Unknown to Known: Advancing Knowledge of Coral Gene Function

Cleves, Phillip A.; Shumaker, Alexander; Lee, Jun Mo; Putnam, Hollie M.; Bhattacharya, Debashish

doi:10.1016/j.tig.2019.11.001

Cited by 39 publications

(37 citation statements)

References 66 publications

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“…We recognize however that our findings are largely summary in nature and serve as an initial step in understanding the transcriptome (vis-à-vis functional capacity) of M. capitata gametes. In conclusion we present here the first study of the transcriptome of coral sperm and eggs and reach interesting conclusions that pave the way for future multi-omics and genetics investigations on this topic (Cleves et al, 2020), particularly in the context of anthropogenic climate change influences on the marine environment.…”

Section: Discussionsupporting

confidence: 53%

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Transcriptome analysis provides a blueprint of coral egg and sperm functions

Etten

Shumaker

Mass

et al. 2020

PeerJ

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Background Reproductive biology and the evolutionary constraints acting on dispersal stages are poorly understood in many stony coral species. A key piece of missing information is egg and sperm gene expression. This is critical for broadcast spawning corals, such as our model, the Hawaiian species Montipora capitata, because eggs and sperm are exposed to environmental stressors during dispersal. Furthermore, parental effects such as transcriptome investment may provide a means for cross- or trans-generational plasticity and be apparent in egg and sperm transcriptome data. Methods Here, we analyzed M. capitata egg and sperm transcriptomic data to address three questions: (1) Which pathways and functions are actively transcribed in these gametes? (2) How does sperm and egg gene expression differ from adult tissues? (3) Does gene expression differ between these gametes? Results We show that egg and sperm display surprisingly similar levels of gene expression and overlapping functional enrichment patterns. These results may reflect similar environmental constraints faced by these motile gametes. We find significant differences in differential expression of egg vs. adult and sperm vs. adult RNA-seq data, in contrast to very few examples of differential expression when comparing egg vs. sperm transcriptomes. Lastly, using gene ontology and KEGG orthology data we show that both egg and sperm have markedly repressed transcription and translation machinery compared to the adult, suggesting a dependence on parental transcripts. We speculate that cell motility and calcium ion binding genes may be involved in gamete to gamete recognition in the water column and thus, fertilization.

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Section: Discussionsupporting

confidence: 53%

“…S8. We speculate that these genes are interesting targets for future CRISPR/Cas9 based gene knockdowns (recently developed for Scleractinia; Cleves et al, 2018;Cleves et al, 2020) to explore coral reproductive biology.…”

Section: Fertilizationmentioning

confidence: 99%

Transcriptome analysis provides a blueprint of coral egg and sperm functions

Etten

Shumaker

Mass

et al. 2020

PeerJ

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“…We define dark genes as predicted proteins with RNA-seq validation that are either lineagespecific or shared with other species and do not share significant sequence similarity (BLASTP e-value cut-off ≤ 1e -5 against the nonredundant NCBI database). Dark genes are either novel or too highly diverged to identify putative homologs in existing data, although some may encode a known domain associated with novel sequence (20). For example, 33% of dinoflagellate algal genes lack an annotation, but 1.4% of these unknown proteins contain a known domain (21).…”

Section: Gene Co-expression Network Analysismentioning

confidence: 99%

Multi-omic characterization of the thermal stress phenome in the stony coralMontipora capitata

Pathmanathan

Williams

Stephens

et al. 2021

Preprint

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We used network methods to analyze transcriptomic and polar metabolomic data generated from the stress resistant stony coral Montipora capitata. Corals were exposed to ambient or thermal stress conditions over a five-week period that coincided with a mass spawning event of this species. Gene co-expression networks showed that the early thermal stress response involves downregulation of growth and DNA replication, whereas signaling and the immune response are strongly upregulated. Later stages are dominated by suppression of metabolite transport and biomineralization and enhanced expression of transcriptional regulators. Integration of gene-metabolite data demonstrates that the major outcome of the thermal treatment is activation of animal redox stress pathways with detoxification of reactive oxygen species being dominant. Differential regulation of the highly conserved cytochrome P450 gene family was of particular interest with downregulation of CYP1A1, involved in progesterone metabolism, potentially explaining the attenuated mass spawning observed during the sampling period.

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“…Coral reefs are facing a significant decline because of increasing local and global stressors from disease, climate change, and pollution ( 42 ). Although coral possess a robust innate immune system, the cellular mechanisms these organisms use to respond to disease have not been functionally characterized ( 43 ). In addition, elevated ocean temperatures have emerged as key threats to the long-term survival of coral reefs because of collapse of the coral–algal symbiosis ( 23 , 42 ).…”

Section: Discussionmentioning

confidence: 99%

Caspases from scleractinian coral show unique regulatory features

Shrestha

Tung

Grinshpon

et al. 2020

Journal of Biological Chemistry

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Coral reefs are experiencing precipitous declines around the globe with coral diseases and temperature-induced bleaching being primary drivers of these declines. Regulation of apoptotic cell death is an important component in the coral stress response. Although cnidaria are known to contain complex apoptotic signaling pathways, similar to those in vertebrates, the mechanisms leading to cell death are largely unexplored. We identified and characterized two caspases each from Orbicella faveolata, a disease-sensitive reef-building coral, and Porites astreoides, a disease-resistant reef-building coral. The caspases are predicted homologs of the human executioner caspases-3 and -7, but OfCasp3a (Orbicella faveolata caspase-3a) and PaCasp7a (Porites astreoides caspase-7a), which we show to be DxxDases, contain an amino-terminal caspase activation/recruitment domain (CARD) similar to human initiator/inflammatory caspases. OfCasp3b (Orbicella faveolata caspase-3b) and PaCasp3 (Porites astreoides caspase-3), which we show to be VxxDases, have short pro-domains, like human executioner caspases. Our biochemical analyses suggest a mechanism in coral which differs from that of humans, where the CARD-containing DxxDase is activated on death platforms but the protease does not directly activate the VxxDase. The first X-ray crystal structure of a coral caspase, of PaCasp7a determined at 1.57Å resolution, reveals a conserved fold and an N-terminal peptide bound near the active site that may serve as a regulatory exosite. The binding pocket has been observed in initiator caspases of other species. These results suggest mechanisms for the evolution of substrate selection while maintaining common activation mechanisms of CARD-mediated dimerization.

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Unknown to Known: Advancing Knowledge of Coral Gene Function

Cited by 39 publications

References 66 publications

Transcriptome analysis provides a blueprint of coral egg and sperm functions

Transcriptome analysis provides a blueprint of coral egg and sperm functions

Multi-omic characterization of the thermal stress phenome in the stony coralMontipora capitata

Caspases from scleractinian coral show unique regulatory features

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