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

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.