Plant Systematics and Evolution

, Volume 303, Issue 8, pp 1021–1042 | Cite as

Nucleotide diversity in the two co-resident genomes of allopolyploid cotton

  • Corrinne E. Grover
  • Joseph P. Gallagher
  • Emmanuel P. Szadkowski
  • Justin T. Page
  • Michael A. Gore
  • Joshua A. Udall
  • Jonathan F. Wendel
Original Article
Part of the following topical collections:
  1. Polyploidy in Shallow and Deep Evolutionary Times


Genetic diversity within and among populations lies at the heart of evolution. Unraveling the extent to which each intrinsic or extrinsic factor determines levels of diversity among genes, populations, and species is challenging, given the difficulty of isolating any single potentially important variable from all others. Allopolyploid species provide an opportunity to disentangle external and intrinsic factors, as the two (or more) homoeologous genomes co-occur in the same nucleus, often exhibiting high collinearity along homoeologous chromosomes. Here we evaluate the pace of molecular evolution and intraspecific, intragenomic diversity in two species of allopolyploid Gossypium, G. hirsutum and G. barbadense, using several hundred genes sequenced from multiple accessions of each species. Genic diversity in both species is low, having been influenced both by the polyploid bottleneck and a domestication bottleneck (for cultivated accessions), but with a directional bias in homoeolog diversity favoring the same genome in both allopolyploids. Total diversity is remarkably similar for the two homoeologous genomes overall, but the two copies of many gene pairs have accumulated statistically different diversity levels, and in a biased fashion with respect to genome. Domesticated accessions show reduced diversity in both genomes, as expected, but with a much greater reduction in one of the two homoeologous genomes. Furthermore, this biased reduction affects opposite homoeologous genomes in the two species. Interspecific introgression has played a role in shaping diversity within each species. Introgression was only detected for certain accessions, and only from G. barbadense into G. hirsutum in one of the two co-resident genomes.


Domestication Genetic variation Gossypium Hybridization Introgression Polyploidy 



We thank Guanjing Hu and Mark A. Arick for technical assistance; Daniel Ilut, John Nason, and Matthew Hufford for analytical advice; and Richard Percy for assistance in selecting the G. barbadense accessions. The authors are supported by the USDA-ARS and grants from the National Science Foundation, Supima, and Cotton Incorporated. J. P. Gallagher is supported by National Science Foundation Graduate Research Fellowship DGE1247194.

Compliance with Ethical Standards

Conflict of interest

The authors declare no conflicts of interest.

Human and animal rights statement

The present research does not involve human or animal participants. All authors have approved the manuscript.

Supplementary material

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  1. Abdalla MA, Reddy KOU, El-Zik MK, Pepper EA (2001) Genetic diversity and relationships of diploid and tetraploid cottons revealed using AFLP. Theor Appl Genet 102:222–229. doi: 10.1007/s001220051639 CrossRefGoogle Scholar
  2. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Pl Biol 8:135–141. doi: 10.1016/j.pbi.2005.01.001 CrossRefGoogle Scholar
  3. Aguade M, Miyashita N, Langley CH (1989) Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster. Genetics 122:607–615PubMedPubMedCentralGoogle Scholar
  4. Begun DJ, Aquadro CF (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356:519–520. doi: 10.1038/356519a0 PubMedCrossRefGoogle Scholar
  5. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Pl Cell 16:1679–1691. doi: 10.1105/tpc.021410 CrossRefGoogle Scholar
  6. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD, Mudge J, Bharti AK, Woodward JE, May GD, Gentzbittel L (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci USA 108:E864–E870. doi: 10.1073/pnas.1104032108 PubMedPubMedCentralCrossRefGoogle Scholar
  7. Brubaker CL, Wendel JF (1994) Re-evaluating the origin of domesticated cotton (Gossypium hirsutum; Malvaceae) using nuclear restriction fragment polymorphisms (RFLPs). Amer J Bot 81:1309–1326CrossRefGoogle Scholar
