Comparative transcriptome analysis on the mangrove Acanthus ilicifolius and its two terrestrial relatives provides insights into adaptation to intertidal habitats.

ABSTRACT

Acanthus is a unique genus covering both mangroves and terrestrial species, and thus is an ideal system to comparatively analyze the mechanisms of mangrove adaptation to intertidal habitats. We performed RNA sequencing of the mangrove plant Acanthus ilicifolius and its two terrestrial relatives, Acanthus leucostachyus and Acanthus mollis. A total of 91,125, 118,290, and 141,640 unigenes were obtained. Simple sequence repeats (SSR) analysis showed that A. ilicifolius had more SSRs, the highest frequency of distribution, and higher in polymorphism potential compared to the two terrestrial relatives. Phylogenetic analyses suggested a relatively recent split between A. ilicifolius and A. leucostachyus, i.e., about 16.76 million years ago (Mya), after their ancestor divergence with A. mollis (32.11 Mya), indicating that speciation of three Acanthus species occurred in the Early to Middle Miocene. Gene Ontology (GO) enrichment revealed that the unique unigenes in A. ilicifolius are predominantly related to rhythmic process, reproductive process and response to stimuli. The accelerated evolution and positive selection analyses indicated that the genus Acanthus migrated from terrestrial to intertidal habitats, where 311 pairs may be under positive selection. Functional enrichment analysis revealed that these genes associated with essential metabolism and biosynthetic pathways such as oxidative phosphorylation, plant hormone signal transduction, photosynthetic carbon fixation and arginine and proline metabolism, are related to the adaptation of A. ilicifolius to intertidal habitats, which are characterized by high salinity and hypoxia. Our results indicate the evolutionary processes and the mechanisms underlying the adaptability of Acanthus to various harsh environments from the arid terrestrial to intertidal habitats.