Abstract
Transcriptional coordination is a fundamental component of prokaryotic and eukaryotic cell biology, underpinning the cell cycle, physiological transitions, and facilitating holistic responses to environmental stress, but its overall dynamics in eukaryotic algae remain poorly understood. Better understanding of transcriptional partitioning may provide key insights into the primary metabolism pathways of eukaryotic algae, which frequently depend on intricate metabolic associations between the chloroplasts and mitochondria that are not found in plants. Here, we exploit 187 publically available RNAseq datasets generated under varying nitrogen, iron and phosphate growth conditions to understand the co-regulatory principles underpinning transcription in the model diatom Phaeodactylum tricornutum. Using WGCNA (Weighted Gene Correlation Network Analysis), we identify 28 merged modules of co-expressed genes in the P. tricornutum genome, which show high connectivity and correlate well with previous microarray-based surveys of gene co-regulation in this species. We use combined functional, subcellular localization and evolutionary annotations to reveal the fundamental principles underpinning the transcriptional co-regulation of genes implicated in P. tricornutum chloroplast and mitochondrial metabolism, as well as the functions of diverse transcription factors underpinning this co-regulation. The resource is publically available as PhaeoNet, an advanced tool to understand diatom gene co-regulation.
Highlights
The biology of prokaryotic and eukaryotic cells is dependent on elaborate metabolic, regulatory and gene expression pathways, consisting of multiple interacting components
Considering the repartition of genes within these modules; functional, epigenetic and localization information from the third version annotation of the P. tricornutum genome (Phatr3; Rastogi et al, 2018); and annotated lists of diatom transcription factors (Rayko et al, 2010), we identify core features underpinning the transcriptional partitioning of diatom primary metabolism, including probable metabolic links between the diatom mitochondria and chloroplast; and dissect the diverse ranges of different transcriptional drivers of this co-regulation, notably in the case of chloroplast-targeted sigma factors
P. tricornutum was selected as a model system for this study as vastly greater amounts of gene expression data have been generated for this species than any other marine alga (Ashworth and Ralph, 2018); and as its genome annotation is arguably the most complete of any alga known, allowing unprecedented insight into protein diversity, including variant protein forms generated by alternative splicing, protein sub-cellular localization and epigenetic modifications
Summary
The biology of prokaryotic and eukaryotic cells is dependent on elaborate metabolic, regulatory and gene expression pathways, consisting of multiple interacting components. Gene order plays a limited role in eukaryotic nuclear gene co-expression (Michalak, 2008), which depends instead on the simultaneous transcription, or transcriptional stabilization, of multiple discrete genomic loci. This may occur through common transcription factors (Teichmann and Babu, 2002; Reja et al, 2015); epigenetic modifications based around characteristic histone and DNA marks (Bird, 2002; Bártová et al, 2008); co-ordinated transcript processing events (Norbury, 2010); and the activity of small and long regulatory non-coding RNAs (Tsai et al, 2010; Kim and Sung, 2012). Identifying what gene co-regulation processes occur in microbial eukaryotes may allow us to better understand the biology underpinning the base of planetary food webs; and to better model the robustness of eukaryotic communities to environmental change
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