Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber

Plant Cell

Volumn 27, Issue 6, 2015, Pages 1595-1604

  Zhang, Zhonghua ^a   Mao, Linyong ^b,m   Chen, Huiming ^c   Bu, Fengjiao ^a,d   Li, Guangcun ^a,e   Sun, Jinjing ^a   Li, Shuai ^a   Sun, Honghe ^b   Jiao, Chen ^b   Blakely, Rachel ^b   Pan, Junsong ^f   Cai, Run ^f   Luo, Ruibang ^g   Van de Peer, Yves ^h,i,j   Jacobsen, Evert ^k   Fei, Zhangjun ^b,l   Huang, Sanwen ^a,d  

^a AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^c Hunan Academy of Agricultural Sciences   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e SHANDONG PEANUT RESEARCH INSTITUTE   (China)

^f SHANGHAI JIAO TONG UNIVERSITY   (China)

^g UNIVERSITY OF HONG KONG   (Hong Kong)

^h DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

ⁱ GHENT UNIVERSITY   (Belgium)

^j UNIVERSITY OF PRETORIA   (South Africa)

^k WAGENINGEN UNIVERSITY   (Netherlands)

^l ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

^m HOWARD UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CUCUMIS; CUCUMIS SATIVUS;

ANATOMY AND HISTOLOGY; CHROMOSOMAL MAPPING; COPY NUMBER VARIATION; CUCUMBER; FLOWER; GENETICS; GENOME-WIDE ASSOCIATION STUDY; PHYLOGENY; PLANT GENOME;

CHROMOSOME MAPPING; CUCUMIS SATIVUS; DNA COPY NUMBER VARIATIONS; FLOWERS; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; PHYLOGENY;

EID: 84936931699     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.135848     Document Type: Article

References (55)

