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

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, <i>Platanus</i> × <i>acerifolia</i> (London planetree; Platanaceae) is a widely used street tree. Given the pivotal phylogenetic position of <i>Platanus</i> and its 2-y flowering transition, understanding its flowering-time regulatory mechanism has significant evolutionary implications; however, the impact of <i>Platanus</i> genome evolution on flowering-time genes remains unknown. Here, we assembled a high-quality, chromosome-level reference genome for <i>P.</i> × <i>acerifolia</i> using a phylogeny-based subgenome phasing method. Comparative genomic analyses revealed that <i>P</i>. × <i>acerifolia</i> (2<i>n</i> = 42) is an ancient hexaploid with three subgenomes resulting from two sequential WGD events; <i>Platanus</i> does not seem to share any WGD with other Proteales or with core eudicots. Each <i>P</i>. × <i>acerifolia</i> subgenome is highly similar in structure and content to the reconstructed pre-WGD ancestral eudicot genome without chromosomal rearrangements. The <i>P</i>. × <i>acerifolia</i> genome exhibits karyotypic stasis and gene sub-/neo-functionalization and lacks subgenome dominance. The copy number of flowering-time genes in <i>P. × acerifolia</i> 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 <i>P. × acerifolia</i>. The <i>P</i>. × <i>acerifolia</i> reference genome will greatly expand understanding of the evolution of genome organization, genetic diversity, and flowering-time regulation in angiosperms.