Evolutionary Conservation and Divergence of Gene Coexpression Networks in Gossypium (Cotton) Seeds.

The cotton genus (Gossypium) provides a superior system for the study of diversification, genome evolution, polyploidization, and human-mediated selection. To gain insight into phenotypic diversification in cotton seeds, we conducted coexpression network analysis of developing seeds from diploid and allopolyploid cotton species and explored network properties. Key network modules and functional associations were identified related to seed oil content and seed weight. We compared species-specific networks to reveal topological changes, including rewired edges and differentially coexpressed genes, associated with speciation, polyploidy, and cotton domestication. Network comparisons among species indicate that topologies are altered in addition to gene expression profiles, indicating that changes in transcriptomic coexpression relationships play a role in the developmental architecture of cotton seed development. The global network topology of allopolyploids, especially for domesticated G. hirsutum, resembles the network of the A-genome diploid more than that of the D-genome parent, despite its D-like phenotype in oil content. Expression modifications associated with allopolyploidy include coexpression level dominance and transgressive expression, suggesting that the transcriptomic architecture in polyploids is to some extent a modular combination of that of its progenitor genomes. Among allopolyploids, intermodular relationships are more preserved between two different wild allopolyploid species than they are between wild and domesticated forms of a cultivated cotton, and regulatory connections of oil synthesis-related pathways are denser and more closely clustered in domesticated vs. wild G. hirsutum. These results demonstrate substantial modification of genic coexpression under domestication. Our work demonstrates how network inference informs our understanding of the transcriptomic architecture of phenotypic variation associated with temporal scales ranging from thousands (domestication) to millions (speciation) of years, and by polyploidy.

A Transcriptome Profile for Developing Seed of Polyploid Cotton.

Cotton ranks among the world's important oilseed crops, yet relative to other oilseeds there are few studies of oil-related biosynthetic and regulatory pathways. We present global transcriptome analyses of cotton seed development using RNA-seq and four developmental time-points. Because Upland cotton (Gossypium hirsutum L.) is an allopolyploid containing two genomes (A/D), we partitioned expression into the individual contributions of each homeologous gene copy. Data were explored with respect to genic and subgenomic patterns of expression, globally and with respect to seed pathways and networks. The most dynamic period of transcriptome change is from 20-30 d postanthesis (DPA), with about 20% of genes showing homeolog expression bias. Co-expression analysis shows largely congruent homeolog networks, but also homeolog-specific divergence. Functional enrichment tests show that flavonoid biosynthesis and lipid related genes were significantly represented early and later in seed development, respectively. An involvement of new features in oil biosynthesis was found, like the contribution of DGAT3 (diacylglycerol acyltransferase) to the total triglyceride expression pool. Also, catechin-based and epicatechin-based proanthocyanidin expression are reciprocally biased with respect to homeolog usage. This study provides the first temporal analysis of duplicated gene expression in cotton seed and a resource for understanding new aspects of oil and flavonoid biosynthetic processes.