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Dellaert, Z.

Publications and source records attributed to Dellaert, Z..

5 recordsLinked to original sources

Cross-talk among miRNAs, lncRNAs, and DNA methylation in three coral species reveal conserved epigenetic regulatory architecture

Epigenetic mechanisms support phenotypic plasticity across metazoans, enabling dynamic response to environmental change. DNA methylation and non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), regulate gene expression through distinct but interconnected mechanisms. In vertebrate systems, these layers form integrated networks in which specific miRNAs directly target the protein machinery of other epigenetic processes ("epi-miRNAs") and specialized lncRNAs act as competing endogenous RNAs (ceRNAs), sequestering miRNAs from their mRNA targets. Whether equivalent cross-layer regulatory architectures exist in cnidarians, whose methylomes are invertebrate-characteristic and whose miRNAs function mechanistically like those of plants, is unknown. Here we integrate matched RNA-seq, small RNA-seq, and whole-genome bisulfite sequencing across three species of reef-building coral (Acropora pulchra, Porites evermanni, and Pocillopora tuahiniensis) to characterize the landscape and regulatory interactions of microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and DNA methylation, including the first description of epi-miRNAs and ceRNA networks in cnidarian taxa. Across the study species, miRNAs putatively targeted transcripts encoding a suite of epigenetic processes, including DNA methylation regulators (TET3, MBD, PRDM14), ubiquitin-signaling and histone-modifying machinery, and components of the miRNA pathway itself (e.g., AGO, TNRC6). The conserved miRNA miR-100 also exhibited species-divergent target coexpression, suggesting lineage-specific regulatory roles for deeply conserved miRNAs. Candidate ceRNA networks were also recovered, including predicted derepression of epimachinery transcripts, indicating that lncRNA-mediated buffering operates alongside direct miRNA control. Recovery of these regulatory interactions across three evolutionarily divergent species, despite few orthologous miRNA or lncRNA, suggests that multi-layered epigenetic regulation is a conserved feature of cnidarian biology. These results establish direct miRNA and lncRNA control of epigenetic machinery as an active component of coral gene regulation, and provide foundational resources for studying how multilayered epigenetic interactions contribute to coral resilience to environmental change. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=140 SRC="FIGDIR/small/739451v1_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@7e07dforg.highwire.dtl.DTLVardef@36cf0forg.highwire.dtl.DTLVardef@5406d3org.highwire.dtl.DTLVardef@8c09e3_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

Spatially resolved gene expression analysis illuminates location-specific functions in the reef-building coral Pocillopora acuta

Reef-building coral polyps contain multiple specialized tissue types with distinct functions, from feeding and defense to symbiosis and skeleton formation. While these cell types have been characterized microscopically and more recently via single-cell RNA sequencing, spatially resolved high-throughput gene expression profiling remains limited in corals. Here we combine Laser Capture Microdissection with RNA sequencing to characterize tissue-specific gene expression in the reef building coral Pocillopora acuta. Oral tissues, adjacent to the seawater, exhibited 1,253 upregulated genes enriched for amino acid synthesis, transmembrane transport, signaling, environmental sensing, and secretion. These tissues showed high expression of immune and microbial-recognition genes consistent with their interface with seawater microbiota: mucins, lectins, toll-like receptors (TLRs), and MyD88 that connects TLRs to the NF-{kappa}B pathway. Aboral tissues, which build the corals skeleton, exhibited 552 upregulated genes enriched for developmental processes, cell adhesion, and stimulus response. We identified strong differential expression of biomineralization- associated genes, including Chitin Synthase and Wnt pathway members, suggesting previously underdescribed roles in skeleton formation. Critically, many genes implicated in specialized functions were expressed in multiple tissues. This lack of location specificity suggests functional biomarkers will likely entail multi-gene expression patterns rather than single genes. Collectively, we highlight the need for greater spatial resolution (e.g., single cell/nuclei and spatial transcriptomics) to fully resolve coral responses within their native tissue complexity. As anthropogenic climate change increasingly threatens coral reefs, spatially resolved molecular insight into coral biology will be critical for interpreting stress response mechanisms, forecasting their limits, and applying human interventions.

molecular biology↗

Seasonal plasticity of symbiotic strategies clarifies coral holobiont resistance and resilience

As coral reefs face unprecedented declines driven by thermal stress and the breakdown of coral symbiosis (i.e., coral bleaching), restoration efforts increasingly rely on coral health and resilience rankings. However, seasonal plasticity in symbiosis and holobiont metabolism, along with the presence of cryptic species, can complicate data interpretation. Therefore, quantifying seasonal plasticity in coral physiology and incorporating genetic identification are essential for accurately interpreting and drawing conclusions from trait-based and fitness-based analyses. To test the effect of seasonal and site variation on physiological plasticity we sampled three ecologically dominant genera, Acropora, Pocillopora, and Porites across three lagoon sites (n=15 tagged colonies genus-1 site-1) on the north shore of Moorea French Polynesia in January, March, September, and December of 2020. We identified coral host and intracellular symbiotic Symbiodiniaceae to the highest taxonomic resolution possible and quantified 13 physiological variables within the holobiont. Genetic analyses identified A. pulchra along with cryptic lineages in Pocillopora (P. meandrina, P. tuahiniensis) and Porites (P. evermanni, P. lobata/lutea). A. pulchra was dominated by Durusdinium trenchii and also contained Symbiodinium microadriaticum. Symbiont communities differed between cryptic congeners, with P. meandrina hosting Cladocopium latusorum and P. tuahiniensis hosting Cladocopium pacificum, whereas P. evermanni and P. lobata/lutea both hosted Cladocopium (C15), but each with unique C15 profiles. Weedy taxa such as Acropora and Pocillopora displayed a cycle of symbiont boom and bust in response to seasonally variable light and temperature, likely contributing to the high stress sensitivity of these taxa. In contrast, despite seasonal environmental variability, Porites displayed greater symbiont stability, with temperature--rather than light--serving as the stronger explanatory variable of seasonal variation in host physiology. Increased host biomass under cooler conditions, which provides energy reserves, may serve as an important stabilizing factor in massive Porites well-documented stress resilience. Collectively, our data provide essential evidence of the need for integrative analyses considering baseline physiological states across seasons along with host and symbiont genetics, particularly in light of the plethora of climate change related stress test assays taking place throughout the year across coral taxa with cryptic lineages.

