Abstract

Mangroves invade some very marginal habitats for woody plants-at the interface between land and sea. Since mangroves anchor tropical coastal communities globally, their origin, diversification and adaptation are of scientific significance, particularly at a time of global climate change. In this study, a combination of single-molecule long reads and the more conventional short reads are generated from Rhizophora apiculata for the de novo assembly of its genome to a near chromosome level. The longest scaffold, N50 and N90 for the R. apiculata genome, are 13.3 Mb, 5.4 Mb and 1.0 Mb, respectively. Short reads for the genomes and transcriptomes of eight related species are also generated. We find that the ancestor of Rhizophoreae experienced a whole-genome duplication ~70 Myrs ago, which is followed rather quickly by colonization and species diversification. Mangroves exhibit pan-exome modifications of amino acid (AA) usage as well as unusual AA substitutions among closely related species. The usage and substitution of AAs, unique among plants surveyed, is correlated with the rapid evolution of proteins in mangroves. A small subset of these substitutions is associated with mangroves' highly specialized traits (vivipary and red bark) thought to be adaptive in the intertidal habitats. Despite the many adaptive features, mangroves are among the least genetically diverse plants, likely the result of continual habitat turnovers caused by repeated rises and falls of sea level in the geologically recent past. Mangrove genomes thus inform about their past evolutionary success as well as portend a possibly difficult future.

Highlights

  • One of the most productive and diverse environments for many life forms is at the interface between land and sea

  • No more than 80 tree species have succeeded in invading intertidal zones to become mangroves, compared to over 10 000 that are found at the land–water interface in non-saline systems. (The term ‘mangrove’ refers to many independently evolved lineages of woody plants that occupy these land/saltwater interfaces.) Remarkably, the small number of mangrove species anchors tropical intertidal communities globally by providing key ecological services that include carbon sequestration [1], sediment accretion, seashore protection and ecosystem productivity [2]

  • Using a maximumlikelihood method implemented in the CAFE software [46], we identify 112 gene families that have expanded in R. apiculata during recent evolution (Supplementary Figs 20 and 21, available as Supplementary Data at NSR online)

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Summary

INTRODUCTION

One of the most productive and diverse environments for many life forms is at the interface between land and sea. We searched for adaptive signals in a set of genes involved in salt tolerance and flavonoid biosynthesis by analysing transcriptome profiles under different salt concentrations (see Supplementary Note and Supplementary Figs 16–18, available as Supplementary Data at NSR online). An interesting gene is Dihydroflavonol reductase B [DFR(B)], which is often lost in other taxa but is expressed at an elevated level in Rhizophora in high-salt environments (Supplementary Fig. 19, available as Supplementary Data at NSR online). Using a maximumlikelihood method implemented in the CAFE software [46], we identify 112 gene families that have expanded in R. apiculata during recent evolution (Supplementary Figs 20 and 21, available as Supplementary Data at NSR online). Many of these genes are in the category of ‘response to chemical stimulus’ (Supplementary Table 21, available as Supplementary Data at NSR online)

DISCUSSION
ONLINE METHODS
Findings
Tomlinson P The Botany of Mangroves Cambridge

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