Chromosome-level assembly of Lindenbergia philippensis and comparative genomic analyses shed light on genome evolution in Lamiales

Lamiales, comprising over 23,755 species across 24 families, stands as a highly diverse and prolific plant group, playing a significant role in the cultivation of horticultural, ornamental, and medicinal plant varieties. Whole-genome duplication (WGD) and its subsequent post-polyploid diploidization (PPD) process represent the most drastic type of karyotype evolution, injecting significant potential for promoting the diversity of this lineage. However, polyploidization histories, as well as genome and subgenome fractionation following WGD events in Lamiales species, are still not well investigated. In this study, we constructed a chromosome-level genome assembly of <i>Lindenbergia philippensis</i> (Orobanchaceae) and conducted comparative genomic analyses with 14 other Lamiales species. <i>L. philippensis</i> is positioned closest to the parasitic lineage within Orobanchaceae and has a conserved karyotype. Through a combination of Ks analysis and syntenic depth analysis, we reconstructed and validated polyploidization histories of Lamiales species. Our results indicated that <i>Primulina huaijiensis</i> underwent three rounds of diploidization events following the γ-WGT event, rather than two rounds as reported. Besides, we reconfirmed that most Lamiales species shared a common diploidization event (L-WGD). Subsequently, we constructed the Lamiales Ancestral Karyotype (LAK), comprising 11 proto-chromosomes, and elucidated its evolutionary trajectory, highlighting the highly flexible reshuffling of the Lamiales paleogenome. We identified biased fractionation of subgenomes following the L-WGD event across eight species, and highlighted the positive impacts of non-WGD genes on gene family expansion. This study provides novel genomic resources and insights into polyploidy and karyotype remodeling of Lamiales species, essential for advancing our understanding of species diversification and genome evolution.

唇形目（Lamiales）是一个物种多样性极高且类群丰富的植物类群，包含24个科、总计超过23755个物种，在园艺、观赏及药用植物的培育中发挥着重要作用。全基因组复制（whole-genome duplication, WGD）及其后续的多倍体后二倍体化（post-polyploid diploidization, PPD）过程是该类群最为剧烈的染色体组进化类型，为该谱系的多样性演化提供了重要潜能。然而，目前学界对唇形目物种的多倍化历史，以及全基因组复制事件后发生的基因组与亚基因组分馏，仍缺乏充分研究。本研究构建了菲律宾野胡麻（*Lindenbergia philippensis*，列当科Orobanchaceae）的染色体级基因组组装，并与另外14种唇形目物种开展比较基因组学分析。该物种处于列当科寄生类群的姐妹分支位置，且拥有保守的染色体组型。本研究通过Ks分析与共线性深度分析，重构并验证了唇形目物种的多倍化历史。研究结果显示，怀集报春苣苔（*Primulina huaijiensis*）在γ-全基因组三倍化（γ-WGT）事件后经历了三轮二倍化过程，而非此前报道的两轮。此外，本研究进一步证实，多数唇形目物种共享一次共同的二倍化事件（L-WGD）。随后，本研究构建了包含11条原始染色体的唇形目祖先染色体组型（Lamiales Ancestral Karyotype, LAK），并阐明了其演化轨迹，揭示了唇形目古基因组的重排具有高度灵活性。本研究在8个物种中检测到L-WGD事件后发生的亚基因组偏向性分馏，并阐明了非全基因组复制基因对基因家族扩张的积极作用。本研究为唇形目物种的多倍化与染色体组型重塑提供了全新的基因组资源与研究视角，有助于推动学界对物种多样性演化与基因组进化的认知。