  8. Brubaker CL, Koontz JA, Wendel JF (1993) Bidirectional cytoplasmic and nuclear introgression in the new world cottons, Gossypium barbadense and G. hirsutum (Malvaceae). Amer J Bot 80:1203–1208CrossRefGoogle Scholar
  9. Brubaker CL, Paterson A, Wendel JF (1999a) Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42:184–203CrossRefGoogle Scholar
  10. Brubaker CL, Bourland EM, Wendel JF (1999b) The origin and domestication of cotton. In: Smith CW, Cothren JT (eds) Cotton: origin, history, technology, and production. Wiley, New York, pp 3–31Google Scholar
  11. Cai JJ, Macpherson JM, Sella G, Petrov DA (2009) Pervasive hitchhiking at coding and regulatory sites in humans. PLoS Genet 5:e1000336. doi: 10.1371/journal.pgen.1000336 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Fledel-Alon A, York TL, Polato NR, Olsen KM, Nielsen R, McCouch SR (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3:e163. doi: 10.1371/journal.pgen.0030163 PubMedCentralCrossRefGoogle Scholar
  13. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier M-C, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee T-H, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury J-M, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 345:950–953. doi: 10.1126/science.1253435 PubMedCrossRefGoogle Scholar
  14. Charif D, Lobry JR (2007) Seqin{r} 1.0-2: A contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In: Bastolla U, Porto M, Roman HE, Vendruscolo M (eds) Structural approaches to sequence evolution: molecules, networks, populations. Springer, New York, pp 207–232CrossRefGoogle Scholar
  15. Charlesworth B, Campos JL (2014) The relations between recombination rate and patterns of molecular variation and evolution in Drosophila. Annual Rev Genet 48:383–403. doi: 10.1146/annurev-genet-120213-092525 CrossRefGoogle Scholar
  16. Charlesworth B, Betancourt A, Kaiser V, Gordo I (2009) Genetic recombination and molecular evolution. Cold Spring Harbor Symp Quant Biol 74:177–186. doi: 10.1101/sqb.2009.74.015 PubMedCrossRefGoogle Scholar
  17. Chee PW, Paterson AH, Udall JA, Wendel JF (2016) Interspecific hybridization for upland cotton improvement. In: Mason AS (ed) Polyploidy and hybridization for crop improvement. CRC Press, Boca Raton, pp 1–26Google Scholar
  18. Clark RM, Linton E, Messing J, Doebley JF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci USA 101:700–707. doi: 10.1073/pnas.2237049100 PubMedCrossRefGoogle Scholar
  19. Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950. doi: 10.1038/nrg2482 PubMedCrossRefGoogle Scholar
  20. Corbett-Detig RB, Hartl DL, Sackton TB (2015) Natural selection constrains neutral diversity across a wide range of species. PLoS Biol 13:e1002112. doi: 10.1371/journal.pbio.1002112 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Core Team R (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  22. Cutter AD, Moses AM (2011) Polymorphism, divergence, and the role of recombination in Saccharomyces cerevisiae genome evolution. Molec Biol Evol 28:1745–1754. doi: 10.1093/molbev/msq356 PubMedCrossRefGoogle Scholar
  23. Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14:262–274. doi: 10.1038/nrg3425 PubMedPubMedCentralCrossRefGoogle Scholar
  24. d’Eeckenbrugge GC, Lacape J-M (2014) Distribution and differentiation of wild, feral, and cultivated populations of perennial upland cotton (Gossypium hirsutum L.) in Mesoamerica and the Caribbean. PLoS ONE 9:e107458. doi: 10.1371/journal.pone.0107458 CrossRefGoogle Scholar
  25. Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321. doi: 10.1016/j.cell.2006.12.006 PubMedCrossRefGoogle Scholar
  26. Durand EY, Patterson N, Reich D, Slatkin M (2011) Testing for ancient admixture between closely related populations. Molec Biol Evol 28:2239–2252. doi: 10.1093/molbev/msr048 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ellegren H, Galtier N (2016) Determinants of genetic diversity. Nat Rev Genet 17:422–433. doi: 10.1038/nrg.2016.58 PubMedCrossRefGoogle Scholar
  28. Fang DD, Hinze LL, Percy RG, Li P, Deng D, Thyssen G (2013) A microsatellite-based genome-wide analysis of genetic diversity and linkage disequilibrium in upland cotton (Gossypium hirsutum L.) cultivars from major cotton-growing countries. Euphytica 191:391–401. doi: 10.1007/s10681-013-0886-2 CrossRefGoogle Scholar
