Genomic innovation and regulatory rewiring during evolution of the cotton genus Gossypium

Authors: WANG, MAOJUN - Huazhong Agricultural University; LI, JIANYING - Huazhong Agricultural University; QI, ZHENGYANG - Huazhong Agricultural University; LONG, YUEXUAN - Huazhong Agricultural University; PEI, LIULING - Huazhong Agricultural University; HUANG, XIANHUI - Huazhong Agricultural University; GROVER, CORRINNE - Iowa State University; DU, XIONGMING - Huazhong Agricultural University; Fang, David; XIA, CHUNJIAN - Huazhong Agricultural University; WANG, PENGCHENG - Huazhong Agricultural University; LIU, ZHENPING - Huazhong Agricultural University; YOU, JIAQI - Huazhong Agricultural University; TIAN, XUEHUI - Huazhong Agricultural University; MA, YIZAN - Huazhong Agricultural University; WANG, RUIPENG - Huazhong Agricultural University; CHEN, XINYUAN - Huazhong Agricultural University; HE, XIN - Huazhong Agricultural University; SUN, YUQIANG - Huazhong Agricultural University; TU, LILI - Huazhong Agricultural University; JIN, SHUANGXIA - Huazhong Agricultural University; ZHU, LONGFU - Huazhong Agricultural University; WENDEL, JONATHAN - Iowa State University; ZHANG, XIANLONG - Huazhong Agricultural University

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/20/2022
Publication Date: 12/6/2022
Citation: Wang, M., Li, J., Qi, Z., Long, Y., Pei, L., Huang, X., Grover, C.E., Du, X., Fang, D.D., Xia, C., Wang, P., Liu, Z., You, J., Tian, X., Ma, Y., Wang, R., Chen, X., He, X., Sun, Y., Tu, L., Jin, S., Zhu, L., Wendel, J.F., Zhang, X. 2022. Genomic innovation and regulatory rewiring during evolution of the cotton genus Gossypium. Nature Genetics. 54:1959-1971. https://doi.org/10.1038/s41588-022-01237-2.
DOI: https://doi.org/10.1038/s41588-022-01237-2

Interpretive Summary: Cotton phenotypic diversity is due to the variations in DNA sequences and structures of chromosomes. Such variations may also cause rewiring of regulatory networks. Here, we constructed a pan-genome of the cotton genus using de novo assemblies of 10 representative diploid genomes. We documented the genomic evolutionary history of the genus and the impact of lineage-specific transposon amplification on differential genome composition. Three dimension genome construction unraveled the evolutionary connections between transposon-driven genome size variation and both higher-order chromatin structure reorganization and the rewiring of the chromatin interactome. We linked changes in chromatin structures to phenotypic differences in cotton fiber and identified regulatory variations that decode the genetic basis of fiber length, the latter enabled by sequencing 1,005 transcriptomes during fiber development. We showcased how pan-genomic, pan-3D genomic and genetic regulatory data serve as a resource for delineating the evolutionary basis of spinnable cotton fiber. Our work provides new insights into the evolution of genome organization and regulation in Gossypium, and will enhance cotton improvement by enabling a regulatome-based approach.

Technical Abstract: Phenotypic diversity and evolutionary innovation ultimately trace to variations in genomic sequence and 3D structure and rewiring of regulatory networks. Here, we constructed a pan-genome of the cotton (Gossypium) genus using de novo assemblies of 10 representative diploid genomes. We documented the genomic evolutionary history of the genus and the impact of lineage-specific transposon amplification on differential genome composition. Pan-3D genome construction unraveled the evolutionary connections between transposon-driven genome size variation and both higher-order chromatin structure reorganization and the rewiring of the chromatin interactome. We linked changes in chromatin structures to phenotypic differences in cotton fiber and identified regulatory variations that decode the genetic basis of fiber length, the latter enabled by sequencing 1,005 transcriptomes during fiber development. We showcased how pan-genomic, pan-3D genomic and genetic regulatory data serve as a resource for delineating the evolutionary basis of spinnable cotton fiber. Our work provides new insights into the evolution of genome organization and regulation in Gossypium, and will enhance cotton improvement by enabling a regulatome-based approach.