An overview of transcription in dinoflagellates

Zaheri, Bahareh; Morse, David

doi:10.1016/j.gene.2022.146505

Cited by 16 publications

(7 citation statements)

References 190 publications

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“…Dinoflagellates have characteristic morphological features that suggest transcription may be difficult to regulate, including permanently condensed chromatin that lack nucleosomes (Bodansky et al, 1979; Herzog & Soyer, 1981; Riaz et al, 2018). There are also fewer transcription factors than might be expected, as when the genomes of F. kawagutii and the diatom Thalassiosira pseudonana are compared, the fraction of genes annotated as transcription factors is almost 5 fold less in the dinoflagellate (Zaheri & Morse, 2022). Dinoflagellate mRNAs also have unusually long half‐lives (Morey & van Dolah, 2013), consistent with a low rate of transcription.…”

Section: Discussionmentioning

confidence: 99%

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

Bowazolo,

Morse

2023

Molecular Microbiology

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Dinoflagellates respond to daily changes in light and dark by changes in cellular metabolism, yet the mechanisms used are still unclear. For example, Fugacium (previously Symbiodinium) kawagutii shows little difference in the transcriptome between day and night suggesting little transcriptional control over gene expression. Here, we have performed ribosome profiling at 2 h intervals over a daily light–dark cycle to assess the degree to which protein synthesis rates might change over the daily cycle. The number of F. kawagutii coding sequences with significant differences in the number of ribosome‐protected fragments (RPF) over the 24‐h cycle was 2923 using JTK_Cycle and 3655 using ECHO. The majority of the regulated transcripts showed peak translation at the onset of the dark period. The regulated sequences were assigned to different KEGG pathways and transcripts that were translated at roughly the same time were termed concurrently regulated. Both analyses revealed concurrent regulation of many transcripts whose gene products were involved in spliceosome or lysosome biogenesis with peak translation rates around the onset of the dark period, while others, involved in nitrate metabolism and ribosomal proteins, were preferentially translated around the onset of the day phase or the end of the night phase, respectively. In addition, some sequences involved in DNA synthesis were preferentially translated at the end of the day. We conclude that light–dark cycles seem able to synchronize translation of some transcripts encoding proteins involved in a range of different cellular processes, and propose that these changes may help the cells adapt and alter their metabolism as a function of the time of day.

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Section: Discussionmentioning

confidence: 99%

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

Bowazolo,

Morse

2023

Molecular Microbiology

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“…Given the paucity of transcription factors and differentially expressed genes at transcriptional level, dinoflagellates preferentially control gene expression through post-transcriptional regulation (Roy & Morse, 2013, Zaheri & Morse, 2022. Despite lacking significant difference in the transcriptome over a daily light-dark cycle, dinoflagellates Lingulodinium and Symbiodinium possess coordinated changes in the number of ribosome-protected fragments (Bowazolo & Morse, 2023, Bowazolo et al, 2022, suggesting translational control serves as a major strategy for regulating gene expression.…”

Section: Discussionmentioning

confidence: 99%

“…Their unique characteristics, including permanently condensed liquid-crystalline chromosomes lacking nucleosomes (Wisecaver & Hackett, 2011, Wong, 2019), alternating unidirectional gene arrays (Nand, Zhan et al, 2021, Nelson, Hazzouri et al, 2021, Shoguchi, Shinzato et al, 2013, Stephens, González-Pech et al, 2020), mRNA maturation with trans-splicing (Lidie & Van Dolah, 2007, Zhang, Hou et al, 2007), and non-typical promoter harbouring no TATA box (Guillebault, Sasorith et al, 2002, Lin, Cheng et al, 2015), distinguish them from other eukaryotes in terms of chromatin organization and gene expression. Instead of controlling gene expression at transcriptional level, it was believed that dinoflagellates mainly rely on post-transcriptional regulation (Roy & Morse, 2013, Zaheri & Morse, 2022). There is a clear paucity of both basal and promoter-specific transcription factors in dinoflagellates genomes, which encode only half number of expected components of RNA polymerase II (RNAP II) and less than 10% of gene specific transcription factors compared to classical eukaryotes (Roy & Morse, 2013, Zaheri & Morse, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…Instead of controlling gene expression at transcriptional level, it was believed that dinoflagellates mainly rely on post-transcriptional regulation (Roy & Morse, 2013, Zaheri & Morse, 2022). There is a clear paucity of both basal and promoter-specific transcription factors in dinoflagellates genomes, which encode only half number of expected components of RNA polymerase II (RNAP II) and less than 10% of gene specific transcription factors compared to classical eukaryotes (Roy & Morse, 2013, Zaheri & Morse, 2022). Numerous studies also indicated that for different dinoflagellate species including Symbiodinium sp., Lingulodinium sp., Scrippsiella sp., Alexandrium sp., only a few genes exhibited significant changes in their transcript abundance under light-dark transition, temperature change, circadian rhythm and stressful conditions (Chen, Dougan et al, 2023, Moustafa, Evans et al, 2010, Roy, Beauchemin et al, 2014, Yang, Beszteri et al, 2011, Zaheri, Dagenais-Bellefeuille et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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The highly abundant mRNA m¹A modification: a new layer of gene regulation in dinoflagellates

