Divergent Evolutionary Routes of Hypoxia Tolerance in Mangroves

Extreme environments impose conditions that are lethal to most organisms, yet a limited number of evolutionary lineages have adapted to chronic stress. However, whether distinct lineages exposed to the similar stressors rely on shared adaptive mechanisms remains poorly understood. Mangroves offer a compelling system to address this question, as they thrive in shared harsh environments. Here, we examine two mangrove species, Kandelia obovata and Avicennia marina, both inhabiting intertidal zones but deploying contrasting strategies to withstand hypoxia. Phylogenomic analyses revealed that K. obovata experienced an ancestral whole-genome duplication (WGD) prior to intertidal colonization, whereas A. marina underwent two rounds of WGD that expanded its repertoire of hypoxia-responsive genes. Comparative genomic analyses showed that K. obovata underwent contraction of hypoxia-related gene families and harbours fewer gene copies, but each copy is enriched with cis-regulatory elements. In contrast, A. marina retained significantly more hypoxia-related genes derived from recent WGD. Transcriptomic profiling under controlled hypoxia gradients further showed that K. obovata relies on rapid but stable gene expression responses, while A. marina exhibits delayed but hierarchical gene regulatory networks. Together, these results demonstrate that even under identical extreme selective pressures, plant lineages can follow distinct evolutionary routes, shaped by differences in genome evolution and regulatory architecture.