Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations

Abstract

The mangrove ecosystems are characterised by high salinity and hypoxia. When viviparous mangrove propagules detach from the mother plants and find a substratum, their roots must respond appropriately to the external environment. Therefore, for an improved understanding of the dynamics of mangrove adaptations to fluctuating intertidal habitats, root transcriptomic and anatomical responses of the germinated propagules of Rhizophora mucronata Lam. and Kandelia candel Druce were analysed. Both species had larger cortexes with aerenchyma spaces, and root cortical/stelar area decreased above five parts per thousand (ppt) of salinity treatment after 60 days. The percentage of suberised endodermal cells in R. mucronata was above 80%, while it increased in K. candel after 60 days of treatment. De novo transcriptome sequencing of K. candel and R. mucronata at 45 and 60 days after salinity treatments identified 766,040 and 558,190 transcripts with predicted open reading frames, respectively, and differential gene expression analysis unveiled ~ 16,000 salt-responsive transcripts. Gene ontology analysis showed enrichment of transcripts related to cell wall biosynthesis (cellulose synthase, expansins), membrane transporters (aquaporins, salt overly sensitive 1, vacuolar ATPase), and hormone signal transduction (delay of germination 1 domain-containing protein, auxin-responsive protein). Interestingly, the differentially expressed solute transporter protein transcripts were higher in K. candel than in R. mucronata. Pathway enrichment analysis revealed the significant expression of flavonoid/flavonol and taurine/hypotaurine biosynthesis pathways, indicating the role of specialised metabolites in stress response. A total of 10 differentially expressed transcripts were validated using qRT-PCR, and a positive correlation of 0.62 (K. candel) and 0.68 (R. mucronata) was observed between the RNA sequencing data and qRT-PCR. Overall, this study contributes to understanding mangrove ecological adaptations and stress response mechanisms to salinity stress in the early developing propagules.