Comparative transcriptome and metabolome analysis reveals the differential roles of aboveground and belowground pneumatophores in carbon, nitrogen, and sulfur metabolisms in the adaptation of Avicennia marina to coastal intertidal habitat

SUMMARY Avicennia marina is a dominant mangrove plant that inhabits coastal intertidal wetlands where are featured by low oxygen and nitrogen (N), but high sulfur (S). Its pneumatophore is a unique characteristic of its root system. To understand the roles of the pneumatophore in carbon (C), N, and S metabolisms for intertidal adaptation, we firstly compared the anatomy between aboveground pneumatophore (PA), belowground pneumatophore (PB) and feeding root. The photosynthetic oxygen evolution from PA was assayed by non‐invasive micro‐test technology, and the metabolisms of C, N, and S between PA and PB were comparatively analyzed by transcriptome and metabolome approaches. The results illustrated that most genes related to photosynthetic C assimilation and S reduction were significantly up‐regulated in PA, while genes associated with N uptake, transport, and reduction were significantly up‐regulated in PB. Additionally, the expression level of the gene for sulfite oxidase was up‐regulated in PA, indicating a tight regulation of S assimilation by PA. Importantly, our findings revealed that key reductases for both S and N assimilation are ferredoxin‐dependent, with electrons supplied by the corticular photosynthesis in PA. Integrative multi‐omics analysis showed that methylthioadenosine (MTA) was negatively associated with genes related to serine and cysteine biosynthesis but positively connected with genes related to the Yang cycle. This suggests a pivotal role of MTA in coordinating C, N, S, and ethylene metabolism in pneumatophores. The overall results illustrate that the green cortex of PA functions analogously to a leaf, providing reductants and C skeletons for N and S metabolism while coordinating with ethylene metabolism. This facilitates the adaptation of A. marina pneumatophore to the intertidal habitat.