Mangrove forests are natural laboratories for studying epigenetic and climate change. 1-4 Mangroves are salt-tolerant plant species that grow in coastal saline water and are adapted to harsh environmental conditions such as high ultraviolet light, low nutrition, and fluctuating salinity in coastal zones. They are highly productive and biologically diverse wetlands that serve as nurseries and habitats to many juvenile fishes, mollusks, and crustaceans like shrimps. Some mangroves began disappearing due to ozone depletion, freshwater diversion, ocean acidification, atmospheric aerosol pollution, and the introduction of exotic chemicals and modified organisms in the shrimp farms nearby mangrove habitats. Mangroves sequester large quantities of carbon that become significant sources of greenhouse gases when disturbed through land-use change. They also support diverse species of microorganisms such as fungi, and bacteria associated with biogeochemical transformations of nutrients. They trap sediments and assimilate nutrients along with associated sediment contaminants such as antibiotics and endocrine disrupting chemicals (EDCs) like metals, PCBs, PAHs, bisphenols, and glyphosate-based herbicides, among others. Mangrove species are known to have very low genetic diversity caused by their stressful living conditions, suggesting that epigenetic variation is likely a vital source for them to respond to environmental changes. The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and nongenetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the nongenetic contributions to variation. 1-4
Epigenetic modifications, such as cytosine methylation, are inherited in plant species and may occur in response to biotic or abiotic stress, affecting gene expression without changing genome sequence. The long-term goal of the MangroveENCODE project of the FUCOBI Foundation of Ecuador is to study the epigenetic mechanisms associated with the interactions of CO2 uptake, EDCs in sentinel species (shellfish), and microbial communities considering environmental degradation-related health issues. The plan is to obtain baseline information for future studies to test mechanism-driven hypotheses to examine the interactions of CO2, EDCs, and microbial diversity using computational ecology tools. The short-term goals include characterization of the microbiome (bacterial communities), CO2 uptake, and EDC concentrations in mangrove sediment and shrimp. This mini review provides an overview of available studies on epigenetic regulation and adaptation of mangroves and summarizes (a) the best technologies to assess the microbiome and CO2 stocks from >1-meter-deep mangrove sediment, and (b) the genome sizes, microbiomes, and transposable elements of mangroves. For example, availability of the genome assembly and in natura epigenome analyses of Bruguiera gymnorhiza, one of the dominant mangrove species, allowed genome‐guided transcriptome assembly for mangrove species. 1-2 The 309-Mb of the genome, predicted to encode 34,403 genes, has a repeat content of 48%. Depending on its growing environment, the natural B. gymnorhiza population showed drastic morphological changes associated with expression changes in thousands of genes. Moreover, high‐salinity environments induced genome‐wide DNA hypermethylation of transposable elements (TEs) in the B. gymnorhiza. DNA hypermethylation was concurrent with the transcriptional regulation of chromatin modifier genes, suggesting robust epigenome regulation of TEs in the B. gymnorhiza genome under high‐salinity environments. The genome and epigenome data provided novel insights into the epigenome regulation of mangroves and a better understanding of the adaptation of plants to fluctuating, harsh natural environments.
Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions and is potentially threatened by anthropogenic environmental changes. 3 Researchers studied (a) the levels of genetic and epigenetic diversity in natural populations of R. mangle, (b) how genetic and epigenetic variation are structured within and among populations, and (c) how faithfully epigenetic variation is inherited. They found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field and epigenetic differences among offspring grown in common gardens were explained by maternal family. It shows epigenetic variation could be an important source of response to challenging environments in populations of this foundation species.
Laguncularia racemosa occurs in naturally contrasting habitats where it is subjected daily to salinity and nutrient variations leading to morphological differences. 4 Researchers unraveled how CpG-methylation variation is distributed among individuals from two nearby habitats, at a riverside (RS) or near a salt marsh (SM), with different environmental pressures and how this variation is correlated with the observed morphological variation. Significant differences were observed in morphological traits such as tree height, tree diameter, leaf width and leaf area between plants from RS and SM locations, resulting in smaller plants and smaller leaf size in SM plants. Genetic and epigenetic (CpG-methylation) variation in genomes from these populations revealed that SM plants were hypomethylated (14.6% of loci had methylated samples) in comparison to RS (32.1% of loci had methylated samples). Within-population diversity was significantly greater for epigenetic than genetic data in both locations, but SM also had less epigenetic diversity than RS, and significantly greater differentiation among locations for epigenetic than genetic data. Individuals with similar genetic profiles presented divergent epigenetic profiles that were characteristic of the population in a particular environment, suggesting that CpG-methylation changes may be associated with environmental heterogeneity, suggesting epigenetic variation in natural populations play an important role in helping individuals to cope with different environments.
References
1. Miryeganeh M, Marlétaz F, Gavriouchkina D, Saze H. 2022. De novo genome assembly and in natura epigenomics reveal salinity-induced DNA methylation in the mangrove tree Bruguiera gymnorhiza. New Phytol. 2022 Mar;233(5):2094-2110. doi: 10.1111/nph.17738.
2. Miryeganeh M. and Saze H. 2021. The First De Novo Transcriptome Assembly and Transcriptomic Dynamics of the Mangrove Tree Rhizophora stylosa Griff. (Rhizophoraceae). Int J Mol Sci. 22(21):11964. doi: 10.3390/ijms222111964.
3. Mounger J, Boquete, MT, Schmid, M.W. et al. 2021. Inheritance of DNA methylation differences in the mangrove Rhizophora mangle. Evol. Dev. 23(4):351-374. doi: 10.1111/ede.12388. Epub 2021 Aug 12.
4. Lira-Medeiros CF, Parisod C, Avancini Fernandes R, et. al. 2010. Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One. 5(4):e10326. doi: 10.1371/journal.pone.0010326.