Distinct molecular responses of mangrove plants to hypoxia and reoxygenation stresses contribute to their resilience in coastal wetland environment

Abstract

Mangroves adapt to periodical submergence and constitute resilient ecosystems in coastal environments. The question is whether they can sustain long submergence stress when sea level rises as a consequence of climate change. To address this, seedlings of two representative mangrove species that acclimate to low to mid tide (Avicennia marina) and mid to high tide (Kandelia obovata) conditions were treated with continual submergence for 7 days as extended hypoxia, or semi-diurnal cyclic submergence and reoxygenation for 7 days. At specific time points, leaves were collected to construct RNA-Sequencing libraries for gene expression analysis. Through the lens of transcriptome, the initial response of A. marina to submergence was mild but more dramatic after prolong immersion. However, the initial response of K. obovata was drastic and reduced in latitude later, suggesting distinct species-specific responses. After adapting to diurnal cycles, both species minimized transcriptome fluctuations similarly. Metabolically, during initial response, sucrose and starch were converted into glucose for fermentation to increase glycolytic flux, coupled with regeneration of NAD⁺. The energy amelioration was accompanied by longer term phytohormone regulations where ethylene signal transduction pathway was enhanced, but abscisic acid biosynthesis was reduced. Notably, gibberellic acids biosynthesis increased in A. marina but decreased in K. obovata as a unique feature. Genomic level analysis indicated that only about 30 % of the conserved plant submergence responsive genes were expressed during submergence in these mangroves. The function of an ethylene responsive gene was validated in transgenic Arabidopsis. This research elucidates distinct molecular mechanisms and metabolic pathways that empower A. marina and K. obovata to endure prolonged submergence and hypoxia. By highlighting their unique adaptive strategies in response to rising sea levels, these findings enhance our understanding of mangrove resilience and provide insights for the conservation and management of these essential coastal ecosystems in the face of climate change.

Keywords: Ethylene response factor; Flooding response; Hypoxia; Mangroves; Reoxygenation stress; Sea level rise.