Genomic insights into molecular adaptation to intertidal environments in the mangrove Aegiceras corniculatum

Abstract

Summary Mangroves have colonised extreme intertidal environments characterised by high salinity, hypoxia and other abiotic stresses. Aegiceras corniculatum, a pioneer mangrove species that has evolved two specialised adaptive traits (salt secretion and crypto‐vivipary) is an attractive ecological model to investigate molecular mechanisms underlying adaptation to intertidal environments. We assembled de novo a high‐quality reference genome of A. corniculatum and performed comparative genomic and transcriptomic analyses to investigate molecular mechanisms underlying adaptation to intertidal environments. We provide evidence that A. corniculatum experienced a whole‐genome duplication (WGD) event c. 35 Ma. We infer that maintenance of cellular environmental homeostasis is an important adaptive process in A. corniculatum. The 14‐3‐3 and H+‐ATPase protein‐coding genes, essential for the salt homeostasis, were preferentially retained after the recent WGD event. Using comparative transcriptomics, we show that genes upregulated under high‐salt conditions are involved in salt transport and ROS scavenging. We also found that all homologues of DELAY OF GERMINATION1 (DOG1) had lost their heme‐binding ability in A. corniculatum, and that this may contribute to crypto‐vivipary. Our study provides insight into the genomic correlates of phenotypic adaptation to intertidal environments. This could contribute not only within the genomics community, but also to the field of plant evolution.

Genetic and molecular mechanisms underlying mangrove adaptations to intertidal environments

“…The convergent evolution reduces genome size by optimizing the number of genes specific for adaptive pathways as exemplified by pathogen resistant gene families ( He et al., 2020 ; Losos, 2011 ). Genetic similarity between different mangrove species such as Avicennia marina and A. corniculatum also shows convergent evolution of mangroves ( Feng et al., 2021 ; Xu et al., 2020 ). Whole genome sequencing of mangroves revealed two noteworthy genomic convergences viz.…”

“…This event is known to have led to the divergence of mangroves from its terrestrial Rhizophoraceae ancestor family ( Guo et al., 2017 ). Similarly, phylogenetic analysis on Aegiceras corniculatum and Kandelia obovata genome indicated the WGD event as a turning point in adaptive evolution and mangrove emergence from Myrsinaceae and Rhizophoraceae, respectively ( Feng et al., 2021 ; Hu et al., 2020 ). WGD is often followed by fractionation by which most of the gene duplicates created are lost.…”

“…Interestingly, duplicated genes retained after fractionation may acquire novel functions or contribute to stress tolerance mechanisms, thereby giving a survival advantage to the plants ( Panchy et al., 2016 ). The genes coding for H + ATPase and 14-3-3 regulatory proteins are the gene duplicates in A. corniculatum that are responsible for development of adaptation to intertidal zones ( Feng et al., 2021 ). The retained genes are mostly involved in protein phosphorylation, ion transport, transcriptional regulation, energy metabolism, and signal transduction pathways ( Feng et al., 2020 , 2021 ).…”

“…The genes coding for H + ATPase and 14-3-3 regulatory proteins are the gene duplicates in A. corniculatum that are responsible for development of adaptation to intertidal zones ( Feng et al., 2021 ). The retained genes are mostly involved in protein phosphorylation, ion transport, transcriptional regulation, energy metabolism, and signal transduction pathways ( Feng et al., 2020 , 2021 ).…”

The First De Novo Transcriptome Assembly and Transcriptomic Dynamics of the Mangrove Tree Rhizophora stylosa Griff. (Rhizophoraceae)

“…Nevertheless, research about mangroves is still rare, and the molecular mechanisms underlying their high adaptability to coastal zone is not well understood, mostly because of unavailability of genome references for these species. To this date, among more than 80 mangrove species, only four of them have had their genome assembled [ 12 , 13 , 14 , 15 ]. De novo RNA sequencing (RNA-Seq) and transcriptome assembly is a helpful and compromising way to study transcriptional profile and gene expression of non-model plants, with no available reference genome [ 16 ].…”