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In China, Dolichandrone spathacea is a rare and endangered semi-mangrove plant species with an extremely small population, naturally distributed only in Zhanjiang City and the east coast of Hainan Island. Despite conservation concerns, the population status of D. spathacea has received little scientific attention. In this study, we evaluated the current status of D. spathacea on Hainan Island, China, in order to propose sustainable conservation strategies for future ecological restoration of its natural population. D. spathacea on Hainan Island can be divided into four populations. All the D. spathacea populations present a state of overall dispersion, local concentration, and occasionally sporadic existence, and they exist in geographical isolation. The young, middle, and old D. spathacea plants account for 20.42%, 66.20%, and 13.38%, respectively, indicating that the D. spathacea population on Hainan Island is declining. Furthermore, instead of temporal structure, we used diameter at breast height (DBH) to establish a static life table, draw a population survival curve, and quantify the future development trend through population dynamic analysis and time-series prediction. These results suggest that the D. spathacea population in the Bamen Gulf (Wenchang) and Qingmei Harbor (Sanya) on Hainan Island is sensitive to external disturbances and possesses two main increases in mortality rate—namely, in its juvenile and mature stages—due to competition and anthropogenic interferences, which might be the most important reasons for its endangered status. Depending on the current conditions of the D. spathacea population, we should conserve and expand mature trees in situ, preserve their germplasm resources, rehabilitate their habitats to promote provenance restoration, and conduct artificial cultivation and spreading planting in order to realize the sustainable conservation and management of D. spathacea. [ABSTRACT FROM AUTHOR]

Nypa fruticans (Wurmb), a mangrove palm species with origins dating back to the Late Cretaceous period, is a unique species for investigating long‐term adaptation strategies to intertidal environments and the early evolution of palms. Here, we present a chromosome‐level genome sequence and assembly for N. fruticans. We integrated the genomes of N. fruticans and other palm family members for a comparative genomic analysis, which confirmed that the common ancestor of all palms experienced a whole‐genome duplication event around 89 million years ago, shaping the distinctive characteristics observed in this clade. We also inferred a low mutation rate for the N. fruticans genome, which underwent strong purifying selection and evolved slowly, thus contributing to its stability over a long evolutionary period. Moreover, ancient duplicates were preferentially retained, with critical genes having experienced positive selection, enhancing waterlogging tolerance in N. fruticans. Furthermore, we discovered that the pseudogenization of Early Methionine‐labelled 1 (EM1) and EM6 in N. fruticans underly its crypto‐vivipary characteristics, reflecting its intertidal adaptation. Our study provides valuable genomic insights into the evolutionary history, genome stability, and adaptive evolution of the mangrove palm. Our results also shed light on the long‐term adaptation of this species and contribute to our understanding of the evolutionary dynamics in the palm family. [ABSTRACT FROM AUTHOR]

Although gene loss is common in evolution, it remains unclear whether it is an adaptive process. In a survey of seven major mangrove clades that are woody plants in the intertidal zones of daily environmental perturbations, we noticed that they generally evolved reduced gene numbers. We then focused on the largest clade of Rhizophoreae and observed the continual gene set reduction in each of the eight species. A great majority of gene losses are concentrated on environmental interaction processes, presumably to cope with the constant fluctuations in the tidal environments. Genes of the general processes for woody plants are largely retained. In particular, fewer gene losses are found in physiological traits such as viviparous seeds, high salinity, and high tannin content. Given the broad and continual genome reductions, we propose the May–Wigner theory (MWT) of system stability as a possible mechanism. In MWT, the most effective solution for buffering continual perturbations is to reduce the size of the system (or to weaken the total genic interactions). Mangroves are unique as immovable inhabitants of the compound environments in the land–sea interface, where environmental gradients (such as salinity) fluctuate constantly, often drastically. Extending MWT to gene regulatory network (GRN), computer simulations and transcriptome analyses support the stabilizing effects of smaller gene sets in mangroves vis-à-vis inland plants. In summary, we show the adaptive significance of gene losses in mangrove plants, including the specific role of promoting phenotype innovation and a general role in stabilizing GRN in unstable environments as predicted by MWT. [ABSTRACT FROM AUTHOR]

