Multiomics resolution of molecular events during a day in the life of Chlamydomonas

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Significance

Chlamydomonas reinhardtii is the premier reference organism for understanding unicellular green algae. Chlamydomonas is an important model for photosynthesis as well as fermentation and other anaerobic pathways under dark anoxic conditions. We have produced a diurnal transcriptome, validated by subproteomic analyses, and matched with measurements of pigments, select metabolites, and physiological parameters. We report that the majority of the algal genome is differentially expressed over the course of the day and the timing of specific genes is dictated by their biological function. We also discovered that fermentation rather than respiration is the preferred metabolic fate of starch-derived glycolytic pyruvate. We offer our rich dataset to the algal and plant communities.

Abstract

The unicellular green alga Chlamydomonas reinhardtii displays metabolic flexibility in response to a changing environment. We analyzed expression patterns of its three genomes in cells grown under light–dark cycles. Nearly 85% of transcribed genes show differential expression, with different sets of transcripts being up-regulated over the course of the day to coordinate cellular growth before undergoing cell division. Parallel measurements of select metabolites and pigments, physiological parameters, and a subset of proteins allow us to infer metabolic events and to evaluate the impact of the transcriptome on the proteome. Among the findings are the observations that Chlamydomonas exhibits lower respiratory activity at night compared with the day; multiple fermentation pathways, some oxygen-sensitive, are expressed at night in aerated cultures; we propose that the ferredoxin, FDX9, is potentially the electron donor to hydrogenases. The light stress-responsive genes PSBS, LHCSR1, and LHCSR3 show an acute response to lights-on at dawn under abrupt dark-to-light transitions, while LHCSR3 genes also exhibit a later, second burst in expression in the middle of the day dependent on light intensity. Each response to light (acute and sustained) can be selectively activated under specific conditions. Our expression dataset, complemented with coexpression networks and metabolite profiling, should constitute an excellent resource for the algal and plant communities.

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The canonical histone proteins are encoded by replication-dependent genes and must rapidly reach high levels of expression during S phase. In metazoans the genes that encode these proteins produce mRNAs that, instead of being polyadenylated, contain a unique 3' end structure. By contrast, the synthesis of the variant, replication-independent histones, which are encoded by polyadenylated mRNAs, persists outside of S phase. Accurate positioning of both histone types in chromatin is essential for proper transcriptional regulation, the demarcation of heterochromatic boundaries and the epigenetic inheritance of gene expression patterns. Recent results suggest that the coordinated synthesis of replication-dependent and variant histone mRNAs is achieved by signals that affect formation of the 3' end of the replication-dependent histone mRNAs.

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Plant growth is driven by photosynthetic carbon fixation during the day. Some photosynthate is accumulated, often as starch, to support nocturnal metabolism and growth at night. The rate of starch degradation in Arabidopsis leaves at night is essentially linear, and is such that almost all of the starch is used by dawn. We have investigated the timer that matches starch utilization to the duration of the night. The rate of degradation adjusted immediately and appropriately to an unexpected early onset of night. Starch was still degraded in an appropriate manner when the preceding light period was interrupted by a period of darkness. However, when Arabidopsis was grown in abnormal day lengths (28 h or 17 h) starch was exhausted approximately 24 h after the last dawn, irrespective of the actual dawn. A mutant lacking the LHY and CCA1 clock components exhausted its starch at the dawn anticipated by its fast-running circadian clock, rather than the actual dawn. Reduced growth of wild-type plants in 28-h days and lhy/cca1 mutants in 24-h days was attributable to the inappropriate rate of starch degradation and the consequent carbon starvation at the end of night. Thus, starch degradation is under circadian control to ensure that carbohydrate availability is maintained until the next anticipated dawn, and this control is necessary for maintaining plant productivity.

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The diurnal cycle strongly influences many plant metabolic and physiological processes. Arabidopsis thaliana rosettes were harvested six times during 12-h-light/12-h-dark treatments to investigate changes in gene expression using ATH1 arrays. Diagnostic gene sets were identified from published or in-house expression profiles of the response to light, sugar, nitrogen, and water deficit in seedlings and 4 h of darkness or illumination at ambient or compensation point [CO(2)]. Many sugar-responsive genes showed large diurnal expression changes, whose timing matched that of the diurnal changes of sugars. A set of circadian-regulated genes also showed large diurnal changes in expression. Comparison of published results from a free-running cycle with the diurnal changes in Columbia-0 (Col-0) and the starchless phosphoglucomutase (pgm) mutant indicated that sugars modify the expression of up to half of the clock-regulated genes. Principle component analysis identified genes that make large contributions to diurnal changes and confirmed that sugar and circadian regulation are the major inputs in Col-0 but that sugars dominate the response in pgm. Most of the changes in pgm are triggered by low sugar levels during the night rather than high levels in the light, highlighting the importance of responses to low sugar in diurnal gene regulation. We identified a set of candidate regulatory genes that show robust responses to alterations in sugar levels and change markedly during the diurnal cycle.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A

Journal ID (hwp): pnas

Journal ID (pmc): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Print): 5 February 2019

Publication date (Electronic): 18 January 2019

Publication date PMC-release: 18 January 2019

Volume: 116

Issue: 6

Pages: 2374-2383

Affiliations

[1] ^aInstitute for Genomics and Proteomics, University of California, Los Angeles , CA 90095;

[2] ^bDepartment of Chemistry and Biochemistry, University of California, Los Angeles , CA 90095;

[3] ^cEnvironmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory (PNNL) , US Department of Energy, Richland, WA 99352;

[4] ^dBiological Sciences Divison, PNNL , US Department of Energy, Richland, WA 99352;

[5] ^eInstitute of Plant Biochemistry, Cluster of Excellence on Plant Science, Heinrich Heine University , 40225 Düsseldorf, Germany;

[6] ^fCenter for Plant Science Innovation, University of Nebraska , Lincoln, NE 68588

Author notes

³To whom correspondence should be addressed. Email: sabeeha@ 123456chem.ucla.edu .

Contributed by Sabeeha S. Merchant, November 26, 2018 (sent for review September 7, 2018; reviewed by Ariane Atteia and Michel Goldschmidt-Clermont)

Author contributions: D.S. and S.S.M. designed research; D.S., S.S., S.D.G., P.A.S., S.O.P., C.D.N., T.M.-A., E.S., and G.J.B. performed research; S.D.G., S.O.P., C.D.N., T.M.-A., E.S., A.P.M.W., M.S.L., and G.J.B. contributed new reagents/analytic tools; D.S., S.S., S.D.G., P.A.S., S.O.P., C.D.N., T.M.-A., E.S., A.P.M.W., M.S.L., G.J.B., and S.S.M. analyzed data; and D.S., P.A.S., and S.S.M. wrote the paper.

Reviewers: A.A., UMR Marbec; and M.G.-C., University of Geneva.

¹Present address: Horticultural Sciences Department, University of Florida, Gainesville, FL 32611.

²Present addresses: Department of Plant and Microbial Biology and Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720.