Abstract
The origin and monophyly of the polyploid cotton (Gossypium) species has been largely accepted, despite the lack of explicit phylogenetic evidence. Recent studies in other polyploid systems have demonstrated that multiple origins for polyploid species are much more common than once thought, raising the possibility that Gossypium polyploids also had multiple origins, as postulated by some authors. To test the monophyly of polyploid cotton, we sequenced a 2.8-kb intergenic region from all diploid species belonging to the genome groups from which the polyploid originates. The resulting phylogenetic analyses strongly support a single origin of polyploid cotton involving a D-genome ancestor related to Gossypium raimondii and an A-genome ancestor that was sister to both extant A-genome species.
References
Adams KL, Wendel JF (2005) Novel patterns of gene expression in polyploid plants. Trends Genet 21(10):539–543
Adams KL, Wendel J (2006) Allele-specific, bi-directional silencing of an alcohol dehydrogenase gene in different organs of interspecific cotton hybrids. Genetics 17:2139–2142
Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100(8):4649–4654
Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168(4):2217–2226
Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20(3):407–415
Alvarez I, Cronn R, Wendel JF (2005) Phylogeny of the New World diploid cottons (Gossypium L., Malvaceae) based on sequences of three low-copy nuclear genes. Plant Syst Evol 252(3–4):199–214
Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF (2009a) Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182(2):503–517
Chaudhary B, Hovav R, Flagel L, Mittler R, Wendel JF (2009b) Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium). BMC Genomics 10:378
Cronn RC, Zhao X, Paterson AH, Wendel JF (1996) Polymorphism and concerted evolution in a tandemly repeated gene family: 5S ribosomal DNA in diploid and allopolyploid cottons. J Mol Evol 42(6):685–705
Cronn R, Small RL, Haselkorn T, Wendel JF (2003) Cryptic repeated genomic recombination during speciation in Gossypium gossypioides. Evolution 57(11):2475–2489
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi:10.1093/nar/gkh340
Endrizzi JE, Turcotte EL, Kohel RJ (1985) Genetics, cytology, and evolution of Gossypium. In: Caspari EW, John GS (eds) Advances in genetics, vol 23. Academic, London, pp 271–375
Flagel LE, Chen L, Chaudhary B, Wendel JF (2009) Coordinated and fine-scale control of homoeologous gene expression in allotetraploid cotton. J Hered 100(4):487–490 (pii: esp003)
Fryxell PA (1979) The natural history of the cotton tribe (Malvaceae, tribe Gossypieae), 1st edn. Texas A&M University Press, College Station
Grover CE, Kim H, Wing RA, Paterson AH, Wendel JF (2004) Incongruent patterns of local and global genome size evolution in cotton. Genome Res 14(8):1474–1482. doi:10.1101/gr.2673204
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). Plant J 50(6):995–1006
Grover CE, Yu Y, Wing RA, Paterson AH, Wendel JF (2008) A phylogenetic analysis of indel dynamics in the cotton genus. Mol Biol Evol 25(7):1415–1428
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704
Hall T (2007) BioEdit: biological sequence alignment editor written for Windows 95/98/NT/2000/XP. http://www.mbio.ncsu.edu/bioedit/bioedit.html
Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16(10):1252–1261
Hawkins JS, Hu G, Rapp RA, Grafenberg JL, Wendel JF (2008) Phylogenetic determination of the pace of transposable element proliferation in plants: copia and LINE-like elements in Gossypium. Genome 51(1):11–18
Hovav R, Chaudhary B, Udall JA, Flagel L, Wendel JF (2008) Parallel domestication, convergent evolution and duplicated gene recruitment in allopolyploid cotton. Genetics 179(3):1725–1733
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97–100
Johnson BL (1975) Gossypium palmeri and a Polyphyletic Origin of New World Cottons. Bull Torrey Bot Club 102(6):340–349
McDade L (1990) Hybrids and phylogenetic systematics I. patterns of character expression in hybrids and their implications for cladistic analysis. Evolution 44(6):1685–1700
McDade L (1995) Hybridization and phylogenetics. In: Hoch PC, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, Missouri
Parks CR, Ezell WL, Williams DE, Dreyer DL (1975) The application of flavonoid distribution to taxonomic problems in the genus Gossypium. Bull Torrey Bot Club 102(6):350–361
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256
Rapp R, Udall J, Wendel J (2009) Genomic expression dominance in allopolyploids. BMC Biol 7(1):18
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574
Salmon A, Flagel L, Ying B, Udall JA, Wendel JF (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186(1):123–134. doi:10.1111/j.1469-8137.2009.03093.x
Small RL, Wendel JF (1999) The mitochondrial genome of allotetraploid cotton (Gossypium L.). J Hered 90:251–253
Small RL, Wendel JF (2002) Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol Biol Evol 19(5):597–607
Soltis D, Soltis P (1993) Molecular data facilitate a reevaluation of traditional tenets of polyploid evolution. Crit Rev Plant Sci 12:243
Soltis D, Soltis P (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348
Soltis DE, Soltis PS, Tate JA (2004) Advances in the study of polyploidy since plant speciation. New Phytol 161(1):173–191. doi:10.1046/j.1469-8137.2003.00948.x
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, dePamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96(1):336–348
Tate J, Ni Z, Scheen A, Koh J, Gilbert C (2006) Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2:Unit 2.3. doi:10.1002/0471250953.bi0203s00
Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci 86(11):4132–4136
Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. In: Advances in agronomy, vol 78. Academic Press, London, pp 139–186
Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci 92(1):280–284
Wendel JF, Brubaker CL, Seelanan T (2010) The origin and evolution of Gossypium. In: Stewart JM, Oosterhuis DM, Heitholt JJ (eds) Physiology of cotton. Springer, Dordrecht, pp 1–18
Wilgenbusch JC, Swofford D (2003) Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics Chapter 6: Unit 6.4
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Grover, C.E., Grupp, K.K., Wanzek, R.J. et al. Assessing the monophyly of polyploid Gossypium species. Plant Syst Evol 298, 1177–1183 (2012). https://doi.org/10.1007/s00606-012-0615-7
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DOI: https://doi.org/10.1007/s00606-012-0615-7