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Genome evolution of the ancient hexaploid <i>Platanus</i> × <i>acerifolia</i> (London planetree)

Xu Yan, Gehui Shi, Miao Sun, Shengchen Shan, Runzhou Chen, Runhui Li, Songlin Wu, Zheng Zhou, Yuhan Li, Zhenhua Liu, Yonghong Hu, Zhong‐Jian Liu, Pamela S. Soltis, Jiaqi Zhang, Douglas E. Soltis, Guogui Ning, Manzhu Bao

2024Proceedings of the National Academy of Sciences17 citationsDOIOpen Access PDF

Abstract

Whole-genome duplication (WGD; i.e., polyploidy) and chromosomal rearrangement (i.e., genome shuffling) significantly influence genome structure and organization. Many polyploids show extensive genome shuffling relative to their pre-WGD ancestors. No reference genome is currently available for Platanaceae (Proteales), one of the sister groups to the core eudicots. Moreover, Platanus × acerifolia (London planetree; Platanaceae) is a widely used street tree. Given the pivotal phylogenetic position of Platanus and its 2-y flowering transition, understanding its flowering-time regulatory mechanism has significant evolutionary implications; however, the impact of Platanus genome evolution on flowering-time genes remains unknown. Here, we assembled a high-quality, chromosome-level reference genome for P. × acerifolia using a phylogeny-based subgenome phasing method. Comparative genomic analyses revealed that P . × acerifolia (2 n = 42) is an ancient hexaploid with three subgenomes resulting from two sequential WGD events; Platanus does not seem to share any WGD with other Proteales or with core eudicots. Each P . × acerifolia subgenome is highly similar in structure and content to the reconstructed pre-WGD ancestral eudicot genome without chromosomal rearrangements. The P . × acerifolia genome exhibits karyotypic stasis and gene sub-/neo-functionalization and lacks subgenome dominance. The copy number of flowering-time genes in P. × acerifolia has undergone an expansion compared to other noncore eudicots, mainly via the WGD events. Sub-/neo-functionalization of duplicated genes provided the genetic basis underlying the unique flowering-time regulation in P. × acerifolia . The P . × acerifolia reference genome will greatly expand understanding of the evolution of genome organization, genetic diversity, and flowering-time regulation in angiosperms.

Topics & Concepts

GenomeBiologyEudicotsGenome evolutionPhylogenetic treeComparative genomicsGeneGeneticsEvolutionary biologyPlant evolutionPhylogeneticsGenomicsBotanyTaxonomy (biology)Chromosomal and Genetic VariationsGenomics and Phylogenetic StudiesPlant Reproductive Biology