physiology↗

Mosaic accumulation of somatic genetic variation and estimates of age in the long-lived reef-building coral Acropora palmata

Somatic genetic variation (SOGV), accumulating during an organisms lifetime, was traditionally viewed as detrimental rather than adaptive due to links with cancer and senescence. However, in modular organisms like corals, deleterious mutations can be purged at the cellular or polyp level, while adaptive mutations may rise in frequency as polyps create genetically distinct modules. Quantifying the somatic genetic landscape in corals is necessary to understand the role these mutations may have in coral and clonal animal development and evolution. Here, we catalog somatic genetic variation in eight Acropora palmata colonies from Curacao. Whole genomes were sequenced (70-100x depth), documenting mutation variant allele frequency shifts as genets aged. Large numbers of SOGVs were observed in six- to ten-year-old colonies, and inferred mutation rates were used to age a genet of uncertain age to almost a century old. Although mutations were not fixed at the polyp or branch levels, i.e. they always displayed frequencies <0.5 as expected at mutating homozygous sites, their allele frequencies followed a power-law distribution, similar to aging human tissues. No signs of positive selection were found; instead SOGVs in the colony of uncertain age were under purifying selection. In one colony, mutations in 28 samples from along a branch were analyzed using a SNP microarray. Contrary to expectations, genetic and physical distances were unrelated. This observation together with the observed lack of fixation may be explained by a large stem cell population, the de-differentiation or dormancy of stem cells, the contribution of strong purifying selection, or a combination of the previously mentioned. Our findings provide a neutral framework against which to test for module-level selection of genetic variation in corals, explore the relationship between physical and genetic distance within a colony, and apply a somatic genetic clock to colonies of Acropora palmata. This work provides necessary fundamental insights into the landscape of somatic mutations in reef-building coral, highlighting the importance of studying these mutations as they may contribute to genetic diversity and adaptability in colonial animals.

genomics↗

Genome assemblies and genetic maps highlight chromosome-scale macrosynteny in Atlantic acroporids

BackgroundCorals belong to the Cnidaria, an early branching phylum of metazoans. Over the course of their long evolutionary history, they have adapted to changing environments, such as rising sea levels and increasing ocean temperatures. While their history speaks to their evolutionary capacity, it is less clear how quickly they may respond to rapid changes. A critical aspect of adaptive capacity is the structure of their genome and the genetic diversity contained within. FindingsHere, we present chromosome-scale genome assemblies and genetic linkage maps of two critically endangered coral species, Acropora palmata and A. cervicornis, the two extant Atlantic acroporid corals. Genomes of both species were resolved into 14 chromosomes with comparable assembly sizes (A. palmata, 287Mb; A. cervicornis, 305Mb). Gene content, repeat content, gene collinearity and macrosynteny were largely preserved between the Atlantic acroporids but a 2.5 Mb inversion and 1.4 Mb translocation were detected between two of the chromosome pairs. Macrosynteny and gene collinearity decreased when comparing Atlantic with Pacific acroporids. Paracentric inversions of whole chromosome arms characterized A. hyacinthus, specifically. In the larger context of cnidarian evolution, the four acroporids and another scleractinian coral with chromosome-resolved genome assemblies retained six of 21 cnidarian ancestral linkage groups, while also privately sharing numerous ALG fission and fusion events compared to other distantly related cnidarians. Genetic linkage maps were built using a 30K genotyping array with 105 offspring in one family for A. palmata and 154 offspring across 16 families for A. cervicornis. The A. palmata consensus linkage map spans 1,013.42 cM and includes 2,114 informative markers. The A. cervicornis consensus map spans 927.36 cM across 4,859 markers. A. palmata and A. cervicornis exhibited similarly high sex-averaged genome-wide recombination rates (3.53 cM/Mb and 3.04 cM/Mb, respectively) relative to other animals. In our gamete-specific maps, we found pronounced sex-based differences in recombination, known as heterochiasmy, in this simultaneous hermaphrodite, with both species showing recombination rates 2-2.5X higher in eggs compared to sperm. ConclusionsThe genomic resources presented here are the first of their kind available for Atlantic coral species. These data sets revealed that adaptive capacity of endangered Atlantic corals is not limited by their recombination rates, with both species exhibiting high recombination rates and heterochiasmy. Nevertheless, the two sister species maintain high levels of macrosynteny and gene collinearity between them. The few large-scale rearrangements detected deserve further study as a potential cause of fertilization barriers between the species. Together, the assemblies and genetic maps presented here now enable genome-wide association studies and discovery of quantitative trait loci; tools that can aid in the conservation of these endangered corals.

evolutionary biology↗