How plants adapt and diverge in extreme environments is a key question of plant evolution and ecology. Mangrove invasion of intertidal environments is facilitated by adaptive phenotypes such as aerial roots, salt‐secreting leaf, and viviparity, and genomic mechanisms including whole genome duplication and transposable element number reduction. However, a number of mangroves lack these typical phenotypes. The question we ask is whether these phenotypically atypical mangroves also have distinct genomic features? The sibling mangrove species Lumnitzera littorea and Lumnitzera racemosa provide a model to study this question. We sequenced and assembled their genomes to chromosome level, together with a closely related species Combretum micranthum. While most mangroves have small genomes, the genomes of both Lumnitzera species are large (1443 and 1317 Mb) and carry a high proportion of repeat sequences (~75%). Moreover, Lumnitzera species have not undergone post‐gamma whole‐genome duplications. Their genome size increased mainly due to the expansion of repeat sequences in their ancestors. However, Lumnitzera genomes have reduced transposable elements by constraining the proliferation of new LTR‐RTs. Meanwhile, the two species have more gene families contracted than expanded, and some gene families with reversed size change may underlie their differentiation in root morphology and local distribution. We identified 86 chromosomal inversions, five of which are measured between 6.5 and 12.8 megabases. A number of genes located in these inversions function in pigment biosynthesis, a process likely involved in flower colour differentiation between the Lumnitzera species. We conclude that the mangroves with atypical phenotypes also have atypical genomic evolution. [ABSTRACT FROM AUTHOR]

Whole‐genome duplication (WGD) is believed to increase the chance of adaptation to a new environment. This conjecture may apply particularly well to new environments that are not only different but also more variable than ancestral habitats. One such prominent environment is the interface between land and sea, which has been invaded by woody plants, collectively referred as mangroves, multiple times. Here, we use two distantly related mangrove species (Avicennia marina and Rhizophora apiculata) to explore the effects of WGD on the adaptive process. We found that a high proportion of duplicated genes retained after WGD have acquired derived differential expression in response to salt gradient treatment. The WGD duplicates differentially expressed in at least one copy usually (>90%) diverge from their paralogues' expression profiles. Furthermore, both species evolved in parallel to have one paralogue expressed at a high level in both fresh water and hypersaline conditions but at a lower level at medium salinity. The pattern contrasts with the conventional view of monotone increase/decrease as salinity increases. Differentially expressed copies have thus probably acquired a new role in salinity tolerance. Our results indicate that the WGD duplicates may have evolved to function collaboratively in coping with different salinity levels, rather than specializing in the intermediate salinity optimal for mangrove plants. In conclusion, WGD and the retained duplicates appear to be an effective solution for adaptation to new and unstable environments. see also the Perspective by Shawn K. Thomas, Hong An and J. Chris Pires [ABSTRACT FROM AUTHOR]

