Abstract
The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely one-half of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ∼5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution.
Highlights
Ever since Darwin’s time, biologists have recognized that human domestication of wild plants and animals offers promising opportunities for enhancing our understanding of the evolutionary process
Based on the criterion of RPKM§5, approximately 12,700 (33.9%) and 12,000 (33.0%) genes were expressed at 10 and 20 dpa, respectively, in most accessions (Table 2); three domesticated accessions (Cascot L-7, Coker 315, and CRB250) showed lower numbers of expressed genes at 20 dpa compared to other accessions, which we attribute to the higher proportions of redundantly mapped reads in these accessions
Concluding remarks the transcriptomic data presented here are extraordinarily complex, as is usually the case in comparative profiling experiments, the data allow a speculative scenario to emerge from a consideration of the different classes of genes and pathways that are enriched under domestication
Summary
Ever since Darwin’s time, biologists have recognized that human domestication of wild plants and animals offers promising opportunities for enhancing our understanding of the evolutionary process. The trait for which cotton was initially domesticated is the remarkably elongated, single-celled epidermal trichomes, or hairs, that cover the cottonseed surface (colloquially termed ‘‘fibers’’) These seed hairs vary greatly in length, color, strength, and density among the myriad wild, semi-domesticated, feral and modern annualized forms that collectively comprise the species G. hirsutum. Gossypium hirsutum was initially domesticated at least 5000 years ago, and following millennia of directional selection, domesticated forms produce long, strong, and fine white fibers along with a dramatically enhanced fiber yield In addition to this increase in fiber length, strength, and quality, the domestication process brought about other morphological transformations, including decreased plant stature, earlier flowering, and loss of seed dormancy
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