Duplicated genes evolve independently after polyploid formation in cotton

Abstract

Of the many processes that generate gene duplications, polyploidy is unique in that entire genomes are duplicated. This process has been important in the evolution of many eukaryotic groups, and it occurs with high frequency in plants. Recent evidence suggests that polyploidization may be accompanied by rapid genomic changes, but the evolutionary fate of discrete loci recently doubled by polyploidy (homoeologues) has not been studied. Here we use locus-specific isolation techniques with comparative mapping to characterize the evolution of homoeologous loci in allopolyploid cotton (Gossypium hirsutum) and in species representing its diploid progenitors. We isolated and sequenced 16 loci from both genomes of the allopolyploid, from both progenitor diploid genomes and appropriate outgroups. Phylogenetic analysis of the resulting 73.5 kb of sequence data demonstrated that for all 16 loci (14.7 kb͞genome), the topology expected from organismal history was recovered. In contrast to observations involving repetitive DNAs in cotton, there was no evidence of interaction among duplicated genes in the allopolyploid. Polyploidy was not accompanied by an obvious increase in mutations indicative of pseudogene formation. Additionally, differences in rates of divergence among homoeologues in polyploids and orthologues in diploids were indistinguishable across loci, with significant rate deviation restricted to two putative pseudogenes. Our results indicate that most duplicated genes in allopolyploid cotton evolve independently of each other and at the same rate as those of their diploid progenitors. These indications of genic stasis accompanying polyploidization provide a sharp contrast to recent examples of rapid genomic evolution in allopolyploids.

A Microsatellite-Based, Gene-Rich Linkage Map Reveals Genome Structure, Function and Evolution in Gossypium

“…G. arboreum are Old World cultivated cotton species and G. hirsutum are New World cultivated cotton species, whereas G. raimondii is wild and cannot produce spinnable fiber. Studies have shown that the expression of duplicated genes in tetraploid species at the transcriptional level may have three fates: (1) silencing of one of the duplicated copies (Wendel 2000;Adams et al 2003); (2) molecular interactions mediated by concerted evolutionary processes leading to a rapid sequence conversion of homologous loci, homology-specific sequence elimination, and extensive genomic rearrangements (Wendel et al 1995;Adams et al 2003); or (3) independent evolution of the duplicated copies in allopolyploids (Cronn et al 1999;Small and Wendel 2000).…”

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

“…(58) Molecular phylogenetic analysis indicated that the orthologous genes in the progenitors evolve independently at relatively similar rates to the homoeologous loci that are combined in the allotetraploids. (59) Similarly, genomic changes in Spartina polyploids occur at a very low frequency. (60) The data suggest that, compared to Brassica and wheat, cotton and Spartina have a high-level of tolerance for genome doubling and interspecific hybridization.…”

Cryptic Repeated Genomic Recombination During Speciation in Gossypium Gossypioides

“…G1121 (0.73 kb), and G1262 (0.89 kb) Cronn et al 1999), partial alcohol dehydrogenase C sequences (AdhC ϭ 0.94 kb) (Small et al 1998;Small and Wendel 2000b), and two partial cellulose synthase genes (CesA1 ϭ 1.09 kb; CesA1b ϭ 1.18 kb). Amplification primers, cycling conditions, and sequencing methods follow previously detailed protocols (Small et al 1998;Small and Wendel 2000b;Liu et al 2001;Cronn et al 2002).…”