  29. Fishman L, Willis JH (2005) A novel meiotic drive locus almost completely distorts segregation in Mimulus (monkeyflower) hybrids. Genetics 169:347–353. doi: 10.1534/genetics.104.032789 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186:184–193. doi: 10.1111/j.1469-8137.2009.03107.x PubMedCrossRefGoogle Scholar
  31. Flagel LE, Wendel J, Udall J (2012) Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton. BMC Genom 13:302. doi: 10.1186/1471-2164-13-302 CrossRefGoogle Scholar
  32. Force A, Lynch M, Pickett FB, Amores A, Y-l Yan, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedPubMedCentralGoogle Scholar
  33. Fryxell PA (1978) The natural history of the cotton tribe (Malvaceae, tribe Gossypieae). Texas A & M University Press, College StationGoogle Scholar
  34. Fryxell PA (1992) A revised taxonomic interpretation of Gossypium L. (Malvaceae). Rheedea 2:108–165Google Scholar
  35. Gaeta RT, Pires JC (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:18–28. doi: 10.1111/j.1469-8137.2009.03089.x PubMedCrossRefGoogle Scholar
  36. Gaut BS, Muse SV, Clark WD, Clegg MT (1992) Relative rates of nucleotide substitution at the rbcL locus of monocotyledonous plants. J Molec Evol 35:292–303. doi: 10.1007/bf00161167 PubMedCrossRefGoogle Scholar
  37. Gaut B, Yang L, Takuno S, Eguiarte LE (2011) The patterns and causes of variation in plant nucleotide substitution rates. Annual Rev Ecol Evol Syst 42:245–266. doi: 10.1146/annurev-ecolsys-102710-145119 CrossRefGoogle Scholar
  38. Gill BS (1991) Nucleo-cytoplasmic interaction (NCI) hypothesis of genome evolution and speciation in polyploid plants. In: Sasakuma T and Kinoshita T (eds) Proceedings of the Dr. H. Kihara memorial international symposium on cytoplasmic engineering in wheat. Kihara Memorial Yokohama Foundation for the Advancement of Life Science, Yokohama, pp 48–53Google Scholar
  39. Gill BS, Friebe B (2013) Nucleocytoplasmic interaction hypothesis of genome evolution and speciation in polyploid plants revisited: polyploid species-specific chromosomal polymorphisms in wheat. In: Chen ZJ, Birchler JA (eds) Polyploid and hybrid genomics. Wiley, Oxford, pp 213–221. doi: 10.1002/9781118552872.ch13 CrossRefGoogle Scholar
  40. Glémin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc Roy Soc London, Ser B, Biol Sci 273:3011–3019. doi: 10.1098/rspb.2006.3657 CrossRefGoogle Scholar
  41. Gong L, Salmon A, Yoo M-J, Grupp KK, Wang Z, Paterson AH, Wendel JF (2012) The cytonuclear dimension of allopolyploid evolution: An example from cotton using rubisco. Molec Biol Evol 29:3023–3036. doi: 10.1093/molbev/mss110 PubMedCrossRefGoogle Scholar
  42. Gong L, Olson M, Wendel JF (2014) Cytonuclear evolution of rubisco in four allopolyploid lineages. Molec Biol Evol 31:2624–2636. doi: 10.1093/molbev/msu207 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gossmann TI, Woolfit M, Eyre-Walker A (2011) Quantifying the variation in the effective population size within a genome. Genetics 189:1389–1402. doi: 10.1534/genetics.111.132654 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Grover CE, Kim H, Wing RA, Paterson AH, Wendel JF (2007) Microcolinearity and genome evolution in the AdhA region of diploid and polyploid cotton (Gossypium). Pl J 50:995–1006. doi: 10.1111/j.1365-313X.2007.03102.x CrossRefGoogle Scholar
  45. Grover CE, Grupp KK, Wanzek RJ, Wendel JF (2012) Assessing the monophyly of polyploid Gossypium species. Pl Syst Evol 298:1177–1183. doi: 10.1007/s00606-012-0615-7 CrossRefGoogle Scholar
  46. Grover CE, Gallagher JP, Jareczek JJ, Page JT, Udall JA, Gore MA, Wendel JF (2015) Re-evaluating the phylogeny of allopolyploid Gossypium L. Molec Phylogen Evol 92:45–52. doi: 10.1016/j.ympev.2015.05.023 CrossRefGoogle Scholar
  47. Guo X-H, Bi Z-G, Wu B-H, Wang Z-Z, Hu J-L, Zheng Y-L, Liu D-C (2013) Chay/bx, a novel chimeric high-molecular-weight glutenin subunit gene apparently created by homoeologous recombination in Triticum turgidum ssp. dicoccoides. Gene 531:318–325. doi: 10.1016/j.gene.2013.08.073 PubMedCrossRefGoogle Scholar
  48. Guo H, Wang X, Gundlach H, Mayer KF, Peterson DG, Scheffler BE, Chee PW, Paterson AH (2014) Extensive and biased intergenomic nonreciprocal DNA exchanges shaped a nascent polyploid genome, Gossypium (cotton). Genetics 197:1153–1163. doi: 10.1534/genetics.114.166124 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hendrix B, Stewart JM (2005) Estimation of the nuclear DNA content of Gossypium species. Ann Bot (Oxford) 95:789–797. doi: 10.1093/aob/mci078 CrossRefGoogle Scholar
