Evolution of sea‐surfing plant propagule as revealed by the genomes of Heritiera mangroves

SUMMARY Coastal forests, such as mangroves, protect much of the tropical and subtropical coasts. Long‐distance dispersal via sea‐surfing propagules is essential for coastal plants, but the genomic and molecular basis of sea‐surfing plant propagule evolution remains unclear. Heritiera fomes and Heritiera littoralis are two coastal plants with typical buoyant fruits. We de novo sequenced and assembled their high‐quality genomes. Our phylogenomic analysis indicates H. littoralis and H. fomes originated (at ~6.08 Mya) just before the start of Quaternary sea‐level fluctuations. Whole‐genome duplication occurred earlier, permitting gene copy gains in the two species. Many of the expanded gene families are involved in lignin and flavonoid biosynthesis, likely contributing to buoyant fruit emergence. It is repeatedly revealed that one duplicated copy to be under positive selection while the other is not. By examining H. littoralis fruits at three different developmental stages, we found that gene expression levels remain stable from young to intermediate. However, ~1000 genes are up‐regulated and ~ 3000 genes are down‐regulated as moving to mature. Particularly in fruit epicarps, the upregulation of WRKY12 and E2Fc likely constrains the production of p‐Coumaroyl‐CoA, the key internal substrate for lignin biosynthesis. Hence, to increase fruit impermeability, methylated lignin biosynthesis is shut down by down‐regulating the genes CCoAOMT, F5H, COMT, and CSE, while unmethylated lignins are preferentially produced by upregulating CAD and CCR. Similarly, cutin polymers and cuticular waxes accumulate with high levels before maturation in epicarps. Overall, our genome assemblies and analyses uncovered the genomic evolution and temporal transcriptional regulation of sea‐surfing propagule. Significance Statement Our de novo sequenced and assembled high‐quality H. fomes and H. littoralis genomes recovered that WGD has contributed to sea‐surfing propagule origin and evolution by facilitating gene copy expansion and producing duplicated paralogs under differential natural selection. We found the temporal transcriptional regulation of genes involved in unmethylated lignins, cutin polymers, and cuticular waxes biosynthesis is essential for sea‐surfing fruit formation, providing insights for coastal forest conservation and molecular breeding.