Origin and domestication of papaya Yh chromosome

Genome Research

Volumn 25, Issue 4, 2015, Pages 524-533

  VanBuren, Robert ^a,b   Zeng, Fanchang ^b   Chen, Cuixia ^b   Zhang, Jisen ^a   Wai, Ching Man ^b   Han, Jennifer ^b   Aryal, Rishi ^b   Gschwend, Andrea R ^b   Wang, Jianping ^b   Na, Jong Kuk ^b   Huang, Lixian ^a   Zhang, Lingmao ^a   Miao, Wenjing ^a   Gou, Jiqing ^c   Arro, Jie ^b   Guyot, Romain ^d   Moore, Richard C ^e   Wang, Ming Li ^f   Zee, Francis ^g   Charlesworth, Deborah ^h   Moore, Paul H ^f   Yu, Qingyi ^c   Ming, Ray ^a,b   more..

^a FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^e MIAMI UNIVERSITY   (United States)

^f HAWAII AGRICULTURE RESEARCH CENTER   (United States)

^g AGRICULTURAL RESEARCH SERVICE   (United States)

^h UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COSTA RICA; CROP; DIOECY; DOMESTICATION; GENE FLOW; GENE MUTATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HERMAPHRODITE; MALE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAPAYA; PLANT CHROMOSOME; POPULATION STRUCTURE; PRIORITY JOURNAL; CARICA; DNA SEQUENCE; GENETICS; MOLECULAR GENETICS; PLANT BREEDING; SEX; SEX CHROMOSOME; SEX DETERMINATION PROCESS; SINGLE NUCLEOTIDE POLYMORPHISM;

CARICA PAPAYA;

BASE SEQUENCE; CARICA; CHROMOSOMES, PLANT; GENE FLOW; HAPLOTYPES; HERMAPHRODITIC ORGANISMS; MOLECULAR SEQUENCE DATA; PLANT BREEDING; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; SEX; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES;

EID: 84927730193     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.183905.114     Document Type: Article

References (51)

1. Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman T-L, Hahn MW, Kitano J, Mayrose I, Ming R, et al. 2014. Sex determination: why so many ways of doing it? PLoS Biol 12: e1001899.
2. Beilstein M, Nagalingum N, Clements M, Manchester S, Mathews S. 2010. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana . Proc Natl Acad Sci 107: 18724-18728.
3. Bellott DW, Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Cho T-J, Koutseva N, Zaghlul S, Graves T, Rock S. 2014. Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508: 494-499.
4. Bemis W, Wilson G. 1953. A new hypothesis explaining the genetics of sex determination in Spinacia oleracea L. J Hered 44: 91-95.
5. Bergero R, Charlesworth D, Filatov DA, Moore RC. 2008. Defining regions and rearrangements of the Silene latifolia Y chromosome. Genetics 178: 2045-2053.
6. Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33: W451-W454.
7. Bowers JE, Chapman BA, Rong J, Paterson AH. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
8. Charlesworth B. 1998.Measures of divergence between populations and the effect of forces that reduce variability. Mol Biol Evol 15: 538-543.
9. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2: e64.
10. Charlesworth B. 2009. Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10: 195-205.
11. Colunga-GarcíaMarín P, Zizumbo-Villarreal D. 2004. Domestication of plants in Maya lowlands. Econ Bot 58: S101-S110.
12. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grützner F, Kaessmann H. 2014. Origins and functional evolution of Y chromosomes across mammals. Nature 508: 488-493.
13. Darling AC, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
14. Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I. 2010. The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64: 2873-2886.
15. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
16. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611-2620.
17. Falush D, Stephens M, Pritchard JK. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
18. Fujita N, Torii C, Ishii K, AonumaW, Shimizu Y, Kazama Y, Abe T, Kawano S. 2012. Narrowing down the mapping of plant sex-determination regions using new Y-chromosome-specific markers and heavy-ion beam irradiation-induced Y-deletion mutants in Silene latifolia. G3 (Bethesda) 2:271-278.
19. Gschwend AR, Yu Q, Moore P, Saski C, Chen C, Wang J, Na JK, Ming R. 2011. Construction of papaya male and female BAC libraries and application in physical mapping of the sex chromosomes. J Biomed Biotechnol 2011: 929472.
20. Gupta AK. 2004. Origin of agriculture and domestication of plants and animals linked to early Holocene climate amelioration. Curr Sci 87: 54-59.
21. Heled J, Drummond AJ. 2010. Bayesian inference of species trees from multilocus data. Mol Biol Evol 27: 570-580.
22. Hughes JF, Skaletsky H, Pyntikova T, Graves TA, van Daalen SK, Minx PJ, Fulton RS, McGrath SD, Locke DP, Friedman C. 2010. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463: 536-539.
23. Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Graves T, Fulton RS, Dugan S, Ding Y, Buhay CJ, Kremitzki C. 2012. Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483: 82-86.
24. Ironside JE, Filatov DA. 2005. Extreme population structure and high inter-specific divergence of the Silene Y chromosome. Genetics 171: 705-713.
25. Kirkpatrick M, Guerrero RF, Scarpino SV. 2010. Patterns of neutral genetic variation on recombining sex chromosomes. Genetics 184: 1141-1152.
26. Lardon A, Georgiev S, Aghmir A, Le Merrer G, Negrutiu I. 1999. Sexual dimorphism in white campion: complex control of carpel number is revealed by Y chromosome deletions. Genetics 151: 1173-1185.
27. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
28. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
29. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI. 2004. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348-352.
30. Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, Marshall D. 2010. Tablet - next generation sequence assembly visualization. Bioinformatics 26: 401-402.
31. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL. 2008. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991-996.
32. Ming R, Bendahmane A, Renner SS. 2011. Sex chromosomes in land plants. Annu Rev Plant Biol 62: 485-514.
33. Na J-K, Wang J, Ming R. 2014. Accumulation of interspersed and sex-specific repeats in the non-recombining region of papaya sex chromosomes. BMC Genomics 15: 335.
34. Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM, Shaw RG, Weigel D, Lynch M. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana . Science 327: 92-94.
35. Pohl MD, Pope KO, Jones JG, Jacob JS, Piperno DR, deFrance SD, Lentz DL, Gifford JA, Danforth ME, Josserand JK. 1996. Early agriculture in the Maya lowlands. Lat Am Antiq 7: 355-372.
36. Pope KO, Pohl ME, Jones JG, Lentz DL, Von Nagy C, Vega FJ, Quitmyer IR. 2001. Origin and environmental setting of ancient agriculture in the lowlands of Mesoamerica. Science 292: 1370-1373.
37. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org/.
38. Ruden DM, Lu X. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6: 80-92.
39. Soderlund C, Bomhoff M, Nelson WM. 2011. SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39: e68.
40. Spigler R, Lewers K, Main D, Ashman T. 2008. Genetic mapping of sex determination in a wild strawberry, Fragaria virginiana, reveals earliest form of sex chromosome. Heredity 101: 507-517.
41. Stanke M, Steinkamp R, Waack S, Morgenstern B. 2004. AUGUSTUS: a webserver for gene finding in eukaryotes. Nucleic Acids Res 32: W309-W312.
42. Storey W. 1976. Papaya. In Evolution of crop plants (ed. Simmonds N), pp. 21-24. Longman, London & New York.
43. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
44. Ueno H, Urasaki N, Natsume S, Yoshida K, Tarora K, Shudo A, Terauchi R, Matsumura H. 2014. Genome sequence comparison reveals a candidate gene involved in male-hermaphrodite differentiation in papaya (Carica papaya) trees. Mol Genet Genomics doi: 10.1007/s00438-014-0955-9.
45. Veyrunes F, Waters PD, Miethke P, Rens W, McMillan D, Alsop AE, Grützner F, Deakin JE, Whittington CM, Schatzkamer K. 2008. Bird-like sex chromosomes of platypus imply recent origin ofmammal sex chromosomes. Genome Res 18: 965-973.
46. Wang J, Na J-K, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, ZhangW. 2012. Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci 109: 13710-13715.
47. Weingartner LA, Moore RC. 2012. Contrasting patterns of X/Y polymorphism distinguish Carica papaya from other sex chromosome systems. Mol Biol Evol 29: 3909-3920.
48. Weir BS, Cockerham CC. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
49. Yu Q, Navajas-Pérez R, Tong E, Robertson J, Moore PH, Paterson AH, Ming R. 2008. Recent origin of dioecious and gynodioecious Y chromosomes in papaya. Trop Plant Biol 1: 49-57.
50. Zhou Q, Bachtrog D. 2012. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337: 341-345.
51. Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MTP, Zhang G. 2014. Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346: 1246338.