Comparative Analysis of Transcriptomes in Rhizophoraceae Provides Insights into the Origin and Adaptive Evolution of Mangrove Plants in Intertidal Environments

Abstract

Mangroves are woody plants that grow at the interface between land and sea in tropical and subtropical latitudes, where they exist in conditions of high salinity, extreme tides, strong winds, high temperatures, and muddy, anaerobic soils. Rhizophoraceae is a key mangrove family, with highly developed morphological and physiological adaptations to extreme conditions. It is an ideal system for the study of the origin and adaptive evolution of mangrove plants. In this study, we characterized and comprehensively compared the transcriptomes of four mangrove species, from all four mangrove genera, as well as their closest terrestrial relative in Rhizophoraceae, using RNA-Seq. We obtained 41,936–48,845 unigenes with N50 values of 982–1,185 bp and 61.42–69.48% annotated for the five species in Rhizophoraceae. Orthology annotations of Gene Ontology, Kyoto Encyclopedia of Genes and Genomes, and Clusters of Orthologous Groups revealed overall similarities in the transcriptome profiles among the five species, whereas enrichment analysis identified remarkable genomic characteristics that are conserved across the four mangrove species but differ from their terrestrial relative. Based on 1,816 identified orthologs, phylogeny analysis and divergence time estimation revealed a single origin for mangrove species in Rhizophoraceae, which diverged from the terrestrial lineage ~56.4 million years ago (Mya), suggesting that the transgression during the Paleocene–Eocene Thermal Maximum may have been responsible for the entry of the mangrove lineage of Rhizophoraceae into intertidal environments. Evidence showed that the ancestor of Rhizophoraceae may have experienced a whole genome duplication event ~74.6 Mya, which may have increased the adaptability and survival chances of Rhizophoraceae during and following the Cretaceous–Tertiary extinction. The analysis of positive selection identified 10 positively selected genes from the ancestor branch of Rhizophoraceae mangroves, which were mainly associated with stress response, embryo development, and regulation of gene expression. Positive selection of these genes may be crucial for increasing the capability of stress tolerance (i.e., defense against salt and oxidative stress) and development of adaptive traits (i.e., vivipary) of Rhizophoraceae mangroves, and thus plays an important role in their adaptation to the stressful intertidal environments.

A general framework for propagule dispersal in mangroves

“…Mangroves comprise a group of terrestrially derived coastal shoreline plants suggested to have evolved around the Tethys Sea during the late Cretaceous to Paleocene–Eocene (Ellison, Farnsworth & Merkt, ). Recently, Guo et al () reported a post‐Cretaceous–Paleogene boundary divergence of the mangrove clade from the terrestrial lineage within Rhizophoraceae. The mangrove ferns of the genus Acrostichum may have evolved and diverged from a terrestrial lineage in the late Cretaceous and are suggested to be among the oldest members of the mangrove ecosystem (Zhang et al , ).…”

Transcriptome analysis of two radiated Cycas species and the subsequent species delimitation of the Cycas taiwaniana complex

“…The overall annotation rates for the two Cycas species studied here, C. hainanensis and C. changjiangensis , were not very high, with only about half of the unigenes annotated using the Nr (45% in C. hainanensis , 52% in C. changjiangensis ) and KOG (42% in C. hainanensis , 48% in C. changjiangensis ) databases. This may be due to the low representation of gymnosperm species in the available annotation databases (Li et al., ), although a small proportion of unannotated genes might be Cycas ‐specific genes associated with certain genus‐specific characteristics (Mao et al., ; Guo et al., ). The high level of similarity between the GO categories associated with the C. changjiangensis and C. hainanensis unigenes might suggest a conserved gene repertoire for these species, and also indicates their very recent divergence (Yang et al., ).…”

“…Cycas hainanensis grows well in thick forests with high temperatures and wet substrates, whereas C. changjiangensis is mainly distributed on bare rock in arid conditions. These differences in the microhabitats of these two Cycas species suggests that natural selection may be the major force that has driven their divergence and evolution (Guo et al., ). The pattern of selective pressures across a genome may therefore be useful for making inferences about adaptive evolution (Kunstner et al., ; Siol et al., ).…”

Evolutionary and ecological functional genomics, from lab to the wild

“…There has also been more work probing adaptation to harsh and unconventional environments including elevated mountain areas (Yang et al ., ; Jia et al ., ), inter‐tidal mangrove areas (Yang et al ., ; Guo et al ., ), and even the Antarctic (Cho et al ., ). In the case of biotic interactions, field transcriptomes have been sequenced from microbial plant colonizers and the plant host in tandem in a dual RNA‐seq approach (Hubbard et al ., ; Kamitani et al ., ).…”