Insights into the evolution of the New World diploid cottons (Gossypium, subgenus Houzingenia) based on genome sequencing

Authors: GROVER, CORRINE - Iowa State University; ARICK, MARK - Mississippi State University; THRASH, ADAM - Mississippi State University; CONOVER, JUSTIN - Iowa State University; SANDERS, WILLIAMS - Mississippi State University; PETERSON, DANIEL - Mississippi State University; Frelichowski, James - Jim; Scheffler, Jodi; Scheffler, Brian; WENDEL, JONATHAN - Iowa State University

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/20/2018
Publication Date: 11/23/2018
Citation: Grover, C.E., Arick, M.A., Thrash, A., Conover, J.L., Sanders, W.S., Peterson, D.G., Frelichowski, J.E., Scheffler, J.A., Scheffler, B.E., Wendel, J.F. 2018. Insights into the evolution of the New World diploid cottons (Gossypium, subgenus Houzingenia) based on genome sequencing. Genome Biology and Evolution. 11(1):53-71. https://doi.org/10.1093/gbe/evy256.
DOI: https://doi.org/10.1093/gbe/evy256

Interpretive Summary: Cultivated cotton is the result of hybridization between two wild cotton species. Investigating the wild species that contributed to cultivated cotton can help us better understand them and find ways to improve cotton as an important natural fiber crop. The genomes of one group of related wild cottons with similar genetic make-up were studied to determine which were more closely related and the reason behind their small genome size compared to other cotton relatives. This group of wild cottons were estimated to have originated about six million years ago and has since diversified and spread. They are now found in the USA, Mexico, Peru and the Galapagos Islands. Over time, it appears their genome size remained small due to deletions that counteracted insertions and duplications and which occurred as the different species evolved.

Technical Abstract: Phylogenomic methods were employed to study molecular evolutionary processes and phylogeny in the geographically widely dispersed New World diploid cottons (Gossypium, subg. Houzingenia). Whole genome resequencing data (average of 33X genomic coverage) were generated to reassess the phylogenetic history of the subgenus and provide a temporal framework for its diversification. Phylogenetic analyses indicate that the subgenus likely originated following trans-oceanic dispersal from Africa about 6.6 million years ago (mya), but that nearly all of the biodiversity evolved following rapid diversification in the mid-Pleistocene (0.5-2.0 mya), with multiple long-distance dispersals required to account for range expansion to Arizona, the Galapagos Islands and Peru. Comparative analyses of chloroplast DNA vs. nuclear DNA data indicate that this history was accompanied by several clear cases of interspecific introgression. Repetitive DNAs contribute roughly half of the total 880 Mega base (Mb) pairs genome, but most transposable element families are relatively old and stable among species. In the genic fraction, pairwise synonymous mutation rates average 1% per million years, with non-synonymous changes being about seven times less frequent. Over 1.1 million insertion or deletions (indels) were detected and phylogenetically characterized, revealing a two-fold bias toward deletions over insertions. We suggest that this genome down-sizing bias counteracts genome size growth by transposable element (TE) amplification and insertions, and helps explain the relatively small genomes that are found in this subgenus. Compared to the rate of nucleotide substitution, the rate of indel occurrence is much lower averaging about 17 nucleotide substitutions per indel event.