
4. Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BB, Jones JD. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 1997, 91(6):821-832. 10.1016/S0092-8674(00)80470-5, 9413991.
5. McDowell JM, Dhandaydham M, Long TA, Aarts MGM, Goff S, Holub EB, Dangl JL. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 1998, 10(11):1861-1874. 143965, 9811794.
6. Caicedo AL, Schaal BA, Kunkel BN. Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc Natl Acad Sci USA 1999, 96(1):302-306. 10.1073/pnas.96.1.302, 15134, 9874813.
7. Ellis JG, Lawrence GJ, Luck JE, Dodds PN. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 1999, 11(3):495-506. 144189, 10072407.
8. Noël L, Moores TL, van der Biezen EA, Parniske M, Daniels MJ, Parker JE, Jones JDG. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 1999, 11(11):2099-2112. 144120, 10559437.
9. Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 2000, 12(5):663-676. 139919, 10810142.
10. Dodds PN, Lawrence GJ, Ellis JG. Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. Plant J 2001, 27(5):439-453. 10.1046/j.1365-313X.2001.01114.x, 11576428.
11. Van der Hoorn RAL, Kruijt M, Roth R, Brandwagt BF, Joosten MHAJ, De Wit PJGM. Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium. Proc Natl Acad Sci USA 2001, 98(18):10493. 10.1073/pnas.181241798, 56988, 11517316.
12. Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW. Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 2004, 16(11):2870-2894. 10.1105/tpc.104.025502, 527186, 15494555.
13. Kuang H, Wei F, Marano MR, Wirtz U, Wang X, Liu J, Shum WP, Zaborsky J, Tallon LJ, Rensink W. The R1 resistance gene cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant J 2005, 44(1):37-51. 10.1111/j.1365-313X.2005.02506.x, 16167894.
14. Kuang H, Caldwell KS, Meyers BC, Michelmore RW. Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J 2008, 54(1):69-80. 10.1111/j.1365-313X.2008.03408.x, 18182023.
15. Chen Q, Han Z, Jiang H, Tian D, Yang S. Strong positive selection drives rapid diversification of R-genes in Arabidopsis relatives. J Mol Evol 2010, 70(2):137-148. 10.1007/s00239-009-9316-4, 20044783.
16. Ashfield T, Egan A, Pfeil B, Chen N, Podicheti R, Ratnaparkhe M, Ameline-Torregrosa C, Denny R, Cannon S, Doyle J. Evolution of a complex disease resistance gene cluster in diploid phaseolus and tetraploid glycine1. Plant Physiol 2012, 112:195040.
17. Luo S, Peng J, Li K, Wang M, Kuang H. Contrasting evolutionary patterns of the Rp1 resistance gene family in different species of Poaceae. Mol Biol Evol 2011, 28(1):313-325. 10.1093/molbev/msq216, 20713469.
18. Grant MR, McDowell JM, Sharpe AG, de Torres ZM, Lydiate DJ, Dangl JL. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc Natl Acad Sci USA 1998, 95(26):15843-15848. 10.1073/pnas.95.26.15843, 28132, 9861058.
19. Henk AD, Warren RF, Innes RW. A new Ac-like transposon of Arabidopsis is associated with a deletion of the RPS5 disease resistance gene. Genetics 1999, 151(4):1581-1589. 1460570, 10101179.
20. Shen J, Araki H, Chen L, Chen JQ, Tian D. Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 2006, 172(2):1243-1250. 1456222, 16452149.
21. Tian D, Araki H, Stahl E, Bergelson J, Kreitman M. Signature of balancing selection in Arabidopsis. Proc Natl Acad Sci USA 2002, 99(17):11525-11530. 10.1073/pnas.172203599, 123289, 12172007.
22. Tian D, Traw M, Chen J, Kreitman M, Bergelson J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 2003, 423(6935):74-77. 10.1038/nature01588, 12721627.
23. Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 2013, 496(7443):91-95. 10.1038/nature12028, 23535592.
24. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D. The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet 2010, 42(10):833-839. 10.1038/ng.654, 20802477.
25. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 2008, 452(7190):991-996. 10.1038/nature06856, 2836516, 18432245.
26. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P. The genome of the cucumber, Cucumis sativus L. Nat Genet 2009, 41(12):1275-1281. 10.1038/ng.475, 19881527.
27. Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E. The genome of melon (Cucumis melo L.). Proc Natl Acad Sci USA 2012, 109:11872-11877. 10.1073/pnas.1205415109, 3406823, 22753475.
28. Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 2012, 45:51-58. 10.1038/ng.2470, 23179023.
