Comparative Evolutionary and Developmental Dynamics of the Cotton (Gossypium hirsutum) Fiber Transcriptome

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.

Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement

“…13). However, in a specific tissue or developmental stage, 20-40% of homoeologous gene pairs showed biased A-or D-homoeolog expression (Supplementary Table 17), which is consistent with the published data 4,34 and may lead to subfunctionalization because of expression divergence 35 . There were slightly more genes with expression bias toward the D homoeologs than toward the A homoeologs (Supplementary Fig.…”

“…14). Although the number of genes that were biased toward either A-or D-homeolog expression in cotton fiber elongation (10 days post-anthesis (DPA)) and secondary cell wall synthesis (20 DPA) were similar to those previously reported 34 , more transcription factor genes (such as MYB family members) were expressed in the A homoeologs ( Supplementary Fig. 15), suggesting important roles in fiber development 36 .…”

“…Interestingly, these A-and D-subgenome PSGs were enriched in different gene ontology groups. Many of the A-homoeologous PSGs (343/470) were enriched in the synthesis of ethylene and very-long-chain fatty acids, which are known to affect fiber elongation 40 , and in sucrose metabolism and beta-d-glucan biosynthetic pathway to produce UDP-glucose, the preferred substrate for cellulose biosynthesis 34,41,42 (Fig. 4a).…”

Discovering new biology through RNA-Seq

“…Comparative analysis of gene expression during cotton fiber development in four wild and five cultivated accessions of cotton revealed, among other important findings, that human selection during domestication has led to a prolonged duration of fiber elongation. Also, the wild accessions allocate a larger part of their transcriptional investment to stressresponse pathways, whereas the domesticated species allocate more to growth-related processes (Yoo and Wendel, 2014). Again, comparison of wild ancestors with cultivated accessions showed a dramatic and wide-ranging rewiring of the transcriptome as a consequence of domestication (Yoo and Wendel, 2014).…”

Recent Developments in Fiber Genomics of Tetraploid Cotton Species

“…This has been shown by comparative transcriptome profiling of developing fiber using RNA-Seq analysis. Over 5000 differentially expressed genes were found with a regulatory or participatory role in primary and secondary cell wall synthesis between wild and domesticated cottons, which arose from artificial selection [69]. Some 210,965 unigenes of more than 100 bp were obtained from 47.2 million paired end reads of the anthers of TM-1 through transcriptome sequencing.…”