  50. Hinze LL, Fang DD, Gore MA, Scheffler BE, John ZY, Frelichowski J, Percy RG (2015) Molecular characterization of the Gossypium diversity reference set of the US national cotton germplasm collection. Theor Appl Genet 128:313–327. doi: 10.1007/s00122-014-2431-7 PubMedCrossRefGoogle Scholar
  51. Hinze LL, Gazave E, Gore MA, Fang DD, Scheffler BE, Yu JZ, Jones DC, Frelichowski J, Percy RG (2016) Genetic diversity of the two commercial tetraploid cotton species in the Gossypium diversity reference set. J Heredity 107:274–286. doi: 10.1093/jhered/esw004 CrossRefGoogle Scholar
  52. Hough J, Williamson RJ, Wright SI (2013) Patterns of selection in plant genomes. Annual Rev Ecol Evol Syst 44:31–49. doi: 10.1146/annurev-ecolsys-110512-135851 CrossRefGoogle Scholar
  53. Hu G, Houston NL, Pathak D, Schmidt L, Thelen JJ, Wendel JF (2011) Genomically biased accumulation of seed storage proteins in allopolyploid cotton. Genetics 189:1103–1115. doi: 10.1534/genetics.111.132407 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hufford MB, Xu X, Van Heerwaarden J, Pyhäjärvi T, Chia J-M, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811. doi: 10.1038/ng.2309 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Huynh LY, Maney DL, Thomas JW (2010) Contrasting population genetic patterns within the white-throated sparrow genome (Zonotrichia albicollis). BMC Genet 11:1. doi: 10.1186/1471-2156-11-96 CrossRefGoogle Scholar
  56. Ji X, Griffing A, Thorne JL (2016) A phylogenetic approach finds abundant interlocus gene conversion in yeast. Molec Biol Evol 33:2469–2476. doi: 10.1093/molbev/msw114 PubMedCrossRefGoogle Scholar
  57. Jiang C-X, Wright RJ, El-Zik KM, Paterson AH (1998) Polyploid formation created unique avenues for response to selection in Gossypium (cotton). Proc Natl Acad Sci USA 95:4419–4424PubMedPubMedCentralCrossRefGoogle Scholar
  58. Jiang C-X, Chee PW, Draye X, Morrell PL, Smith CW, Paterson AH (2000) Multilocus interactions restrict gene introgression in interspecific populations of polyploid Gossypium (cotton). Evolution 54:798–814PubMedCrossRefGoogle Scholar
  59. Korneliussen TS, Albrechtsen A, Nielsen R (2014) Angsd: analysis of next generation sequencing data. BMC Bioinform 15:1–13. doi: 10.1186/s12859-014-0356-4 CrossRefGoogle Scholar
  60. Krapovickas A, Seijo G (2008) Gossypium ekmanianum (Malvaceae), algodón silvestre de la república dominicana. Bonplandia 17:55–63Google Scholar
  61. Kubo T, Yoshimura A (2005) Epistasis underlying female sterility detected in hybrid breakdown in a japonica–indica cross of rice (Oryza sativa L.). Theor Appl Genet 110:346–355. doi: 10.1007/s00122-004-1846-y PubMedCrossRefGoogle Scholar
  62. Lacape J-M, Dessauw D, Rajab M, Noyer J-L, Hau B (2007) Microsatellite diversity in tetraploid Gossypium germplasm: assembling a highly informative genotyping set of cotton SSRs. Molec Breed 19:45–58. doi: 10.1007/s11032-006-9042-1 CrossRefGoogle Scholar
  63. Lange C, Zerulla K, Breuert S, Soppa J (2011) Gene conversion results in the equalization of genome copies in the polyploid haloarchaeon Haloferax volcanii. Molec Microbiol 80:666–677. doi: 10.1111/j.1365-2958.2011.07600.x CrossRefGoogle Scholar
  64. Lashermes P, Combes MC, Hueber Y, Severac D, Dereeper A (2014) Genome rearrangements derived from homoeologous recombination following allopolyploidy speciation in coffee. Pl J 78:674–685. doi: 10.1111/tpj.12505 CrossRefGoogle Scholar
  65. Lashermes P, Hueber Y, Combes M-C, Severac D, Dereeper A (2016) Inter-genomic DNA exchanges and homoeologous gene silencing shaped the nascent allopolyploid coffee genome (Coffea arabica L.). Genes Genomes Genet 6:2937–2948. doi: 10.1534/g3.116.030858 Google Scholar
  66. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Ségurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10:e1001388. doi: 10.1371/journal.pbio.1001388 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Li Z, Pinson SR, Paterson AH, Park WD, Stansel JW (1997) Genetics of hybrid sterility and hybrid breakdown in an intersubspecific rice (Oryza sativa L.) population. Genetics 145:1139–1148PubMedPubMedCentralGoogle Scholar
