Evolutionary dynamics of chromatin structure and duplicate gene expression in diploid and allopolyploid cotton

Authors: HU, GUANJING - CHINESE ACADEMY OF AGRICULTURAL SCIENCES; GROVER, CORRINNE - IOWA STATE UNIVERSITY; VERA, DANIEL - FLORIDA STATE UNIVERSITY; LUNG, PEI-YAU - FLORIDA STATE UNIVERSITY; GIRIMURUGAN, SENTIL - FLORIDA GULF COAST UNIVERSITY; MILLER, EMMA - IOWA STATE UNIVERSITY; CONOVER, JUSTIN - IOWA STATE UNIVERSITY; OU, SHUJUN - THE OHIO STATE UNIVERSITY; XIONG, XIANPENG - CHINESE ACADEMY OF AGRICULTURAL SCIENCES; ZHU, DE - CHINESE ACADEMY OF AGRICULTURAL SCIENCES; DONGMING, LI - ZHENGZHOU UNIVERSITY; Gallagher, Joseph - Joe; Udall, Joshua - Josh; SUI, XIN - FLORIDA STATE UNIVERSITY; ZHANG, JINFENG - FLORIDA STATE UNIVERSITY; BASS, HANK - FLORIDA STATE UNIVERSITY; WENDEL, JONATHAN - IOWA STATE UNIVERSITY

Submitted to: Nature Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2024
Publication Date: 5/17/2024
Citation: Hu, G., Grover, C.E., Vera, D.L., Lung, P., Girimurugan, S.B., Miller, E.R., Conover, J.L., Ou, S., Xiong, X., Zhu, D., Dongming, L., Gallagher, J.P., Udall, J.A., Sui, X., Zhang, J., Bass, H.W., Wendel, J.F. 2024. Evolutionary dynamics of chromatin structure and duplicate gene expression in diploid and allopolyploid cotton. Nature Plants. 41(5). https://doi.org/10.1093/molbev/msae095.
DOI: https://doi.org/10.1093/molbev/msae095

Interpretive Summary: Polyploidy is the state of having more than two complete sets of chromosomes. Many crop species are polyploid or have polyploid varieties, yet the nuances of how gene regulation evolves after genome duplication is still under investigation. The organization of DNA and proteins into chromatin and specifically structures called nucleosomes can affect how easily DNA is accessed and thus how genes are expressed. Approximately 1-2 million years ago, two cotton species most similar to modern Gossypium arboreum (A-genome) and G. raimondii (D-genome) underwent hybridization and genome duplication (allopolyploidization) to produce the ancestor of modern polyploid cultivated cotton, G. hirsutum (AD-genome). Here, we used a technique called differential micrococcal nuclease digested nucleosomal DNA sequencing (dns-MNase-seq) to assess the effect of nucleosome organization and chromatin accessibility on gene expression in these three cotton species and a hybrid of G. arboreum and G. raimondii. We observed a synchronization of chromatin accessibility and regulatory motifs between the two subgenomes in the allopolyploid G. hirsutum. Additionally, we found that A- or D-biased gene expression patterns were correlated with accessibility of chromatin in the corresponding genes of the allopolyploid. This research informs how patterns of chromatin organization and gene regulation evolve in polyploid species, and will be invaluable in future research connecting these phenomena to specific phenotypes in polyploid and hybrid crops.

Technical Abstract: Polyploidy is a prominent mechanism of plant speciation and adaptation, yet the mechanistic understandings of duplicated gene regulation remain elusive. Chromatin structure dynamics are suggested to govern gene regulatory control. Here we characterized genome-wide nucleosome organization and chromatin accessibility in allotetraploid cotton, Gossypium hirsutum (AADD, 2n=4X=52), relative to its two diploid parents (AA and DD genomes) and their synthetic diploid hybrid, using dns-MNase-seq. The larger A-genome exhibited wider nucleosome spacing in diploids, and this inter-genomic difference diminished in the allopolyploid but not hybrid. Allopolyploidization also altered accessibility more than did hybridization, increasing promoter accessibility genome-wide and synchronizing cis-regulatory motifs between subgenomes. A prominent cis-acting effect was inferred for chromatin dynamics and demonstrated by promoter TE depletion. Linking accessibility to gene expression patterns, we revealed distinct regulatory effects for hybridization and later allopolyploid stages, including nuanced establishment of homoeolog expression bias and expression level dominance. Histone gene expression and nucleosome organization are interrelated through chromatin accessibility. Our study reveals the role of chromatin dynamics in cis-regulatory landscape evolution and duplicate gene expression in polyploids, illuminating regulatory ties to subgenomic asymmetry and dominance.