Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement

Authors: CHEN, Z. JEFFREY - University Of Texas At Austin; SREEDASYAM, AVINASH - Hudsonalpha Institute For Biotechnology; ANDO, ATSUMI - University Of Texas At Austin; SONG, QINGXIN - University Of Texas At Austin; DE SANTIAGO, LUIS - Texas A&M University; Hulse-Kemp, Amanda; DING, MINGQUAN - University Of Texas At Austin; YE, WENXUE - Nanjing Agricultural University; KIRKBRIDE, RYAN - University Of Texas At Austin; JENKINS, JERRY - Hudsonalpha Institute For Biotechnology; PLOTT, CHRISTOPHER - Hudsonalpha Institute For Biotechnology; LOVELL, JOHN - Hudsonalpha Institute For Biotechnology; YU-MING, LIN - Texas A&M University; VAUGHN, ROBERT - Texas A&M University; LIU, BO - Texas A&M University; Simpson, Sheron; Scheffler, Brian

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/16/2020
Publication Date: 4/20/2020
Citation: Chen, Z., Sreedasyam, A., Ando, A., Song, Q., De Santiago, L., Hulse-Kemp, A.M., Ding, M., Ye, W., Kirkbride, R., Jenkins, J., Plott, C., Lovell, J., Yu-Ming, L., Vaughn, R., Liu, B., Simpson, S.A., Scheffler, B.E. 2020. Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement. Nature Genetics. https://doi.org/10.1038/s41588-020-0614-5.
DOI: https://doi.org/10.1038/s41588-020-0614-5

Interpretive Summary: In order to understand the polyploid event that led to two extraordinary cotton species that produce 99% of the world's cotton crop, we have sequenced to high-quality the five distinct cotton species that formed following a single polyploidization event 1-1.6 million years ago. By comparing the first complete set of high-quality tetraploid genome sequences we were able to find that despite wide geographic distribution and diversification following polyploidization, there are a very limited number of differences in the genome sequences. We have explored the differences in repetitive sequences, gene sequences, and specific gene families and all show striking levels of similarity. The smaller subgenome appears to play an important role in the superior traits of agronomic importance including disease resistance genes and genes important for quality characteristics. Recombination is essential for breeders to be able to develop new cultivar lines, we find that "cold spots" of recombination in the genome coincide with regions that have special marks on the DNA which limit the ability to make these new recombinations. These findings are likely why the ultimate combination of Upland cotton with Pima cotton has eluded breeders for centuries. These results will empower efforts to breed the next generation of cultivars for improved cotton production. To our knowledge, this is the first effort in any crop polyploidization event to have sequenced most of the resulting polyploid member species to such high a quality, which allowed for a thorough investigation of the entire genome and the changes that follow a radiation event.

Technical Abstract: Cotton is the largest source of renewable textile fiber and also a powerful model for studying polyploid evolution and crop domestication. Allotetraploid cottons (AADD-genome) formed monophyletically 1-1.6 million years ago and diversified into five or more species, including the economically important Upland and Pima cottons. Despite wide geographic distribution and diversification following polyploidization, the five allotetraploids experienced limited structural variation and retained collinearity and conservation of gene content and number. Evolution and selection were accompanied by transposon exchanges between subgenomes and diversification of R-gene families and subgenomic expression patterns, while domesticated cottons and wild species possess unique genes and co-expression networks, contributing respectively to fiber and seed traits and reproductive adaptation. Moreover, the smaller D subgenome has fewer gene losses, more disease-resistant genes and more expression diversity in most organs. In domesticated cottons, recombination “cold spots” coincide with DNA hypermethylation and weak chromatin connection, creating genetic bottlenecks that can be disrupted by interspecific hybridization. These results will empower efforts to manipulate genetic recombination, modify epigenetic landscapes, and edit target genes for cotton improvement.