A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Yang, Luming ^a   Li, Dawei ^a,b   Li, Yuhong ^a,b   Gu, Xingfang ^c   Huang, Sanwen ^c   Garcia Mas, Jordi ^d   Weng, Yiqun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NORTHWEST A F UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d IRTA   (Spain)

Author keywords

Comparative mapping; Cucumber; Cucumis sativus; Genetic mapping; Map integration; NB LRR; Resistance gene homolog

Indexed keywords

CUCUMIS; CUCUMIS SATIVUS;

ARTICLE; CHROMOSOME MAP; CUCUMBER; GENETICS; METHODOLOGY; PLANT GENOME;

CHROMOSOME MAPPING; CUCUMIS SATIVUS; GENOME, PLANT;

MLCS; MLOWN;

EID: 84875314914     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-53     Document Type: Article

References (70)

1. Jones JDG, Dangl JL. The plant immune system. Nature 2006, 444(7117):323-329. 10.1038/nature05286, 17108957.
2. Martin GB, Bogdanove AJ, Sessa G. Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 2003, 54:23-61. 10.1146/annurev.arplant.54.031902.135035, 14502984.
3. Ellis J, Dodds P, Pryor T. Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 2000, 3(4):278-284. 10.1016/S1369-5266(00)00080-7, 10873844.
4. McDowell JM, Woffenden BJ. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol 2003, 21(4):178-183. 10.1016/S0167-7799(03)00053-2, 12679066.
5. Lukasik E, Takken FLW. STANDing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol 2009, 12(4):427-436. 10.1016/j.pbi.2009.03.001, 19394891.
6. 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.
7. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F. Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 2008, 66(6):619-636. 10.1007/s11103-008-9293-9, 18247136.
8. Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G. Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS One 2012, 7(4):e34775. 10.1371/journal.pone.0034775, 3321028, 22493716.
9. Jupe F, Pritchard L, Etherington G, MacKenzie K, Cock P, Wright F, Sharma SK, Bolser D, Bryan G, Jones J. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics 2012, 13(1):75. 10.1186/1471-2164-13-75, 3297505, 22336098.
10. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 2004, 271(4):402-415. 10.1007/s00438-004-0990-z, 15014983.
11. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A. The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457(7229):551-556. 10.1038/nature07723, 19189423.
12. Yang S, Zhang X, Yue J-X, Tian D, Chen J-Q. 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.
13. Ribas AF, Cenci A, Combes MC, Etienne H, Lashermes P. Organization and molecular evolution of a disease-resistance gene cluster in coffee trees. BMC Genomics 2011, 12:240. 10.1186/1471-2164-12-240, 3113787, 21575174.
14. 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.
15. Porter BW, Paidi M, Ming R, Alam M, Nishijima WT, Zhu YJ. Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genomics 2009, 281(6):609-626. 10.1007/s00438-009-0434-x, 19263082.
16. 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.
17. Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 1998, 8(11):1113-1130.
18. Yahiaoui N, Brunner S, Keller B. Rapid generation of new powdery mildew resistance genes after wheat domestication. Plant J 2006, 47(1):85-98. 10.1111/j.1365-313X.2006.02772.x, 16740148.
19. Meyers BC, Kaushik S, Nandety RS. Evolving disease resistance genes. Curr Opin Plant Biol 2005, 8(2):129-134. 10.1016/j.pbi.2005.01.002, 15752991.
20. Mazourek M, Cirulli ET, Collier SM, Landry LG, Kang BC, Quirin EA, Bradeen JM, Moffett P, Jahn MM. The fractionated orthology of Bs2 and Rx/Gpa2 supports shared synteny of disease resistance in the Solanaceae. Genetics 2009, 182(4):1351-1364. 10.1534/genetics.109.101022, 2728872, 19474202.