  68. Li F, Fan G, Lu C, Xiao G, Zou C, Kohel RJ, Ma Z, Shang H, Ma X, Wu J, Liang X, Huang G, Percy RG, Liu K, Yang W, Chen W, Du X, Shi C, Yuan Y, Ye W, Liu X, Zhang X, Liu W, Wei H, Wei S, Huang G, Zhang X, Zhu S, Zhang H, Sun F, Wang X, Liang J, Wang J, He Q, Huang L, Wang J, Cui J, Song G, Wang K, Xu X, Yu JZ, Zhu Y, Yu S (2015) Genome sequence of cultivated upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530. doi: 10.1038/nbt.3208 PubMedCrossRefGoogle Scholar
  69. Martin NH, Bouck AC, Arnold ML (2005) Loci affecting long-term hybrid survivorship in Louisiana irises: implications for reproductive isolation and introgression. Evolution 59:2116–2124PubMedCrossRefGoogle Scholar
  70. Martin SH, Davey JW, Jiggins CD (2014) Evaluating the use of abba–baba statistics to locate introgressed loci. Molec Biol Evol 32:244–257. doi: 10.1093/molbev/msu269 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Matyasek R, Lim KY, Kovarik A, Leitch AR (2003) Ribosomal DNA evolution and gene conversion in Nicotiana rustica. Heredity 91:268–275. doi: 10.1038/sj.hdy.6800333 PubMedCrossRefGoogle Scholar
  72. Melissa DL-S, Uygun S, Moghe G, Panchy N, Fang L, David EH, Hannah LJ, Feig M, Shiu S-H (2015) Molecular evidence for functional divergence and decay of a transcription factor derived from whole genome duplication in Arabidopsis thaliana. Pl Physiol 168:1717–1734. doi: 10.1104/pp.15.00689 CrossRefGoogle Scholar
  73. Moyle LC, Graham EB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169:355–373. doi: 10.1534/genetics.104.029546 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Nei M, Li W-H (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ness RW, Wright SI, Barrett SC (2010) Mating-system variation, demographic history and patterns of nucleotide diversity in the tristylous plant Eichhornia paniculata. Genetics 184:381–392. doi: 10.1534/genetics.109.110130 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196. doi: 10.1371/journal.pbio.0030196 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ohno S (1970) Evolution by gene duplication. Springer, BerlinCrossRefGoogle Scholar
  78. Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan MD (2006) Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173:975–983. doi: 10.1534/genetics.106.056473 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Olson MS, Robertson AL, Takebayashi N, Silim S, Schroeder WR, Tiffin P (2010) Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). New Phytol 186:526–536. doi: 10.1111/j.1469-8137.2009.03174.x PubMedCrossRefGoogle Scholar
  80. 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. doi: 10.1126/science.1180677 PubMedCrossRefGoogle Scholar
  81. Page JT, Gingle AR, Udall JA (2013a) PolyCat: a resource for genome categorization of sequencing reads from allopolyploid organisms. Genes Genomes Genet 3:517–525. doi: 10.1534/g3.112.005298 Google Scholar
  82. Page JT, Huynh MD, Liechty ZS, Grupp KK, Stelly D, Hulse AM, Ashrafi H, Van Deynze A, Wendel JF, Udall JA (2013b) Insights into the evolution of cotton diploids and polyploids from whole-genome re-sequencing. Genes Genomes Genet 3:1809–1818. doi: 10.1534/g3.113.007229 Google Scholar
  83. Page JT, Liechty ZS, Alexander RH, Clemons K, Hulse-Kemp AM, Ashrafi H, Van Deynze A, Stelly DM, Udall JA (2016) DNA sequence evolution and rare homoeologous conversion in tetraploid cotton. PLoS Genet 12:e1006012. doi: 10.1371/journal.pgen.1006012 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Paradis E (2010) Pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26:419–420. doi: 10.1093/bioinformatics/btp696 PubMedCrossRefGoogle Scholar
  85. Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. doi: 10.1093/bioinformatics/btg412 PubMedCrossRefGoogle Scholar
  86. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall JA, Yoo M-J, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover CE, Grupp KK, Hu G, Lee T-H, Li J, Lin L, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, Tan X, Tang H, Xu C, Wang J, Wang Z, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers JE, Brubaker CL, Chee PW, Das S, Gingle AR, Haigler CH, Harker D, Hoffmann LV, Hovav R, Jones DC, Lemke C, Mansoor S, Rahman MU, Rainville LN, Rambani A, Reddy UK, Rong J-K, Saranga Y, Scheffler BE, Scheffler JA, Stelly DM, Triplett BA, Van Deynze A, Vaslin MFS, Waghmare VN, Walford SA, Wright RJ, Zaki EA, Zhang T, Dennis ES, Mayer KFX, Peterson DG, Rokhsar DS, Wang X, Schmutz J (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427. doi: 10.1038/nature11798 PubMedCrossRefGoogle Scholar
