Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism

Abstract

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 35 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 daytime than the night likely contribute to these changes via 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 40 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. 45Keywords:Proteomics / circadian rhythms / metabolism / photoperiod / seasonality . CC-BY 4.0 International license not peer-reviewed) is the author/funder. It is made available under a

Diurnal changes in concerted plant protein phosphorylation and acetylation in Arabidopsis organs and seedlings

“…Significant protein phosphorylation changes were most frequently found in flowers (ED) and in rosettes (EN), whereas significant protein acetylation changes were most abundant in roots (ED) and in seedlings (EN) (Data S2; Table ). In contrast, few proteins in the proteomes from the same organs and seedlings had a Log2‐fold abundance change of >1.0 at the corresponding time points (Data S3), consistent with previous reports (Baerenfaller et al ., ; Graf et al ., ; Seaton et al ., ). To determine whether the observed changes in PTM levels resulted from changes in protein abundance we compared the quantified PTMome and total proteome.…”

“…Our current understanding of circadian and light control is largely derived from genetic and transcriptomic studies, which have revealed the extent to which the expression of genes is regulated by the clock and the diurnal cycle (Endo et al ., ; Greenham and McClung, ; Nagel et al ., ; Nohales and Kay, ). More recent studies have shown that transcript and protein abundance may not always be correlated at the light–dark transitions during the diurnal cycle, indicating that transcriptional changes are not necessarily predictive for regulation at the protein level (Baerenfaller et al ., ; Graf et al ., ; Seaton et al ., ). Moreover, it is currently unknown if this lack of coincident transcript and protein‐level regulation also extends to proteins whose function is circadian clock‐ or light controlled by phosphorylation or acetylation, or both.…”

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

“…This makes it difficult to distinguish between direct and indirect effects when individual mutants are studied. Furthermore, although transcripts for proteins involved in photosynthesis, sucrose and starch metabolism and nitrogen metabolism often exhibit circadian rhythms (Farré & Weise, ; Harmer, ; Harmer et al, ; Harmer, Panda, & Kay, ; Michael et al, ; Smith et al, ; Usadel et al, ), these rarely lead to significant diel changes in the abundance of the encoded proteins (Baerenfaller et al, ; Dodd, Belbin, Frank, & Webb, ; Gibon, Bläsing, et al, ; Gibon et al, ; Seaton et al, ; Skeffington, Graf, Duxbury, Gruissem, & Smith, ; Stitt & Gibon, ). This underlines the need for studies of emergent metabolic responses that integrate circadian outputs, irrespective of whether the outputs act transcriptionally, posttranscriptionally, or posttranslationally.…”

Integration of large-scale multi-omic datasets: A protein-centric view

“…In Arabidopsis, the combined analysis of protein and mRNA abundance changes in diurnal regulation identified the synchronization of peaks in transcript levels and translation rates [43]. The authors suggest this result might be “translational coincidence” controlling the most dominant expression changes during the photoperiod.…”

“…While this example demonstrates how transcription and translation can oppose one another to achieve the desired outcome, examples of concordant regulation also exist. In Arabidopsis, the combined analysis of protein and mRNA abundance changes in diurnal regulation identified the synchronization of peaks in transcript levels and translation rates [43]. The authors suggest this result might be “translational coincidence” controlling the most dominant expression changes during the photoperiod.…”