Dataset Information

Parallel and Intertwining Threads of Domestication in Allopolyploid Cotton.

ABSTRACT: The two cultivated allopolyploid cottons, Gossypium hirsutum and Gossypium barbadense, represent a remarkable example of parallel independent domestication, both involving dramatic morphological transformations under selection from wild perennial plants to annualized row crops. Deep resequencing of 643 newly sampled accessions spanning the wild-to-domesticated continuum of both species, and their allopolyploid relatives, are combined with existing data to resolve species relationships and elucidate multiple aspects of their parallel domestication. It is confirmed that wild G. hirsutum and G. barbadense were initially domesticated in the Yucatan Peninsula and NW South America, respectively, and subsequently spread under domestication over 4000-8000 years to encompass most of the American tropics. A robust phylogenomic analysis of infraspecific relationships in each species is presented, quantify genetic diversity in both, and describe genetic bottlenecks associated with domestication and subsequent diffusion. As these species became sympatric over the last several millennia, pervasive genome-wide bidirectional introgression occurred, often with striking asymmetries involving the two co-resident genomes of these allopolyploids. Diversity scans revealed genomic regions and genes unknowingly targeted during domestication and additional subgenomic asymmetries. These analyses provide a comprehensive depiction of the origin, divergence, and adaptation of cotton, and serve as a rich resource for cotton improvement.

SUBMITTER: Yuan D

PROVIDER: S-EPMC8132148 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Parallel and Intertwining Threads of Domestication in Allopolyploid Cotton.

Yuan Daojun D Grover Corrinne E CE Hu Guanjing G Pan Mengqiao M Miller Emma R ER Conover Justin L JL Hunt Spencer P SP Udall Joshua A JA Wendel Jonathan F JF

Advanced science (Weinheim, Baden-Wurttemberg, Germany) 20210315 10

The two cultivated allopolyploid cottons, <i>Gossypium hirsutum</i> and <i>Gossypium barbadense</i>, represent a remarkable example of parallel independent domestication, both involving dramatic morphological transformations under selection from wild perennial plants to annualized row crops. Deep resequencing of 643 newly sampled accessions spanning the wild-to-domesticated continuum of both species, and their allopolyploid relatives, are combined with existing data to resolve species relationsh ...[more]

PMID: 34026441

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Project description:Allopolyploidization is accompanied by changes in gene expression that are thought to contribute to phenotypic diversification. Here we describe global changes in the single-celled cotton fiber proteome of two natural allopolyploid species (Gossypium hirsutum and G. barbadense) and living models of their diploid parents using two different proteomic approaches. In total, 1323 two-dimensional gel electrophoresis spots and 1652 identified proteins by isobaric tags for relative and absolute quantitation were quantitatively profiled during fiber elongation. Between allopolyploids and their diploid A- and D-genome progenitors, amounts of differential expression ranged from 4.4 to 12.8%. Over 80% of the allopolyploid proteome was additively expressed with respect to progenitor diploids. Interestingly, the fiber proteome of G. hirsutum resembles the parental A-genome more closely, where long, spinable fiber first evolved, than does the fiber proteome of G. barbadense. More protein expression patterns were A-dominant than D-dominant in G. hirsutum, but in G. barbadense, the direction of expression-level dominance switched from the D-genome to the A-genome during fiber development. Comparison of developmental changes between the two allopolyploid species revealed a high level of proteomic differentiation despite their shared ancestry, relatively recent evolutionary divergence, and similar gross morphology. These results suggest that the two allopolyploid species have achieved superficially similar modern fiber phenotypes through different evolutionary routes at the proteome level. We also detected homeolog-specific expression for 1001 proteins and present a novel approach to infer the relationship between homeolog-specific and duplicate expression patterns. Our study provides a proteomic perspective on understanding evolutionary consequences of allopolyploidization, showing how protein expression has been altered by polyploidization and subsequently has diversified among species.

Project description:BackgroundModern allotetraploid cotton contains an "A" and "D" genome from an ancestral polyploidy event that occurred approximately 1-2 million years ago. Diploid A- and D-genome species can be compared to the A- and D-genomes found within these allotetraploids to make evolutionary inferences about polyploidy. In this paper we present a comprehensive EST assembly derived from diploid and model allotetraploid cottons and demonstrate several evolutionary inferences regarding genic evolution that can be drawn from these data.ResultsWe generated a set of cotton expressed sequence tags (ESTs), comprising approximately 4.4 million Sanger and next-generation (454) transcripts supplemented by approximately 152 million Illumina reads from diploid and allotetraploid cottons. From the EST alignments we inferred 259,192 genome-specific single nucleotide polymorphisms (SNPs). Molecular evolutionary analyses of protein-coding regions demonstrate that the rate of nucleotide substitution has increased among both allotetraploid genomes relative to the diploids, and that the ratio of nonsynonymous to synonymous substitutions has increased in one of the two polyploid lineages we sampled. We also use these SNPs to show that a surprisingly high percentage of duplicate genes (~7 %) show a signature of non-independent evolution in the allotetraploid nucleus, having experienced one or more episodes of nonreciprocal homoeologous recombination (NRHR).ConclusionsIn this study we characterize the functional and mutational properties of the cotton transcriptome, produce a large genome-specific SNP database, and detect illegitimate genetic exchanges between duplicate genomes sharing a common allotetraploid nucleus. Our findings have important implications for our understanding of the consequences of polyploidy and duplicate gene evolution. We demonstrate that cotton genes have experienced an increased rate of molecular evolution following duplication by polyploidy, and that polyploidy has enabled considerable levels of nonreciprocal exchange between homoeologous genes.

Dataset Information

Parallel and Intertwining Threads of Domestication in Allopolyploid Cotton.

Publications

Parallel and Intertwining Threads of Domestication in Allopolyploid Cotton.

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