21. Drader T, Kleinhofs A. A synteny map and disease resistance gene comparison between barley and the model monocot Brachypodium distachyon. Genome 2010, 53(5):406-417. 10.1139/G10-014, 20616871.
22. Weng Y, Sun ZY. Chapter 1 Major Cucurbits. Genetics, Genomics and Breeding of Cucurbits 2012, 1-16. New York: CRC Press, Wang YH, Behera TK, Kole C.
23. 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.
24. Cavagnaro PF, Senalik DA, Yang L, Simon PW, Harkins TT, Kodira CD, Huang S, Weng Y. Genome-wide characterization of simple sequence repeats in cucumber (Cucumis sativus L.). BMC Genomics 2010, 11:569. 10.1186/1471-2164-11-569, 3091718, 20950470.
25. Woycicki R, Witkowicz J, Gawronski P, Dabrowska J, Lomsadze A, Pawelkowicz M, Siedlecka E, Yagi K, Plader W, Seroczynska A. The genome sequence of the north-European cucumber (Cucumis sativus L.) unravels evolutionary adaptation mechanisms in plants. PLoS One 2011, 6(7):22728.
26. Li Z, Zhang ZH, Yan PC, Huang SW, Fei ZJ, Lin K. RNA-Seq improves annotation of protein-coding genes in the cucumber genome. BMC Genomics 2011, 12:540. 10.1186/1471-2164-12-540, 3219749, 22047402.
27. Yang L, Koo DH, Li Y, Zhang X, Luan F, Havey MJ, Jiang J, Weng Y. Chromosome rearrangements during domestication of cucumber as revealed from high-density genetic mapping and draft genome assembly. Plant J 2012, 71(6):895-906. 10.1111/j.1365-313X.2012.05017.x, 22487099.
28. Li Y, Yang L, Pathak M, Li D, He X, Weng Y. Fine genetic mapping of cp: a recessive gene for compact (dwarf) plant architecture in cucumber, Cucumis sativus L. Theor Appl Genet 2011, 123(6):973-983. 10.1007/s00122-011-1640-6, 21735235.
29. van Leeuwen H, Garcia-Mas J, Coca M, Puigdomenech P, Monfort A. Analysis of the melon genome in regions encompassing TIR-NBS-LRR resistance genes. Mol Genet Genomics 2005, 273(3):240-251. 10.1007/s00438-004-1104-7, 15902490.
30. Brotman Y, Silberstein L, Kovalski I, Perin C, Dogimont C, Pitrat M, Klingler J, Thompson GA, 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.
31. Shang W, Zhou RH, Jia JZ, Gao LF. RGA-ILP, a new type of functional molecular markers in bread wheat. Euphytica 2010, 172(2):263-273.
32. Kang HX, Weng YQ, Yang YH, Zhang ZH, Zhang SP, Mao ZC, Cheng GH, Gu XF, Huang SW, Xie BY. 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.
33. Bachlava E, Radwan OE, Abratti G, Tang S, Gao W, Heesacker AF, Bazzalo ME, Zambelli A, Leon AJ, Knapp SJ. Downy mildew (Pl (8) and Pl (14)) and rust (R (Adv)) resistance genes reside in close proximity to tandemly duplicated clusters of non-TIR-like NBS-LRR-encoding genes on sunflower chromosomes 1 and 13. Theor Appl Genet 2011, 122(6):1211-1221. 10.1007/s00122-010-1525-0, 21293840.
34. Bakker E, Borm T, Prins P, van der Vossen E, Uenk G, Arens M, de Boer J, van Eck H, Muskens M, Vossen J. A genome-wide genetic map of NB-LRR disease resistance loci in potato. Theor Appl Genet 2011, 123(3):493-508. 10.1007/s00122-011-1602-z, 3135832, 21590328.
35. Okuyama Y, Kanzaki H, Abe A, Yoshida K, Tamiru M, Saitoh H, Fujibe T, Matsumura H, Shenton M, Galam DC. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J 2011, 66(3):467-479. 10.1111/j.1365-313X.2011.04502.x, 21251109.
36. Liu XQ, Lin F, Wang L, Pan QH. The in silico map-based cloning of Pi36, a rice coiled-coil-nucleotide-binding site-leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics 2007, 176(4):2541-2549. 10.1534/genetics.107.075465, 1950653, 17507669.
