Parallel and intertwining threads of domestication in allopolyploid cotton

Authors: YUAN, DAOJUN - Huazhong Agricultural University; GROVER, CORRINNE - Iowa State University; HU, GUANJING - Iowa State University; PAN, MENGQIAO - Nanjing Agricultural University; MILLER, EMMA - Iowa State University; CONOVER, JUSTIN - Iowa State University; HUNT, SPENCER - Biofire Diagnostics; Udall, Joshua - Josh; WENDEL, JONATHAN - Iowa State University

Submitted to: Advanced Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/2/2021
Publication Date: 3/15/2021
Citation: Yuan, D., Grover, C.E., Hu, G., Pan, M., Miller, E., Conover, J.L., Hunt, S., Udall, J.A., Wendel, J.F. 2021. Parallel and intertwining threads of domestication in allopolyploid cotton. Advanced Science. Article 2003634. https://doi.org/10.1002/advs.202003634.
DOI: https://doi.org/10.1002/advs.202003634

Interpretive Summary: There are two different species of cotton, Gossypium hirsutum, or Upland cotton; and G. barbadense or Pima cotton. They originated in different parts of the world. Upland cotton came from Central America and Pima cotton came from South America. Both species have the same number of chromosomes. They both are cultivated for fiber and textile production, but for different end products. In both cases, genetic improvement of cultivars depends on the amount of available genetic variation. In this study, we sequenced a collection of cotton genomes from more than 700 cotton varieties and we cataloged the genetic variation that is available to cotton breeders. This collection was carefully selected to include old varieties and also wild progenitors of cotton. Once the genetic variation was cataloged, we also identified genome regions that were selected for good fiber during the domestication process of cotton. In addition, a significant amount of historical inter-mating occurred between the two species. These genetic interchanges represent genome regions important for disease resistance and fiber quality.

Technical Abstract: The two cultivated allopolyploid cotton species, Gossypium hirsutum and G. barbadense, represent a remarkable example of parallel independent domestication, both of which involve dramatic morphological transformations under directional human selection from wild perennial plants to annualized row crops. Utilizing deep resequencing of 643 newly sampled accessions spanning the wild-to-domesticated continuum of both species, combined with existing data, and through inclusion of all other allopolyploid relatives, we resolve species relationships and elucidate multiple aspects of the parallel domestication process. We confirm that wild forms of G. hirsutum and G. barbadense were initially domesticated in the Yucatan Peninsula and northwest South America, respectively, from where they spread under domestication during their 4,000 - 8,000 year history to encompass most of the American tropics. We present a robust phylogenomic analysis of infraspecific relationships in each species, quantify genetic diversity in both species, and describe genetic bottlenecks associated with domestication and subsequent diffusion. As the two species became sympatric over the last several millennia, pervasive and genome-wide bidirectional introgression occurred, often with striking asymmetries with respect to the two co-resident genomes of these allopolyploids. Genomic diversity scans revealed genome wide regions and genes unknowingly targeted during the domestication process, and additional asymmetries with respect to the two subgenomes. Our new genome-scale understanding of genetic variation provides a comprehensive depiction of the origin, divergence, and adaptation of cotton, and should serve as a rich resource for cotton improvement.