Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)

Abstract

Avicennia marina forests fulfill essential blue carbon and ecosystem services, including halting coastal erosion and supporting fisheries. Genetic studies of A. marina tissues could yield insight into halophyte adaptive strategies, empowering saline agriculture research. We compare transcriptomes from A. marina pneumatophores, stems, leaves, flowers, seeds, and transcriptomes across four widely divergent environments in the Indo-Pacific (Red Sea, Arabian Gulf, Bay of Bengal, and Red River Delta) to decipher the shared and location-, tissue-, and condition-specific functions. On average, 4.8% of transcripts per tissue were uniquely expressed in that tissue, and 12.2% were shared in all five tissues. Flowers’ transcript expression was the most distinct, with domain-centric gene ontology analysis showing high enrichment for stimulus-responsive processes, as well as genes implicated in flowering (hydroxygeraniol dehydrogenase, TPM = 3687) and floral scent biosynthesis (e.g., benzoyl_coenzyme_A, 2497.2 TPM). Pneumatophores highly expressed antioxidant genes, such as glutathione S-transferase (GST, TPM = 4759) and thioredoxin (TRX, TPM = 936.2), as well as proteins in the GO term ‘Hydroquinone:oxygen oxidoreductase activity’ (enrichment Z = 7.69, FDR-corr. p = 0.000785). Tissue-specific metabolic pathway reconstruction revealed unique processes in the five tissues; for example, seeds showed the most complete expression of lipid biosynthetic and degradation pathways. The leaf transcriptome had the lowest functional diversity among the expressed genes in any tissue, but highly expressed a catalase (TPM = 4181) and was enriched for the GO term ‘transmembrane transporter activity’ (GO:0015238; Z = 11.83; FDR-corr. p = 1.58 × 10−9), underscoring the genes for salt exporters. Metallothioneins (MTs) were the highest-expressed genes in all tissues from the cultivars of all locations; the dominant expression of these metal-binding and oxidative-stress control genes indicates they are essential for A. marina in its natural habitats. Our study yields insight into how A. marina tissue-specific gene expression supports halotolerance and other coastal adaptative strategies in this halophytic angiosperm.