1. Alkan, C., Coe, B. P., and Eichler, E. E. (2011). Genome structural variation discovery and genotyping. Nat. Rev. Genet. 12: 363-376.
2. Anonymous (1973). Vademecum voor de Glastuinbouw: Glasgroenten, Glasbloemen, Champignons. (The Hague, The Netherlands: Landbouw-Economisch Instituut).
3. Baker, M. (2012). Structural variation: the genome's hidden architecture. Nat. Methods 9: 133-137.
4. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
5. Bradbury, P. J., Zhang, Z., Kroon, D. E., Casstevens, T. M., Ramdoss, Y., and Buckler, E. S. (2007). TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23: 2633-2635.
6. Cao, J., et al. (2011). Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43: 956-963.
7. Chia, J.-M., et al. (2012). Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44: 803-807.
8. Diskin, S. J., et al. (2009). Copy number variation at 1q21. 1 associated with neuroblastoma. Nature 459: 987-991.
9. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696-704.
10. Guo, S., Zheng, Y., Joung, J. G., Liu, S., Zhang, Z., Crasta, O. R., Sobral, B. W., Xu, Y., Huang, S., and Fei, Z. (2010). Transcriptome sequencing and comparative analysis of cucumber flowers with different sex types. BMC Genomics 11: 384.
11. Handsaker, R. E., Korn, J. M., Nemesh, J., and McCarroll, S. A. (2011). Discovery and genotyping of genome structural polymorphism by sequencing on a population scale. Nat. Genet. 43: 269-276.
12. Hodgkinson, A., and Eyre-Walker, A. (2011). Variation in the mutation rate across mammalian genomes. Nat. Rev. Genet. 12: 756-766.
13. Hollister, J. D., Ross-Ibarra, J., and Gaut, B. S. (2010). Indel-associated mutation rate varies with mating system in flowering plants. Mol. Biol. Evol. 27: 409-416.
14. Horiguchi, G., Gonzalez, N., Beemster, G. T., Inzé, D., and Tsukaya, H. (2009). Impact of segmental chromosomal duplications on leaf size in the grandifolia-D mutants of Arabidopsis thaliana. Plant J. 60: 122-133.
15. Huang, S., et al. (2009). The genome of the cucumber, Cucumis sativus L. Nat. Genet. 41: 1275-1281.
16. Iafrate, A. J., Feuk, L., Rivera, M. N., Listewnik, M. L., Donahoe, P. K., Qi, Y., Scherer, S. W., and Lee, C. (2004). Detection of large-scale variation in the human genome. Nat. Genet. 36: 949-951.
17. Jovelin, R., and Cutter, A. D. (2013). Fine-scale signatures of molecular evolution reconcile models of indel-associated mutation. Genome Biol. Evol. 5: 978-986.
18. Kim, P. M., Lam, H. Y., Urban, A. E., Korbel, J. O., Affourtit, J., Grubert, F., Chen, X., Weissman, S., Snyder, M., and Gerstein, M. B. (2008). Analysis of copy number variants and segmental duplications in the human genome: Evidence for a change in the process of formation in recent evolutionary history. Genome Res. 18: 1865-1874.
19. Klambauer, G., Schwarzbauer, K., Mayr, A., Clevert, D. A., Mitterecker, A., Bodenhofer, U., and Hochreiter, S. (2012). cn. MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res. 40: e69.
20. Knopf, R. R., and Trebitsh, T. (2006). The female-specific Cs-ACS1G gene of cucumber. A case of gene duplication and recombination between the non-sex-specific 1-aminocyclopropane-1-carboxylate synthase gene and a branched-chain amino acid transaminase gene. Plant Cell Physiol. 47: 1217-1228.
21. Lee, J. A., Carvalho, C. M., and Lupski, J. R. (2007). A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131: 1235-1247.
22. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
23. Li, R., et al. (2010). De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20: 265-272.
24. Li, Z., Zhang, Z., Yan, P., Huang, S., Fei, Z., and Lin, K. (2011). RNASeq improves annotation of protein-coding genes in the cucumber genome. BMC Genomics 12: 540.
25. Lv, J., et al. (2012). Genetic diversity and population structure of cucumber (Cucumis sativus L.). PLoS ONE 7: e46919.
26. Maron, L. G., et al. (2013). Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc. Natl. Acad. Sci. USA 110: 5241-5246.
27. McCarthy, S. E., et al. ; Wellcome Trust Case Control Consortium (2009) Microduplications of 16p11. 2 are associated with schizophrenia. Nat. Genet. 41: 1223-1227.
28. McDonald, M. J., Wang, W. C., Huang, H. D., and Leu, J. Y. (2011). Clusters of nucleotide substitutions and insertion/deletion mutations are associated with repeat sequences. PLoS Biol. 9: e1000622.
29. McHale, L. K., Haun, W. J., Xu, W. W., Bhaskar, P. B., Anderson, J. E., Hyten, D. L., Gerhardt, D. J., Jeddeloh, J. A., and Stupar, R. M. (2012). Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol. 159: 1295-1308.
30. Mills, R. E., et al. ; 1000 Genomes Project (2011). Mapping copy number variation by population-scale genome sequencing. Nature 470: 59-65.
31. Müller, S., Han, S., and Smith, L. G. (2006). Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol. 16: 888-894.
32. Muñoz-Amatriaín, M., et al. (2013). Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol. 14: R58.
33. Pinto, D., et al. (2010). Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466: 368-372.
34. Qi, J., et al. (2013). A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat. Genet. 45: 1510-1515.
35. Saxena, R. K., Edwards, D., and Varshney, R. K. (2014). Structural variations in plant genomes. Brief Funct. Genomics 13: 296-307.
36. Schnable, P. S., et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
37. Sebat, J., et al. (2007). Strong association of de novo copy number mutations with autism. Science 316: 445-449.
38. Shifriss, O. (1961). Sex control in cucumbers. J. Hered. 51: 5-12.
39. Stefansson, H., et al. (2008) Large recurrent microdeletions associated with schizophrenia. Nature 455: 232-236.
40. Tanurdzic, M., and Banks, J. A. (2004). Sex-determining mechanisms in land plants. Plant Cell 16 (suppl.): S61-S71.
41. Tian, D., Wang, Q., Zhang, P., Araki, H., Yang, S., Kreitman, M., Nagylaki, T., Hudson, R., Bergelson, J., and Chen, J. Q. (2008). Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 455: 105-108.
42. Trebitsh, T., Staub, J. E., and O'Neill, S. D. (1997). Identification of a 1-aminocyclopropane-1-carboxylic acid synthase gene linked to the female (F) locus that enhances female sex expression in cucumber. Plant Physiol. 113: 987-995.
43. Vermeulen, P. C. M. (2012). Kwantitatieve informatie voor de Glastuinbouw 2012-2013: Kengetallen voor groenten, snijbloemen, potplanten tewelten. (Wageningen, The Netherlands: Wageningen UR Glastuinbouw).
44. Xiao, H., Jiang, N., Schaffner, E., Stockinger, E. J., and van der Knaap, E. (2008). A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527-1530.
45. Xu, Z., and Wang, H. (2007). LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35: W265-W268.
46. Yalcin, B., Wong, K., Bhomra, A., Goodson, M., Keane, T. M., Adams, D. J., and Flint, J. (2012). The fine-scale architecture of structural variants in 17 mouse genomes. Genome Biol. 13: R18.
47. Yalcin, B., et al. (2011). Sequence-based characterization of structural variation in the mouse genome. Nature 477: 326-329.
48. Yang, L., et al. (2013). Diverse mechanisms of somatic structural variations in human cancer genomes. Cell 153: 919-929.
49. Yang, X., Zhang, W., He, H., Nie, J., Bie, B., Zhao, J., Ren, G., Li, Y., Zhang, D., Pan, J., and Cai, R. (2014). Tuberculate fruit gene Tu encodes a C2 H2 zinc finger protein that is required for the warty fruit phenotype in cucumber (Cucumis sativus L.). Plant J. 78: 1034-1046.
50. Ye, K., Schulz, M. H., Long, Q., Apweiler, R., and Ning, Z. (2009). Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25: 2865-2871.
51. Yu, P., Wang, C. H., Xu, Q., Feng, Y., Yuan, X. P., Yu, H. Y., Wang, Y. P., Tang, S. X., and Wei, X. H. (2013). Genome-wide copy number variations in Oryza sativa L. BMC Genomics 14: 649.
52. Zeitouni, B., Boeva, V., Janoueix-Lerosey, I., Loeillet, S., Legoix-né, P., Nicolas, A., Delattre, O., and Barillot, E. (2010). SVDetect: a tool to identify genomic structural variations from paired-end and mate-pair sequencing data. Bioinformatics 26: 1895-1896.
53. Zhang, W., He, H., Guan, Y., Du, H., Yuan, L., Li, Z., Yao, D., Pan, J., and Cai, R. (2010a). Identification and mapping of molecular markers linked to the tuberculate fruit gene in the cucumber (Cucumis sativus L.). Theor. Appl. Genet. 120: 645-654.
54. Zhang, Z., Ersoz, E., Lai, C. Q., Todhunter, R. J., Tiwari, H. K., Gore, M. A., Bradbury, P. J., Yu, J., Arnett, D. K., Ordovas, J. M., and Buckler, E. S. (2010b). Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42: 355-360.
55. Zichner, T., Garfield, D. A., Rausch, T., Stütz, A. M., Cannavó, E., Braun, M., Furlong, E. E., and Korbel, J. O. (2013). Impact of genomic structural variation in Drosophila melanogaster based on population-scale sequencing. Genome Res. 23: 568-579.