  87. Percy RG (2009) The worldwide gene pool of Gossypium barbadense L. and its improvement. In: Paterson AH (ed) Genetics and genomics of cotton. Springer, New York, pp 53–68CrossRefGoogle Scholar
  88. Percy R, Wendel JF (1990) Allozyme evidence for the origin and diversification of Gossypium barbadense L. Theor Appl Genet 79:529–542PubMedCrossRefGoogle Scholar
  89. Pfeifer B, Wittelsbuerger U, Ramos-Onsins SE, Lercher MJ (2014) Popgenome: an efficient swiss army knife for population genomic analyses in R. Molec Biol Evol 31:1929–1936. doi: 10.1093/molbev/msu136 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Prathepha P (2009) The fragrance (fgr) gene in natural populations of wild rice (Oryza rufipogon Griff.). Genet Resources Crop Evol 56:13–18. doi: 10.1007/s10722-008-9337-7 CrossRefGoogle Scholar
  91. Reinisch AJ, Dong J-M, Brubaker CL, Stelly DM, Wendel JF, Paterson AH (1994) A detailed RFLP map of cotton, Gossypium hirsutum x Gossypium barbadense: chromosome organization and evolution in a disomic polyploid genome. Genetics 138:829–847PubMedPubMedCentralGoogle Scholar
  92. Renny-Byfield S, Page JT, Udall JA, Sanders WS, Peterson DG, Arick MA, Grover CE, Wendel JF (2016) Independent domestication of two old world cotton species. Genome Biol Evol 8:1940–1947. doi: 10.1093/gbe/evw129 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Rhyne CL (1958) Linkage studies in Gossypium. I. Altered recombination in allotetraploid G. hirsutum L. Following linkage group transference from related diploid species. Genetics 43:822PubMedPubMedCentralGoogle Scholar
  94. Rieseberg LH and Wendel JF (1993) Introgression and its consequences in plants. Oxford University Press, New York and OxfordGoogle Scholar
  95. Rong J, Abbey C, Bowers JE, Brubaker CL, Chang C, Chee PW, Delmonte TA, Ding X, Garza JJ, Marler BS (2004) A 3347-locus genetic recombination map of sequence-tagged sites reveals features of genome organization, transmission and evolution of cotton (Gossypium). Genetics 166:389–417PubMedPubMedCentralCrossRefGoogle Scholar
  96. Roselius K, Stephan W, Städler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763. doi: 10.1534/genetics.105.043877 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA (2013) The fate of duplicated genes in a polyploid plant genome. Pl J 73:143–153. doi: 10.1111/tpj.12026 CrossRefGoogle Scholar
  98. Rungis D, Llewellyn D, Dennis E, Lyon B (2005) Simple sequence repeat (SSR) markers reveal low levels of polymorphism between cotton (Gossypium hirsutum L.) cultivars. Crop Pasture Sci 56:301–307. doi: 10.1071/AR04190 CrossRefGoogle Scholar
  99. Saha S, Jenkins JN, Wu J, McCarty JC, Gutiérrez OA, Percy RG, Cantrell RG, Stelly DM (2006) Effects of chromosome-specific introgression in upland cotton on fiber and agronomic traits. Genetics 172:1927–1938. doi: 10.1534/genetics.105.053371 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Salmon A, Flagel L, Ying B, Udall JA, Wendel JF (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186:123–134. doi: 10.1111/j.1469-8137.2009.03093.x PubMedCrossRefGoogle Scholar
  101. Salmon A, Udall JA, Jeddeloh JA, Wendel JF (2012) Targeted capture of homoeologous coding and noncoding sequence in polyploid cotton. Genes Genomes Genet 2:921–930. doi: 10.1534/g3.112.003392 Google Scholar
  102. Schmid KJ, Ramos-Onsins S, Ringys-Beckstein H, Weisshaar B, Mitchell-Olds T (2005) A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics 169:1601–1615. doi: 10.1371/journal.pone.0144339 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Sehrish T, Symonds VV, Soltis DE, Soltis PS, Tate JA (2015) Cytonuclear coordination is not immediate upon allopolyploid formation in Tragopogon miscellus (Asteraceae) allopolyploids. PLoS ONE 10:e0144339. doi: 10.1371/journal.pone.0144339 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Sella G, Petrov DA, Przeworski M, Andolfatto P (2009) Pervasive natural selection in the Drosophila genome? PLoS Genet 5:e1000495PubMedPubMedCentralCrossRefGoogle Scholar
