Reconstructing the evolutionary trajectory of Chamaelirium (Melanthiaceae) through phylogenomics: insights from plastome dynamics and historical biogeography.

BACKGROUND: The East Asia-eastern North America disjunction represents a classic biogeographic pattern, widely interpreted as a relic of Tertiary temperate forests that were widespread across the Northern Hemisphere. Although this pattern has been well-documented in woody plants, disjunctions in herbaceous taxa have remained relatively unexplored, despite their potential to provide significant evolutionary insights. The genus Chamaelirium represents a suitable system for investigating herbaceous discontinuity between East Asia and eastern North America. However, unresolved section-level relationships within the genus based on limited molecular data indicated that its systematics still required clarification. Here, we generated complete plastid genomes (plastomes) for five Chamaelirium species covering all sections of the genus and performed the phylogenomic analysis for the first time with a reexamination of its historical biogeography. RESULTS: Comparative genomic analyses revealed that Chamaelirium plastomes exhibit relatively conserved structures and content organization; however, several noteworthy variations were observed. Specifically, an expansion of the IR region was identified in the plastid genomes of C. viridiflorum and C. chinense, while the loss of the rps16 gene in C. japonicum and C. koidzumianum may have contributed to a reduction in genome size. Phylogenetic analysis combined with niche modeling revealed two major clades within Chamaelirium, corresponding to the two sections proposed in traditional classifications. Robust support for interspecific relationships within each section was provided by morphological characters, plastome variations, and geographical distributions. Divergence time estimates and ancestral region reconstructions indicate that Chamaelirium originated in the Eocene (ca. 53.03 Ma), with the ancestral area of its crown most likely located in East Asia. The divergence between the East Asian and North American lineages occurred during the early Miocene (ca. 17.95 Ma), with the Bering Land Bridge acting as a corridor; subsequent global cooling likely facilitated the establishment of an intercontinental disjunction in the genus. The rise of the East Asian monsoon during the late Miocene may have further triggered its diversification in East Asia. CONCLUSIONS: Our phylogenomic analyses of Chamaelirium have resolved previously ambiguous section-level relationships and provide novel genomic resources for clarifying infrageneric boundaries. Furthermore, by presenting Chamaelirium as a new case, this study highlights the significance of the Miocene and the Bering Land Bridge in shaping the East Asian-North American disjunction pattern among herbaceous plants.