Genome Assembly of Three Shrub Mangroves in the Genus Acanthus Reveals Two Polyploidy Events and Expansion of Genes Linked to Root Adaptation in Coastal Habitats.

backgroundThe genomes of mangrove Acanthus species have not been reported, despite their ecological and medicinal importance. Here, we generated reference genomes for three shrub mangroves in the genus Acanthus to clarify their whole-genome duplication and hybridization events and identify genomic features underlying their evolution.

resultsUsing PacBio and Hi-C data, we generated a chromosome-scale genome assembly of the recently identified allotetraploid species Acanthus tetraploideus (2n = 96). The genomes of diploid progenitors, Acanthus ilicifolius and Acanthus ebracteatus (2n = 48), were assembled from single-tube long fragment read data. We identified an Acanthus-specific whole-genome duplication (WGD) event that occurred ∼43 million years ago (Mya). Ancestral karyotype reconstruction revealed a shift in haploid chromosome number from 11 to 24 in the progenitors, following the WGD and subsequent chromosomal fission events. The hybridization that formed A. tetraploideus was estimated to have occurred 0.7-1.8 Mya. Phylogenomic and synteny analyses clearly showed that A. tetraploideus inherited subgenomes SG1 and SG2 from A. ilicifolius and A. ebracteatus, respectively. Gene structure and retention analyses revealed a smaller and more structurally flexible genome in A. ebracteatus and SG2 compared with A. ilicifolius and SG1. Gene family and machine learning analyses identified expansions in protein families related to Casparian strip formation, root development, and salt stress response. Several of these families were expanded in A. ilicifolius and SG1 but contracted in A. ebracteatus and SG2. These genomic patterns might have contributed to the establishment of A. tetraploideus within the habitat of A. ebracteatus. For all three species, population analysis revealed clear genetic divergence between samples from the eastern and western coasts of Thailand.

conclusionsThese genome assemblies clarify the polyploidy and hybridization history of Acanthus and highlight gene family changes potentially associated with coastal root adaptation and habitat establishment in intertidal environments. This study provides valuable genomic resources and insights into the evolutionary adaptation of plants to intertidal environments.