Evolution of woody plants to the land‐sea interface – The atypical genomic features of mangroves with atypical phenotypic adaptation

Abstract How plants adapt and diverge in extreme environments is a key question of plant evolution and ecology. Mangrove invasion of intertidal environments is facilitated by adaptive phenotypes such as aerial roots, salt‐secreting leaf, and viviparity, and genomic mechanisms including whole genome duplication and transposable element number reduction. However, a number of mangroves lack these typical phenotypes. The question we ask is whether these phenotypically atypical mangroves also have distinct genomic features? The sibling mangrove species Lumnitzera littorea and Lumnitzera racemosa provide a model to study this question. We sequenced and assembled their genomes to chromosome level, together with a closely related species Combretum micranthum . While most mangroves have small genomes, the genomes of both Lumnitzera species are large (1443 and 1317 Mb) and carry a high proportion of repeat sequences (~75%). Moreover, Lumnitzera species have not undergone post‐gamma whole‐genome duplications. Their genome size increased mainly due to the expansion of repeat sequences in their ancestors. However, Lumnitzera genomes have reduced transposable elements by constraining the proliferation of new LTR‐RTs. Meanwhile, the two species have more gene families contracted than expanded, and some gene families with reversed size change may underlie their differentiation in root morphology and local distribution. We identified 86 chromosomal inversions, five of which are measured between 6.5 and 12.8 megabases. A number of genes located in these inversions function in pigment biosynthesis, a process likely involved in flower colour differentiation between the Lumnitzera species. We conclude that the mangroves with atypical phenotypes also have atypical genomic evolution.