Li,

Guo

et al. 2023

Preprint

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The N1-methyladenosine (m1A) is a positively charged RNA modification known to disrupt base pairing and influence RNA stability. Despite its limited presence in the mRNA of various organism models, including yeast, mouse, and human, the exact processes of m1A biosynthesis, distribution, regulation, and function remain controversial. Dinoflagellates are a major group of single-celled eukaryotic phytoplankton having peculiar crystalline chromosomes. Their genes are arranged in unidirectional gene clusters along the chromosomes and only have minimal transcriptional regulation, implying the involvement of other critical regulatory mechanisms in gene expression. Here, we found that m1A rather than m6A is the most prevalent mRNA modification in dinoflagellates and asymmetrically distributed along mature transcripts. Utilizing the dinoflagellate speciesAmphidinium carteraeas a study model, we identified 13481 m1A peaks characterized by a non-tRNA T-loop-like sequence motif within the transcripts of 10794 genes, many of which are involved in carbon and nitrogen metabolism. With enrichment around stop codon region and 3’ UTR, dinoflagellate mRNA m1A exhibits negative correlation with translation efficiency. Notably, nitrogen depletion (N-depletion) treatment led to significant global decrease of mRNA m1A amount, causing dramatic variation in translation rates with minimal changes in transcription. Additionally, our analysis uncovered distinctive methylation patterns of m1A modification that appears to post-transcriptionally modulate gene expression through regulating translation efficiency. Thus, our findings provide the first comprehensive m1A map of dinoflagellate mRNA, shedding light on its crucial role as a post-transcriptional regulatory layer to compensate the degeneration of transcriptional regulation in dinoflagellate. This study also sets the stage for further investigation into the biogenesis and functional significance of mRNA m1A in eukaryotes.

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“…With a low protein/chromatin DNA ratio of ~1:10 and high levels of chromosomal divalent cations, dinoflagellate chromosomes occur in cholesteric liquid crystalline state, which are strongly birefringent and permanently condensed 17,18 . Their genes are clustered into unidirectional arrays along the LCCs and lack of transcriptional regulation [19][20][21] . Instead of the core histones, bacterial nucleoidassociated protein HU-derived "histone like proteins" (HLPs) and algae virusesoriginated dinoflagellate viral nucleoproteins (DVNPs) constitute their major chromosomal packaging proteins 17 .…”

Section: Introductionmentioning

confidence: 99%

The exotic thymidine modification 5-hydroxymethyluridine in dinoflagellateAmphidinium carterae

Li,

Wang

et al. 2023

Preprint

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Dinoflagellate chromosomes are extraordinary, as their organization is independent of architectural nucleosomes unlike typical eukaryotes and shows a cholesteric liquid crystal state. 5-hydroxymethyluridine (5hmU) is present at unusually high levels and its function remains an enigma in dinoflagellates chromosomal DNA. Here, we demonstrate that 5hmU exhibits content variations in different dinoflagellates and is generated at the poly-nucleotide level through hydroxylation of thymidine. Importantly, we identified the enzyme, which is a putative dinoflagellate TET/JBP homologue, catalyzing 5hmU production using eitherin vivoorin vitrobiochemical assay. Based on the near-chromosomal level genome assembly of dinoflagellateAmphidinium carterae, we depicted a comprehensive 5hmU landscape and found that most 5hmU peaks share a conserved TG-rich motif, and are significantly enriched in repeat elements, which mark partially overlapping regions with 5-methylcytosine (5mC) sites. Moreover, inhibition of 5hmU via dioxygenase inhibitor leads to transcriptional activation of 5hmU-marked transposable elements (TEs), implying that 5hmU appears to serve as epigenetic marks for silencing retrotransposon. Together, our results revealed the biogenesis, genome-wide landscape and molecular function of dinoflagellate 5hmU, providing mechanic insight into the function of this enigmatic DNA mark.

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An overview of transcription in dinoflagellates

Cited by 16 publications

References 190 publications

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

The highly abundant mRNA m¹A modification: a new layer of gene regulation in dinoflagellates

The exotic thymidine modification 5-hydroxymethyluridine in dinoflagellateAmphidinium carterae

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An overview of transcription in dinoflagellates

Cited by 16 publications

References 190 publications

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

Ribosome profiling in the Symbiodiniacean dinoflagellate Fugacium kawagutii shows coordinated protein synthesis of enzymes in different pathways at different times of day

The highly abundant mRNA m1A modification: a new layer of gene regulation in dinoflagellates

The exotic thymidine modification 5-hydroxymethyluridine in dinoflagellateAmphidinium carterae

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The highly abundant mRNA m¹A modification: a new layer of gene regulation in dinoflagellates