Enzymes degraded under high light maintain proteostasis by transcriptional regulation in<i>Arabidopsis</i>

Li, Lie; Duncan, Owen; Ganguly, Diep R; Lee, Chun Pong; Crisp, Peter A.; Wijerathna-Yapa, Akila; Khidhir, Karzan Ghafur; Trösch, Josua; Pogson, Barry J.; Millar, A. Harvey

doi:10.1073/pnas.2121362119

Cited by 6 publications

(4 citation statements)

References 83 publications

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“…More generally, a recent analysis of high-light stress on chloroplast proteostasis found that when rates of N -pt protein turnover increase, there is generally upregulation in mRNA abundance for the corresponding N -pt genes. In contrast, increased turnover of plastid-encoded proteins was rarely associated with an increase in the corresponding plastid mRNAs ( 55 ). These observations are consistent with the hypothesis that mitochondria and plastids are relatively lacking in precise, short-term transcriptional control and that the large standing population of organellar mRNAs offers a means for rapid regulatory responses at a posttranscriptional level.…”

Section: Discussionmentioning

confidence: 99%

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Forsythe

Grover

Miller

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA sequencing (RNA-seq) to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9 to 82.3%) of messenger RNA (mRNA) transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3 to 3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than 10-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.

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Section: Discussionmentioning

confidence: 99%

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Forsythe

Grover

Miller

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Whether or not this would lead to gross changes in protein abundance is unclear, depending on the stability of the protein product (Li et al., 2017 ). Nonetheless, our observations suggest that the transcriptional compensation observed at genes encoding proteins degraded under high light, should result in elevated translation that contributes to maintaining proteostasis during stress (Li et al., 2022 ).…”

Section: Discussionmentioning

confidence: 81%

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

Smith,

Ganguly,

Moore

et al. 2023

The Plant Journal

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SUMMARYTranscript stability is an important determinant of its abundance and, consequently, translational output. Transcript destabilisation can be rapid and is well suited for modulating the cellular response. However, it is unclear the extent to which RNA stability is altered under changing environmental conditions in plants. We previously hypothesised that recovery‐induced transcript destabilisation facilitated a phenomenon of rapid recovery gene downregulation (RRGD) in Arabidopsis thaliana (Arabidopsis) following light stress, based on mathematical calculations to account for ongoing transcription. Here, we test this hypothesis and investigate processes regulating transcript abundance and fate by quantifying changes in transcription, stability and translation before, during and after light stress. We adapt syringe infiltration to apply a transcriptional inhibitor to soil‐grown plants in combination with stress treatments. Compared with measurements in juvenile plants and cell culture, we find reduced stability across a range of transcripts encoding proteins involved in RNA binding and processing. We also observe light‐induced destabilisation of transcripts, followed by their stabilisation during recovery. We propose that this destabilisation facilitates RRGD, possibly in combination with transcriptional shut‐off that was confirmed for HSP101, ROF1 and GOLS1. We also show that translation remains highly dynamic over the course of light stress and recovery, with a bias towards transcript‐specific increases in ribosome association, independent of changes in total transcript abundance, after 30 min of light stress. Taken together, we provide evidence for the combinatorial regulation of transcription and stability that occurs to coordinate translation during light stress and recovery in Arabidopsis.

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“…Whether or not this would lead to gross changes in protein abundance is unclear, depending on the stability of the protein product (51). Nonetheless, our observations suggest that the transcriptional compensation observed at genes encoding proteins degraded under high light, should result in elevated translation that contributes to maintaining proteostasis during stress (84).…”

Section: Discussionmentioning

confidence: 92%

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

Smith

Ganguly

Moore

et al. 2022

Preprint

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The stability of a mRNA is an important determinant of its abundance and, consequently, protein production. There has been extensive research on the pathways governing mRNA stability and translation, however, it is unclear the extent to which these processes are modulated by environmental conditions. We previously modelled rapid recovery gene down-regulation (RRGD) following light stress in Arabidopsis thaliana (Arabidopsis) using mathematical calculations to account for transcription in order to predict half-lives and led to the hypothesis of recovery-specific transcript destabilisation. Here, we test this hypothesis by quantifying changes in transcription, mRNA stability, and translation in leaves of mature Arabidopsis undergoing light stress and recovery and investigate processes regulating transcript abundance and fate. Compared to juvenile plants from prior work, here we find that stability is altered for a range of transcripts that encode proteins involved in post-transcriptional processes in mature leaves. We also observe transcript destabilisation during light stress, followed by re-stabilisation upon recovery. Alongside this, we observe fast transcriptional shut-off in recovery that, when paired with transcript destabilisation, promotes rapid down-regulation of stress-induced genes. Translation was dynamic over the course of light stress and recovery, with substantial transcript-specific increases in polysome loading observed during late stress independently of total mRNA abundance. Taken together, we provide evidence for the combinatorial regulation of transcription, mRNA stability, and translation that occurs during light stress and recovery.

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Enzymes degraded under high light maintain proteostasis by transcriptional regulation inArabidopsis

Cited by 6 publications

References 83 publications

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

Dynamics of mRNA fate during light stress and recovery: from transcription to stability and translation

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