  105. Senchina DS, Alvarez I, Cronn RC, Liu B, Rong J, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Molec Biol Evol 20:633–643. doi: 10.1093/molbev/msg065 PubMedCrossRefGoogle Scholar
  106. Slotte T (2014) The impact of linked selection on plant genomic variation. Brief Funct Genom 13:268–275. doi: 10.1093/bfgp/elu009 CrossRefGoogle Scholar
  107. Small RL, Ryburn JA, Cronn RC, Seelanan T, Wendel JF (1998) The tortoise and the hare: choosing between noncoding plastome and nuclear adh sequences for phylogeny reconstruction in a recently diverged plant group. Amer J Bot 85:1301–1315CrossRefGoogle Scholar
  108. Small RL, Ryburn JA, Wendel JF (1999) Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Molec Biol Evol 16:491–501PubMedCrossRefGoogle Scholar
  109. Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89. doi: 10.1126/science.1163197 PubMedCrossRefGoogle Scholar
  110. Song B-H, Windsor AJ, Schmid KJ, Ramos-Onsins S, Schranz ME, Heidel AJ, Mitchell-Olds T (2009) Multilocus patterns of nucleotide diversity, population structure and linkage disequilibrium in Boechera stricta, a wild relative of Arabidopsis. Genetics 181:1021–1033. doi: 10.1534/genetics.108.095364 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Stephens S (1949) The cytogenetics of speciation in Gossypium. I. Selective elimination of the donor parent genotype in interspecific backcrosses. Genetics 34:627PubMedCentralGoogle Scholar
  112. Stephens S (1951) Possible significance of duplication in evolution. Advances Genet 4:247–265Google Scholar
  113. Stephens S (1967) Evolution under domestication of the new world cottons (Gossypium spp.). Ci & Cult 19:118–134Google Scholar
  114. Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR (2007) Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3:e133. doi: 10.1371/journal.pgen.0030133 PubMedPubMedCentralCrossRefGoogle Scholar
  115. Takuno S, Ran J-H, Gaut BS (2016) Evolutionary patterns of genic DNA methylation vary across land plants. Nat Pl 2:15222. doi: 10.1038/nplants.2015.222 Google Scholar
  116. Tatineni V, Cantrell R, Davis D (1996) Genetic diversity in elite cotton germplasm determined by morphological characteristics and RAPDs. Crop Sci 36:186–192CrossRefGoogle Scholar
  117. Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313. doi: 10.1093/gbe/evu261 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Tyagi P, Gore MA, Bowman DT, Campbell BT, Udall JA, Kuraparthy V (2014) Genetic diversity and population structure in the us upland cotton (Gossypium hirsutum L.). Theor Appl Genet 127:283–295. doi: 10.1007/s00122-013-2217-3 PubMedCrossRefGoogle Scholar
  119. Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L. Genetics 169:967–979. doi: 10.1534/genetics.104.033209 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Udall JA, Swanson JM, Haller K, Rapp RA, Sparks ME, Hatfield J, Yu Y, Wu Y, Dowd C, Arpat AB, Sickler BA, Wilkins TA, Guo JY, Chen XY, Scheffler J, Taliercio E, Turley R, McFadden H, Payton P, Klueva N, Allen R, Zhang D, Haigler C, Wilkerson C, Suo J, Schulze SR, Pierce ML, Essenberg M, Kim H, Llewellyn DJ, Dennis ES, Kudrna D, Wing R, Paterson AH, Soderlund C, Wendel JF (2006a) A global assembly of cotton ESTs. Genome Res 16:441–450. doi: 10.1101/gr.4602906 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Udall JA, Swanson JM, Nettleton D, Percifield RJ, Wendel JF (2006b) A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173:1823–1827. doi: 10.1534/genetics.106.058271 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Udall JA, Flagel LE, Cheung F, Woodward AW, Hovav R, Rapp RA, Swanson JM, Lee JJ, Gingle AR, Nettleton D, Town CD, Chen ZJ, Wendel JF (2007) Spotted cotton oligonucleotide microarrays for gene expression analysis. BMC Genom 8:81. doi: 10.1186/1471-2164-8-81 CrossRefGoogle Scholar
  123. Van Deynze A, Stoffel K, Lee M, Wilkins TA, Kozik A, Cantrell RG, John ZY, Kohel RJ, Stelly DM (2009) Sampling nucleotide diversity in cotton. BMC Pl Biol 9:1. doi: 10.1186/1471-2229-9-125 CrossRefGoogle Scholar
  124. Waghmare VN, Rong J, Rogers CJ, Bowers JE, Chee PW, Gannaway JR, Katageri I, Paterson AH (2016) Comparative transmission genetics of introgressed chromatin in Gossypium (cotton) polyploids. Amer J Bot 103:719–729. doi: 10.3732/ajb.1500266 CrossRefGoogle Scholar