SUMMARY: Adaptation to new environments is a key evolutionary process which presumably involves complex genomic changes. Mangroves, a collection of approximately 80 woody plants that have independently invaded intertidal zones >20 times, are ideal for studying this process. We assembled near‐chromosome‐scale genomes of three Xylocarpus species as well as an outgroup species using single‐molecule real‐time sequencing. Phylogenomic analysis reveals two separate lineages, one with the mangrove Xylocarpus granatum and the other comprising a mangrove Xylocarpus moluccensis and a terrestrial Xylocarpus rumphii. In conjunction with previous studies, we identified several genomic features associated with mangroves: (i) signals of positive selection in genes related to salt tolerance and root development; (ii) genome‐wide elevated ratios of non‐synonymous to synonymous substitution relative to terrestrial relatives; and (iii) active elimination of long terminal repeats. These features are found in the terrestrial X. rumphii in addition to the two mangroves. These genomic features, not being strictly mangrove‐specific, are hence considered pre‐adaptive. We infer that the coastal but non‐intertidal habitat of X. rumphii may have predisposed the common ancestor to invasion of true mangrove habitats. Other features including the preferential retention of duplicated genes and intolerance to pseudogenization are not found in X. rumphii and are likely true adaptive features in mangroves. In conclusion, by studying adaptive shift and partial shifts among closely related species, we set up a framework to study genomic features that are acquired at different stages of the pre‐adaptation and adaptation to new environments. Significance Statement: We sequenced and assembled high‐quality genomes for three Xylocarpus species and one Swietenia species using single‐molecule real‐time sequencing. By illustrating genomic features acquired in different stages of the complex process of adapting to the extreme intertidal environments, we provide evidences for pre‐adaptation and adaptation in different stages of transition to a new environment [ABSTRACT FROM AUTHOR]

Historic climate changes drive geographical populations of coastal plants to contract and recover dynamically, even die out completely. Species suffering from such bottlenecks usually lose intraspecific genetic diversity, but how do these events influence population subdivision patterns of coastal plants? Here, we investigated this question in the typical coastal plant: mangrove species Aegiceras corniculatum. Inhabiting the intertidal zone of the tropical and subtropical coast of the Indo‐West Pacific oceans, its populations are deemed to be greatly shaped by historic sea‐level fluctuations. Using dual methods of Sanger and Illumina sequencing, we found that the 18 sampled populations were structured into two groups, namely, the "Indo‐Malayan" group, comprising three subgroups (the northern South China Sea, Gulf of Bengal, and Bali), and the "Pan‐Australasia" group, comprising the subgroups of the southern South China Sea and Australasia. Based on the approximate Bayesian computations and Stairway Plot, we inferred that the southern South China Sea subgroup, which penetrates the interior of the "Indo‐Malayan" group, originated from the Australasia subgroup, accompanied by a severe bottleneck event, with a spot of gene flow from both the Australasia and "Indo‐Malayan" groups. Geographical barriers such as the Sundaland underlie the genetic break between Indian and Pacific Oceans, but the discontinuity between southern and northern South China Sea was originated from genetic drift in the bottleneck event. Hence, we revealed a case evidencing that the bottleneck event promoted population subdivision. This conclusion may be applicable in other taxa beyond coastal plants. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Sequencing multiple species that share the same ecological niche may be a new frontier for genomic studies. While such studies should shed light on molecular convergence, genomic-level analyses have been unsuccessful, due mainly to the absence of empirical controls. Woody plant species that colonized the global tropical coasts, collectively referred to as mangroves, are ideal for convergence studies. Here, we sequenced the genomes/transcriptomes of 16 species belonging in three major mangrove clades. To detect convergence in a large phylogeny, a CCS+ model is implemented, extending the more limited CCS method (convergence at conservative sites). Using the empirical control for reference, the CCS+ model reduces the noises drastically, thus permitting the identification of 73 convergent genes with P true (probability of true convergence) > 0.9. Products of the convergent genes tend to be on the plasma membrane associated with salinity tolerance. Importantly, convergence is more often manifested at a higher level than at amino-acid (AA) sites. Relative to >50 plant species, mangroves strongly prefer 4 AAs and avoid 5 others across the genome. AA substitutions between mangrove species strongly reflect these tendencies. In conclusion, the selection of taxa, the number of species and, in particular, the empirical control are all crucial for detecting genome-wide convergence. We believe this large study of mangroves is the first successful attempt at detecting genome-wide site convergence. [ABSTRACT FROM AUTHOR]

