Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism

• Published in: Molecular systems biology 2018-03, Vol.14 (3), p.e7962-n/a
• Main Authors: Seaton, Daniel D, Graf, Alexander, Baerenfaller, Katja, Stitt, Mark, Millar, Andrew J, Gruissem, Wilhelm
• Format: Article
• Language: English
• Subjects: Abundance; Algae; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Biosynthesis; Circadian Rhythm; circadian rhythms; Diurnal; EMBO30; EMBO31; EMBO33; Environmental changes; Evening; Gene Expression Regulation, Plant; Gene Regulatory Networks; Leaves; Mass Spectrometry; Mass spectroscopy; Metabolism; Models, Theoretical; Photoperiod; Photoperiods; Photosynthesis; Protein Biosynthesis; Proteins; Proteomes; Proteomics; Rhythms; Ribonucleic acid; RNA; seasonality; Transcription; Translation
• ISSN: 1744-4292; 1744-4292
• DOI: 10.15252/msb.20177962

Plants respond to seasonal cues such as the photoperiod, to adapt to current conditions and to prepare for environmental changes in the season to come. To assess photoperiodic responses at the protein level, we quantified the proteome of the model plant Arabidopsis thaliana by mass spectrometry across four photoperiods. This revealed coordinated changes of abundance in proteins of photosynthesis, primary and secondary metabolism, including pigment biosynthesis, consistent with higher metabolic activity in long photoperiods. Higher translation rates in the day than the night likely contribute to these changes, via an interaction with rhythmic changes in RNA abundance. Photoperiodic control of protein levels might be greatest only if high translation rates coincide with high transcript levels in some photoperiods. We term this proposed mechanism “translational coincidence”, mathematically model its components, and demonstrate its effect on the Arabidopsis proteome. Datasets from a green alga and a cyanobacterium suggest that translational coincidence contributes to seasonal control of the proteome in many phototrophic organisms. This may explain why many transcripts but not their cognate proteins exhibit diurnal rhythms. Synopsis The Arabidopsis proteome changes in a coordinated fashion across four photoperiods. A simple ‘translational coincidence’ mechanism can explain photoperiod‐dependent regulation of protein levels based on clock‐dependent, daily mRNA level changes. Day length altered the abundance of 1,781 proteins, out of 4,344 proteins quantified from leaves of Arabidopsis thaliana , in a pattern consistent with higher metabolic activity in long days. Proteins with clock‐regulated, evening‐peaking RNAs tended to increase in abundance under longer daylengths, whereas proteins with morning‐peaking RNAs did not. A simple, “translational coincidence” model predicted the experimental results, because high, light‐induced translation rates will coincide with high levels of an evening‐expressed RNA only under long days, not short days. Many clock‐controlled genes might gain seasonal control of protein levels via translational coincidence, which we speculate is widespread based upon data from a marine alga and a freshwater cyanobacterium. Graphical Abstract The Arabidopsis proteome changes in a coordinated fashion across four photoperiods. A simple “translational coincidence” mechanism can explain photoperiod‐dependent regulation of protein levels based on cl