Polyploid formation created unique avenues for response to selection in Gossypium (cotton) (quantitative variationycotton fiber qualityycrop evolutionyintergenomic interactionsycomparative quantitative trait locus analysis)

A detailed restriction fragment length polymorphism map was used to determine the chromosomal locations and subgenomic distributions of quantitative trait loci (QTLs) segregating in a cross between cultivars of allotetraploid (AADD) Gossypium hirsutum (‘‘Upland’’ cotton) and Gossypium barbadense (‘‘Sea Island,’’ ‘‘Pima,’’ or ‘‘Egyptian’’ cotton) that differ markedly in the quality and quantity of seed epidermal fibers. Most QTLs influencing fiber quality and yield are located on the ‘‘D’’ subgenome, derived from an ancestor that does not produce spinnable fibers. D subgenome QTLs may partly account for the fact that domestication and breeding of tetraploid cottons has resulted in fiber yield and quality levels superior to those achieved by parallel improvement of ‘‘A’’ genome diploid cottons. The merger of two genomes with different evolutionary histories in a common nucleus appears to offer unique avenues for phenotypic response to selection. This may partly compensate for reduction in quantitative variation associated with polyploid formation and be one basis for the prominence of polyploids among extant angiosperms. These findings impel molecular dissection of the roles of divergent subgenomes in quantitative inheritance in many other polyploids and further exploration of both ‘‘synthetic’’ polyploids and exotic diploid genotypes for agriculturally useful variation. Most angiosperm (flowering plant) genomes are thought to have incurred one or more polyploidization events (1, 2). Geneticists have long debated whether this simply reflects promiscuity of plants or whether a selective advantage is conferred by polyploid formation (3, 4). Among the beststudied polyploids are many of the world’s leading crops, including cotton, wheat, oat, soybean, peanut, canola, tobacco, coffee, and banana, each of which evolved by the joining of divergent genomes in a common nucleus (5). The evolution of the genus Gossypium (cotton) has included a very successful experiment in polyploid formation. World cotton commerce of about $20 billion annually is dominated by improved forms of two (among five extant) ‘‘AD’’ tetraploid (2n 5 4x 5 52) species, Gossypium hirsutum L. and Gossypium barbadense L. Tetraploid cottons are thought to have formed about 1–2 million years ago, in the New World, by hybridization between a maternal Old World ‘‘A’’ genome taxon resembling Gossypium herbaceum (2n 5 2x 5 26) and paternal New World ‘‘D’’ genome taxon resembling Gossypium raimondii (6) or Gossypium gossypioides (7) (both 2n 5 2x 5 26). The antiquity of this New World event precludes human involvement in polyploid formation. Wild A genome diploid and AD tetraploid Gossypium taxa produce spinnable fibers that were a likely impetus for domestication (8, 9). Domesticated tetraploid cottons existed in the New World by 3500–2300 B.C. (10) and have been widely distributed by humans throughout the world’s warmer latitudes. Domesticated A genome diploids existed in the Old World by 2700 B.C. (11), and one (of only two extant) species, Gossypium arboreum, remains intensively bred and cultivated in Asia. Its close relative and possible progenitor, the other extant A genome diploid species G. herbaceum also produces spinnable fiber. Although the seeds of D genome diploids are pubescent, none produce spinnable fibers (12). There is no evidence that domestication of D genome Gossypium taxa has ever been attempted, although their geographic distribution overlaps that of several wild tetraploids. No taxa from the other recognized diploid Gossypium genomes (B, C, E, F, and G) have been domesticated. Intense directional selection by humans has consistently produced AD tetraploid cottons that have superior yield andyor quality characteristics compared to the A genome diploid cultivars. Selective breeding of G. hirsutum (AADD) has emphasized maximum yield, whereas G. barbadense (AADD) is prized for its fibers of superior length, strength, and fineness. Side-by-side trials of 13 elite G. hirsutum genotypes and 21 G. arboreum diploids (AA) adapted to a common production region (India) show average seed cotton yield of 1,135 6 90 kgyha for the tetraploids, a 30% advantage over the 903 6 78 kgyha of the diploids, at similar quality levels (13). Such an equitable comparison cannot be made for G. barbadense and G. arboreum, because they are bred for adaptation to different production regions. However, the fiber of ‘‘extralong-staple’’ G. barbadense tetraploids, representing ;5% of the world’s cotton, commands a premium price due to ;40% higher fiber length ('35 mm), strength ('30 g per tex or more), and fineness over leading A genome cultivars (13), at similar yield levels. Obsolete G. barbadense cultivars reportedly had up to 100% longer fibers (50.8 mm; ref. 14) than modern G. arboreum (25.5 6 1.6 mm; ref. 13). To further investigate cotton fiber evolution, a detailed restriction fragment length polymorphism (RFLP) map (15) was used to determine the chromosomal locations and subgenomic (A versus D) distributions of quantitative trait loci (QTLs) segregating in a cross between a high-fiber-quality G. barbadense cultivar and a high-yielding G. hirsutum cultivar (both AADD). The D subgenome, from the non-fiberproducing ancestor, accounts for much more genetic variation in fiber traits of G. barbadense and G. hirsutum than does the A subgenome, from the fiber-producing ancestor. Lack of correspondence between QTLs in the A and D subgenomes, The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked ‘‘advertisement’’ in accordance with 18 U.S.C. §1734 solely to indicate this fact. © 1998 by The National Academy of Sciences 0027-8424y98y954419-6$2.00y0 PNAS is available online at http:yywww.pnas.org. Abbreviations: PV, phenotypic variance; PVE, phenotypic variance explained. QTL, quantitative trait locus; RFLP, restriction fragment length polymorphism; Ln,length by number; Lw, length by weight; SFCw, short fiber content by weight; CV, coefficient of variation; logSDCT, mass of cotton seed; LB, ratio of log(locule number) to log(boll number); lod, logarithm of odds; cM, centimorgan(s). ‡To whom reprint requests should be addressed.