29. Zhang M, Wu YH, Lee MK, Liu YH, Rong Y, Santos TS, Wu C, Xie F, Nelson RL, Zhang HB. Numbers of genes in the NBS and RLK families vary by more than four-fold within a plant species and are regulated by multiple factors. Nucleic Acids Res 2010, 38(19):6513-6525. 10.1093/nar/gkq524, 2965241, 20542917.
30. Huang S, Xu X, Pan S. Genome sequence and analysis of the tuber crop potato. Nature 2011, 475:U189-U194.
31. Brenchley R, Spannagl M, Pfeifer M, Barker GLA, D/'Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 2012, 491(7426):705-710. 10.1038/nature11650, 3510651, 23192148.
32. Joobeur T, King JJ, Nolin SJ, Thomas CE, Dean RA. The Fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant J 2004, 39(3):283-297. 10.1111/j.1365-313X.2004.02134.x, 15255859.
33. Kang H, Weng Y, Yang Y, Zhang Z, Zhang S, Mao Z, Cheng G, Gu X, Huang S, Xie B. Fine genetic mapping localizes cucumber scab resistance gene Ccu into an R gene cluster. Theor Appl Genet 2011, 122(4):795-803. 10.1007/s00122-010-1487-2, 21104067.
34. Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J. Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics 2013, 14:109. 10.1186/1471-2164-14-109, 3599390, 23418910.
35. Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen JQ, Tian D, Yang S. Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Genet Genomics 2010, 283(5):427-438. 10.1007/s00438-010-0527-6, 20217430.
36. Yang S, Zhang X, Yue JX, Tian D, Chen JQ. Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 2008, 280(3):187-198. 10.1007/s00438-008-0355-0, 18563445.
37. Ameline-Torregrosa C, Wang BB, O'Bleness MS, Deshpande S, Zhu H, Roe B, Young ND, Cannon SB. Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 2008, 146(1):5-21. 2230567, 17981990.
38. Rogozin IB, Wolf YI, Sorokin AV, Mirkin BG, Koonin EV. Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr Biol 2003, 13(17):1512-1517. 10.1016/S0960-9822(03)00558-X, 12956953.
39. Ghebretinsae AG, Thulin M, Barber JC. Relationships of cucumbers and melons unraveled: molecular phylogenetics of Cucumis and related genera (Benincaseae, Cucurbitaceae). Am J Bot 2007, 94(7):1256-1266. 10.3732/ajb.94.7.1256, 21636491.
40. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28(12):1647-1649. 10.1093/bioinformatics/bts199, 3371832, 22543367.
41. Brotman Y, Silberstein L, Kovalski I, Perin C, Dogimont C, Pitrat M, Klingler J, Thompson A, Perl-Treves R. Resistance gene homologues in melon are linked to genetic loci conferring disease and pest resistance. Theor Appl Genet 2002, 104(6-7):1055-1063.
42. Pan Q, Wendel J, Fluhr R. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 2000, 50(3):203-213.
43. Chini A, Grant JJ, Seki M, Shinozaki K, Loake GJ. Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J 2004, 38(5):810-822. 10.1111/j.1365-313X.2004.02086.x, 15144382.
44. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 2005, 15(10):968-973. 10.1016/j.cub.2005.04.053, 15916955.
45. Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B. MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 2012, 109(5):1790-1795. 10.1073/pnas.1118282109, 3277104, 22307647.
46. Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 2011, 25(23):2540-2553. 10.1101/gad.177527.111, 3243063, 22156213.
47. Naqvi S.A.M.H.E Diseases of Fruits and Vegetables 2004, I. Dordrecht, The Netherlands: Diagnosis and Management, Published by Kluwer Academic Publishers, Naqvi S.A.M.H.E.
48. Bernatzky R, Tanksley SD. Toward a saturated linkage map in tomato based on isozymes and random cDNA sequences. Genetics 1986, 112(4):887-898. 1202783, 17246322.
49. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J. The Pfam protein families database. Nucleic Acids Res 2012, 40:D290-301. 10.1093/nar/gkr1065, 3245129, 22127870.
50. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
52. Xu Q, Wen X, Deng X. Phylogenetic and evolutionary analysis of NBS-encoding genes in Rosaceae fruit crops. Mol Phyogenet Evol 2007, 44(1):315-324.
53. Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol 1989, 6(5):526-538.
54. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 2002, 12(12):1871-1884. 10.1101/gr.454902, 187567, 12466291.
55. Richly E, Kurth J, Leister D. Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 2002, 19(1):76-84. 10.1093/oxfordjournals.molbev.a003984, 11752192.