Dataset Information

Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium).

ABSTRACT: Cotton is remarkable among our major crops in that four species were independently domesticated, two allopolyploids and two diploids. In each case thousands of years of human selection transformed sparsely flowering, perennial shrubs into highly productive crops with seeds bearing the vastly elongated and abundant single-celled hairs that comprise modern cotton fiber. The genetic underpinnings of these transformations are largely unknown, but comparative gene expression profiling experiments have demonstrated up-regulation of profilin accompanying domestication in all three species for which wild forms are known. Profilins are actin monomer binding proteins that are important in cytoskeletal dynamics and in cotton fiber elongation. We show that Gossypium diploids contain six profilin genes (GPRF1-GPRF6), located on four different chromosomes (eight chromosomes in the allopolyploid). All but one profilin (GPRF6) are expressed during cotton fiber development, and both homeologs of GPRF1-GPRF5 are expressed in fibers of the allopolyploids. Remarkably, quantitative RT-PCR and RNAseq data demonstrate that GPRF1-GPRF5 are all up-regulated, in parallel, in the three independently domesticated cottons in comparison with their wild counterparts. This result was additionally supported by iTRAQ proteomic data. In the allopolyploids, there This usage of novel should be fine, since it refers to a novel evolutionary process, not a novel discovery has been novel recruitment of the sixth profilin gene (GPRF6) as a result of domestication. This parallel up-regulation of an entire gene family in multiple species in response to strong directional selection is without precedent and suggests unwitting selection on one or more upstream transcription factors or other proteins that coordinately exercise control over profilin expression.

SUBMITTER: Bao Y

PROVIDER: S-EPMC3248529 | biostudies-literature | 2011 Dec

REPOSITORIES: biostudies-literature

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Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium).

Bao Ying Y Hu Guanjing G Flagel Lex E LE Salmon Armel A Bezanilla Magdalena M Paterson Andrew H AH Wang Zining Z Wendel Jonathan F JF

Proceedings of the National Academy of Sciences of the United States of America 20111212 52

Cotton is remarkable among our major crops in that four species were independently domesticated, two allopolyploids and two diploids. In each case thousands of years of human selection transformed sparsely flowering, perennial shrubs into highly productive crops with seeds bearing the vastly elongated and abundant single-celled hairs that comprise modern cotton fiber. The genetic underpinnings of these transformations are largely unknown, but comparative gene expression profiling experiments hav ...[more]

PMID: 22160709

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Project description:BACKGROUND:Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). RESULTS:Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. CONCLUSIONS:This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.

Dataset Information

Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium).

Publications

Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium).

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