Reconstruction of ancestral karyotype illuminates chromosome evolution in the genus Cucumis. (21st July 2021)

• Record Type: Journal Article
• Authors: Zhao, Qinzheng; Meng, Ya; Wang, Panqiao; Qin, Xiaodong; Cheng, Chunyan; Zhou, Junguo; Yu, Xiaqing; Li, Ji; Lou, Qunfeng; Jahn, Molly; Chen, Jinfeng
• Is Part Of: Plant journal. Volume 107:Number 4(2021)
• Page Start: 1243
• Page End: 1259
• Publication Date: 2021-07-21
• Subjects: ancestral karyotype -- chromosome rearrangement -- centromere repositioning -- descending dysploidy -- oligo‐FISH -- Cucumis; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.15381
• Languages: English
• ISSNs: 0960-7412

Abstract

SUMMARY: Karyotype dynamics driven by complex chromosome rearrangements constitute a fundamental issue in evolutionary genetics. The evolutionary events underlying karyotype diversity within plant genera, however, have rarely been reconstructed from a computed ancestral progenitor. Here, we developed a method to rapidly and accurately represent extant karyotypes with the genus, Cucumis, using highly customizable comparative oligo‐painting (COP) allowing visualization of fine‐scale genome structures of eight Cucumis species from both African‐origin and Asian‐origin clades. Based on COP data, an evolutionary framework containing a genus‐level ancestral karyotype was reconstructed, allowing elucidation of the evolutionary events that account for the origin of these diverse genomes within Cucumis . Our results characterize the cryptic rearrangement hotspots on ancestral chromosomes, and demonstrate that the ancestral Cucumis karyotype ( n = 12) evolved to extant Cucumis genomes by hybridizations and frequent lineage‐ and species‐specific genome reshuffling. Relative to the African species, the Asian species, including melon ( Cucumis melo, n = 12), Cucumis hystrix ( n = 12) and cucumber ( Cucumis sativus, n = 7), had highly shuffled genomes caused by large‐scale inversions, centromere repositioning and chromothripsis‐like rearrangement. The deduced reconstructed ancestral karyotype for the genus allowed us to propose evolutionary trajectories and specific events underlying the origin of these Cucumis species. Our findings highlight that the partitioned evolutionary plasticity of Cucumis karyotype is primarily located in the centromere‐proximal regions marked by rearrangement hotspots, which can potentially serve as a reservoir for chromosome evolution due to their fragility. Significance Statement: To date, elucidating karyotype evolution that has been disrupted by complex chromosome rearrangements remains a major challenge in the study of chromosome evolution. By reconstructing a deduced ancestral chromosome and an evolutionary framework using highly customizable comparative oligo‐painting, we demonstrated the evolutionary histories for eight Cucumis species. Our findings highlight that the evolution of Cucumis genomes is marked by partitioned evolutionary plasticity with the essential function of creating karyotype novelty, expanding our understanding for karyotype evolution.