37. Shang JJ, Tao Y, Chen XW, Zou Y, Lei CL, Wang J, Li XB, Zhao XF, Zhang MJ, Lu ZK. Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site-leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics 2009, 182(4):1303-1311. 10.1534/genetics.109.102871, 2728867, 19506306.
38. Bresson A, Jorge V, Dowkiw A, Guerin V, Bourgait I, Tuskan GA, Schmutz J, Chalhoub B, Bastien C, Rampant PF. Qualitative and quantitative resistances to leaf rust finely mapped within two nucleotide-binding site leucine-rich repeat (NBS-LRR)-rich genomic regions of chromosome 19 in poplar. New Phytol 2011, 192(1):151-163. 10.1111/j.1469-8137.2011.03786.x, 21658182.
39. Mutlu N, Miklas PN, Coyne DP. Resistance gene analog polymorphism (RGAP) markers co-localize with disease resistance genes and QTL in common bean. Mol Breed 2006, 17(2):127-135.
40. Knerr LD, Staub JE, Holder DJ, May BP. Genetic diversity in Cucumis sativus L. assessed by variation at 18 allozyme coding loci. Theor Appl Genet 1989, 78(1):119-128.
41. Dijkhuizen A, Kennard WC, Havey MJ, Staub JE. RFLP variation and genetic relationships in cultivated cucumber. Euphytica 1996, 90(1):79-87.
42. Ren Y, Zhang Z, Liu J, Staub JE, Han Y, Cheng Z, Li X, Lu J, Miao H, Kang H. An integrated genetic and cytogenetic map of the cucumber genome. PLoS One 2009, 4(6):e5795. 10.1371/journal.pone.0005795, 2685989, 19495411.
43. Weng YQ, Johnson S, Staub JE, Huang SW. An extended intervarietal microsatellite linkage map of cucumber, Cucumis sativus L. HortSci 2010, 45(6):882-886.
44. Zhang WW, Pan JS, He HL, Zhang C, Li Z, Zhao JL, Yuan XJ, Zhu LH, Huang SW, Cai R. Construction of a high density integrated genetic map for cucumber (Cucumis sativus L.). Theor Appl Genet 2012, 124(2):249-259. 10.1007/s00122-011-1701-x, 21971891.
45. Miao H, Zhang SP, Wang XW, Zhang ZH, Li M, Mu SQ, Cheng ZC, Zhang RW, Huang SW, Xie BY. A linkage map of cultivated cucumber (Cucumis sativus L.) with 248 microsatellite marker loci and seven genes for horticulturally important traits. Euphytica 2011, 182(2):167-176.
46. Zhang SP, Miao H, Gu XF, Yang YH, Xie BY, Wang XW, Huang SW, Du YC, Sun RF, Wehner TC. Genetic mapping of the scab resistance gene in cucumber. J Am Soc Hort Sci 2010, 135(1):53-58.
47. Diaz A, Fergany M, Formisano G, Ziarsolo P, Blanca J, Fei Z, Staub JE, Zalapa JE, Cuevas HE, Dace G. A consensus linkage map for molecular markers and quantitative trait loci associated with economically important traits in melon (Cucumis melo L.). BMC Plant Biol 2011, 11:111. 10.1186/1471-2229-11-111, 3163537, 21797998.
48. Truco MJ, Antonise R, Lavelle D, Ochoa O, Kozik A, Witsenboer H, Fort SB, Jeuken MJ, Kesseli RV, Lindhout P. A high-density, integrated genetic linkage map of lettuce (Lactuca spp.). Theor Appl Genet 2007, 115(6):735-746. 10.1007/s00122-007-0599-9, 17828385.
49. Vezzulli S, Troggio M, Coppola G, Jermakow A, Cartwright D, Zharkikh A, Stefanini M, Grando MS, Viola R, Adam-Blondon AF. A reference integrated map for cultivated grapevine (Vitis vinifera L.) from three crosses, based on 283 SSR and 501 SNP-based markers. Theor Appl Genet 2008, 117(4):499-511. 10.1007/s00122-008-0794-3, 18504538.
50. Muchero W, Diop NN, Bhat PR, Fenton RD, Wanamaker S, Pottorff M, Hearne S, Cisse N, Fatokun C, Ehlers JD. A consensus genetic map of cowpea [Vigna unguiculata (L) Walp.] and synteny based on EST-derived SNPs. Proc Natl Acad Sci U S A 2009, 106(43):18159-18164. 10.1073/pnas.0905886106, 2761239, 19826088.
51. Isobe S, Kolliker R, Hisano H, Sasamoto S, Wada T, Klimenko I, Okumura K, Tabata S. Construction of a consensus linkage map for red clover (Trifolium pratense L.). BMC Plant Biol 2009, 9:57. 10.1186/1471-2229-9-57, 2695442, 19442273.
