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.
Highlights
Mangroves are a group of biogeographically and taxonomically diverse halophytes, predominantly trees that dominate tropical intertidal zones and estuaries (Tomlinson, 1986; Dassanayake et al, 2009)
The results showed that in Rhizophoraceae, the earliest divergence was between mangrove and nonmangrove (Carallia, Ca. brachiata) species (∼56.43 million years ago (Mya), 95% CI: 52.5–61.1 Mya); in the mangrove taxa, Bruguiera (B. gymnorrhiza) diverged first 38.68 Mya, followed by Rhizophora (R. apiculata) 36.47 Mya, while the two sister genera Ceriops (Ce. tagal) and Kandelia (K. obovata) diverged ∼28.31 Mya (Figure 1A)
Dassanayake et al (2009) compared the transcriptomes of two mangrove species, Rhizophora mangle and Heritiera littoralis, with two model terrestrial species, A. thaliana and P. trichocarpa. Their results strongly favored the interpretation that convergent evolution played a role at the transcriptome level in two diverse species that evolved separately to fit a common habitat, based on unusual similarities observed in the two mangrove transcriptome profiles
Summary
Mangroves are a group of biogeographically and taxonomically diverse halophytes, predominantly trees that dominate tropical intertidal zones and estuaries (Tomlinson, 1986; Dassanayake et al, 2009). Mangrove habitats are extreme environments characterized by high salinity, flooding, hypoxia, wind, and high ultraviolet (UV) radiation in typically resource-poor conditions (Tomlinson, 1986; Cheeseman et al, 1991). Mangroves are a valuable resource for understanding and exploiting plant adaptation to extreme environments (Dassanayake et al, 2009, 2010). With a multitude of structural adaptations reflecting responses to common environmental constraints, the mangrove community exemplifies one of the stronger cases for convergent evolution in the plant kingdom (Tomlinson, 1986; Ellison et al, 1999). Studies based on fossils and phylogenetic analysis have suggested that the diverse mangrove genera are of independent origin in different geologic epochs (Shi et al, 2005; Ricklefs et al, 2006). The exact phylogenetic position, divergence time, and species radiation within genera and families are still unclear and are of great interest to many botanists
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