  125. Wang G-L, Dong J-M, Paterson A (1995) The distribution of Gossypium hirsutum chromatin in G. barbadense germ plasm: molecular analysis of introgressive plant breeding. Theor Appl Genet 91:1153–1161. doi: 10.1007/BF00223934 PubMedCrossRefGoogle Scholar
  126. Wang F, Gong Y, Zhang C, Liu G, Wang L, Xu Z, Zhang J (2011) Genetic effects of introgression genomic components from sea island cotton (Gossypium barbadense L.) on fiber related traits in upland cotton (G. hirsutum L.). Euphytica 181:41–53. doi: 10.1007/s10681-011-0378-1 CrossRefGoogle Scholar
  127. Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, Cong L, Shang H, Zhu S, Zou C, Li Q, Yuan Y, Lu C, Wei H, Gou C, Zheng Z, Yin Y, Zhang X, Liu K, Bo Wang, Song C, Shi N, Kohel RJ, Percy RG, Yu JZ, Zhu Y-X, Wang J, Yu S (2012) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44:1098–1103PubMedCrossRefGoogle Scholar
  128. Wang J, Guo H, Jin D, Wang X, Paterson AH (2015) Comparative analysis of gene conversion between duplicated regions in Brassica rapa and B. oleracea genomes. In: Wang X, Kole C (eds) The Brassica rapa genome. Springer, Berlin and Heidelberg, pp 121–129Google Scholar
  129. Wang J, Street NR, Scofield DG, Ingvarsson PK (2016) Natural selection and recombination rate variation shape nucleotide polymorphism across the genomes of three related Populus species. Genetics 202:1185–1200. doi: 10.1534/genetics.115.183152 PubMedCrossRefGoogle Scholar
  130. Wendel JF, Albert VA (1992) Phylogenetics of the cotton genus (Gossypium): character-state weighted parsimony analysis of chloroplast-DNA restriction site data and its systematic and biogeographic implications. Syst Bot 17:115–143CrossRefGoogle Scholar
  131. Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Advances Agron 78:139–186CrossRefGoogle Scholar
  132. Wendel JF, Grover CE (2015) Taxonomy and evolution of the cotton genus, Gossypium. In: Fang D, Percy RG (eds) Cotton. ASA-CSSA-SSSA, Madison, pp 25–44Google Scholar
  133. Wendel JF, Brubaker CL, Percival AE (1992) Genetic diversity in Gossypium hirsutum and the origin of upland cotton. Amer J Bot 79:1291–1310CrossRefGoogle Scholar
  134. Wendel JF, Brubaker CL, Seelanan T (2010) The origin and evolution of Gossypium. In: Stewart JM, Oosterhuis DM, Heitholt JJ, Mauney JR (eds) Physiology of cotton. Springer, Dordrecht, pp 1–18Google Scholar
  135. Westengen OT, Huamán Z, Heun M (2005) Genetic diversity and geographic pattern in early South American cotton domestication. Theor Appl Genet 110:392–402. doi: 10.1007/s00122-004-1850-2 PubMedCrossRefGoogle Scholar
  136. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  137. Wolfe KH, Sharp PM, Li W-H (1989) Rates of synonymous substitution in plant nuclear genes. J Molec Evol 29:208–211CrossRefGoogle Scholar
  138. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artificial selection on the maize genome. Science 308:1310–1314. doi: 10.1126/science.1107891 PubMedCrossRefGoogle Scholar
  139. Wright SI, Foxe JP, DeRose-Wilson L, Kawabe A, Looseley M, Gaut BS, Charlesworth D (2006) Testing for effects of recombination rate on nucleotide diversity in natural populations of Arabidopsis lyrata. Genetics 174:1421–1430. doi: 10.1534/genetics.106.062588 PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wu TD, Nacu S (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873–881. doi: 10.1093/bioinformatics/btq057 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Yin T, Cook D, Lawrence M (2012) ggbio: an R package for extending the grammar of graphics for genomic data. Genome Biol 13:R77. doi: 10.1186/gb-2012-13-8-r77 PubMedPubMedCentralCrossRefGoogle Scholar
  142. Zhang J, Percy RG, McCarty JC (2014) Introgression genetics and breeding between Upland and Pima cotton: a review. Euphytica 198:1–12CrossRefGoogle Scholar
  143. Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537. doi: 10.1038/nbt.3207 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  • Corrinne E. Grover
    • 1
  • Joseph P. Gallagher
    • 1
  • Emmanuel P. Szadkowski
    • 2
  • Justin T. Page
    • 3
  • Michael A. Gore
    • 4
  • Joshua A. Udall
    • 3
  • Jonathan F. Wendel
    • 1
  1. 1.Iowa State UniversityAmesUSA
  2. 2.INRA UR1052 GAFLAvignonFrance
  3. 3.Brigham Young UniversityProvoUSA
  4. 4.Plant Breeding and Genetics Section, School of Integrative Plant ScienceCornell UniversityIthacaUSA

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