Allopatric speciation requiring an unbroken period of geographical isolation has been the standard model of neo-Darwinism. While doubts have been repeatedly raised, strict allopatry without any gene flow remains a plausible mechanism in most cases. To rigorously reject strict allopatry, genomic sequences superimposed on the geological records of a well-delineated geographical barrier are necessary. The Strait of Malacca, narrowly connecting the Pacific and Indian Ocean coasts, serves at different times either as a geographical barrier or a conduit of gene flow for coastal/marine species. We surveyed 1700 plants from 29 populations of 5 common mangrove species by large-scale DNA sequencing and added several whole-genome assemblies. Speciation between the two oceans is driven by cycles of isolation and gene flow due to the fluctuations in sea level leading to the opening/closing of the Strait to ocean currents. Because the time required for speciation in mangroves is longer than the isolation phases, speciation in these mangroves has proceeded through many cycles of mixing-isolation-mixing, or MIM, cycles. The MIM mechanism, by relaxing the condition of no gene flow, can promote speciation in many more geographical features than strict allopatry can. Finally, the MIM mechanism of speciation is also efficient, potentially yielding m n (m  > 1) species after n cycles. [ABSTRACT FROM AUTHOR]

Aim Population genomics data were used to determine the genetic diversity, genetic divergence and genetic structure of the mangrove, Rhizophora apiculata, across its distributional range and to re-assess the evolutionary processes that shaped its current distribution. Location The Indo-Malesian region section of the Indo-West Pacific region. Methods Next-generation sequencing technology was used to sequence 81 nuclear loci from a pooled DNA sample of 31-44 individuals of Rhizophora apiculata from 11 populations. Five nuclear loci from six to eight individuals from 18 populations were sequenced using conventional Sanger sequencing technology to validate the results. Results Genetic diversity at the population level was low (π and θ were < 1.0 × 10−3 in most of the populations), but relatively high at the species level (π = 2.419 × 10−3 and θ = 1.362 × 10−3). The populations of R. apiculata in the Indo-Malesian region were genetically differentiated and grouped into three clusters: east Indian Ocean ( EIO), South China Sea ( SCS) and Australasia ( AUA). Based on the genetic distance matrices, two genetic discontinuities were observed, and they correspond to the Malay Peninsula land barrier and the Wallacea zone. The admixture observed in populations from the Malacca Strait was attributed to asymmetric gene flow through the strait, which was simulated by the isolation-with-migration ( IM) model. Main conclusion Both the Sunda shelf barrier and ocean currents in Wallacea contributed to the observed genetic discontinuity, which separated R. apiculata into three clusters ( SCS, EIO and AUA). The cycle between extinction and recolonization in the SCS in response to Pleistocene sea level fluctuations reduced the genetic diversity within populations. The repeated opening and closing of the gene flow corridors, such as the Malacca Strait, may have blurred the genetic discontinuities to an extent and introduced an admixture into populations in boundary areas. [ABSTRACT FROM AUTHOR]

Aegiceras corniculatum (L.) Blanco is one of the most salt tolerant mangrove species and can thrive in 3% salinity at the seaward edge of mangrove forests. Here we sequenced the transcriptome of A. corniculatum used Illumina GA platform to develop its genomic resources for ecological and evolutionary studies. We obtained about 50 million high-quality paired-end reads with 75 bp in length. Using the short read assembler Velvet, we yielded 49,437 contigs with the average length of 625 bp. A total of 32,744 (66.23%) contigs showed significant similarity to the GenBank non-redundant (NR) protein database. 30,911 and 18,004 of these sequences were assigned to Gene Ontology and eukaryotic orthologous groups of proteins (KOG). A total of 4942 transcripts from our assemblies had significant similarity with KEGG Orthologs and were involved in 144 KEGG pathways, while 9899 unigenes had enzyme commission (EC) numbers. In addition, 9792 transcriptome-derived SSRs were identified from 7342 sequences. With our strict criteria, 4165 candidate SNPs were also identified from 2058 contigs. Some of these SNPs were further validated by Sanger sequencing. Genomic resources generated in this study should be valuable in ecological, evolutionary, and functional genomics studies for this mangrove species. [ABSTRACT FROM AUTHOR]