Cotton D genome assemblies built with long-read data unveil mechanisms of centromere evolution and stress tolerance divergence

Zhaoen Yang,Fuyan Liu,Lisen Liu,Weinan Li,Xiaoyang Ge,Fuguang Li,Shaoliang Peng,Wei Hu,Yanli Chen,Yuying Jin

doi:10.1186/s12915-021-01041-0

Abstract

BackgroundMany of genome features which could help unravel the often complex post-speciation evolution of closely related species are obscured because of their location in chromosomal regions difficult to accurately characterize using standard genome analysis methods, including centromeres and repeat regions.ResultsHere, we analyze the genome evolution and diversification of two recently diverged sister cotton species based on nanopore long-read sequence assemblies and Hi-C 3D genome data. Although D genomes are conserved in gene content, they have diversified in gene order, gene structure, gene family diversification, 3D chromatin structure, long-range regulation, and stress-related traits. Inversions predominate among D genome rearrangements. Our results support roles for 5mC and 6mA in gene activation, and 3D chromatin analysis showed that diversification in proximal-vs-distal regulatory-region interactions shape the regulation of defense-related-gene expression. Using a newly developed method, we accurately positioned cotton centromeres and found that these regions have undergone obviously more rapid evolution relative to chromosome arms. We also discovered a cotton-specific LTR class that clarifies evolutionary trajectories among diverse cotton species and identified genetic networks underlying the Verticillium tolerance of Gossypium thurberi (e.g., SA signaling) and salt-stress tolerance of Gossypium davidsonii (e.g., ethylene biosynthesis). Finally, overexpression of G. thurberi genes in upland cotton demonstrated how wild cottons can be exploited for crop improvement.ConclusionsOur study substantially deepens understanding about how centromeres have developed and evolutionarily impacted the divergence among closely related cotton species and reveals genes and 3D genome structures which can guide basic investigations and applied efforts to improve crops.

Highlights

Many of genome features which could help unravel the often complex post-speciation evolution of closely related species are obscured because of their location in chromosomal regions difficult to accurately characterize using standard genome analysis methods, including centromeres and repeat regions
We found that enhanced salicylic acid (SA) signaling and ethylene biosynthesis contribute to the respective abilities of G. thurberi and G. davidsonii to cope with biotic (Verticillium dahliae) and abiotic stress
Using 284 million and 280 million valid high-throughput chromosome conformation capture (Hi-C) interaction pairs for the G. thurberi and G. davidsonii genomes, respectively (Additional file 1: Table S4), we anchored and oriented 777.2 and 799.2 Mb of the assembly onto 13 pseudochromosomes of G. thurberi and G. davidsonii respectively (Additional file 2: Fig. S1-S2), which represented more than 99.7% of the total assembly, indicating that our new assemblies reached a reference grade for quality

Summary

Introduction

Many of genome features which could help unravel the often complex post-speciation evolution of closely related species are obscured because of their location in chromosomal regions difficult to accurately characterize using standard genome analysis methods, including centromeres and repeat regions. Even though none of the D diploid species produce commercial fibers, the diploid D genome is known as the donor of the D subgenome in wild and domesticated allotetraploid cotton, and the D genome harbors potentially useful genes for improving fiber quality, disease and pest resistance, and cytoplasmic male sterility, as well as drought and salt tolerance in domesticated cotton [8, 9] Because of their close relationships to the agronomically important cultivated cotton, the diversity, distribution, phylogenetic relationships, and taxonomy of the D genome wild cotton species have attracted scientific interest [7, 10]. They showed different phenotypic characters: compared with G. raimondii, G. thurberi is more tolerant to Verticillium wilt and G. davidsonii is more tolerant to salt

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Discussion

Conclusion