52. Mace ES, Rami JF, Bouchet S, Klein PE, Klein RR, Kilian A, Wenzl P, Xia L, Halloran K, Jordan DR. A consensus genetic map of sorghum that integrates multiple component maps and high-throughput Diversity Array Technology (DArT) markers. BMC Plant Biol 2009, 9:13. 10.1186/1471-2229-9-13, 2671505, 19171067.
53. Hwang TY, Sayama T, Takahashi M, Takada Y, Nakamoto Y, Funatsuki H, Hisano H, Sasamoto S, Sato S, Tabata S. High-density integrated linkage map based on SSR markers in soybean. DNA Res 2009, 16(4):213-225. 10.1093/dnares/dsp010, 2725787, 19531560.
54. Hyten DL, Choi IY, Song QJ, Specht JE, Carter TE, Shoemaker RC, Hwang EY, Matukumalli LK, Cregan PB. A high density integrated genetic linkage map of soybean and the development of a 1536 universal soy linkage panel for quantitative trait locus mapping. Crop Sci 2010, 50(3):960-968.
55. Wang J, Lydiate DJ, Parkin IA, Falentin C, Delourme R, Carion PW, King GJ. Integration of linkage maps for the amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genomics 2011, 12:101. 10.1186/1471-2164-12-101, 3042011, 21306613.
56. Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM. The genome of melon (Cucumis melo L.). Proc Natl Acad Sci U S A 2012, 109(29):11872-11877. 10.1073/pnas.1205415109, 3406823, 22753475.
57. Li D, Cuevas HE, Yang L, Li Y, Garcia-Mas J, Zalapa J, Staub JE, Luan F, Reddy U, He X. Syntenic relationships between cucumber (Cucumis sativus L.) and melon (C. melo L.) chromosomes as revealed by comparative genetic mapping. BMC Genomics 2011, 12:396. 10.1186/1471-2164-12-396, 3199783, 21816110.
58. Li Z, Huang SW, Liu SQ, Pan JS, Zhang ZH, Tao QY, Shi QX, Jia ZQ, Zhang WW, Chen HM. Molecular isolation of the m gene suggests that a conserved-residue conversion induces the formation of bisexual flowers in cucumber plants. Genetics 2009, 182(4):1381-1385. 10.1534/genetics.109.104737, 2728875, 19474195.
59. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449(7161):463-465. 10.1038/nature06148, 17721507.
60. Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers BC, Michelmore RW. Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant Microbe Interact 2002, 15(3):251-261. 10.1094/MPMI.2002.15.3.251, 11952128.
61. Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 1998, 10(8):1307-1319. 144378, 9707531.
62. Tan XP, Meyers BC, Kozik A, Al West M, Morgante M, St Clair DA, Bent AF, Michelmore RW. Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol 2007, 7:56. 10.1186/1471-2229-7-56, 2175511, 17956627.
63. Pan QL, Liu YS, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R. Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 2000, 155(1):309-322. 1461067, 10790405.
64. Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D. Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 2011, 157(2):757-769. 10.1104/pp.111.181990, 3192553, 21810963.
65. Sebastian P, Schaefer H, Telford IRH, Renner SS. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc Natl Acad Sci U S A 2010, 107(32):14269-14273. 10.1073/pnas.1005338107, 2922565, 20656934.
66. 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. Nucl Acid Res 2012, 40(D1):D290-D301.
67. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
68. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25(9):1189-1191. 10.1093/bioinformatics/btp033, 2672624, 19151095.
69. 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.
70. Krzywinski M, Schein J, Birol T, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19(9):1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.