Ubiquitin-Specific Proteases UBP12 and UBP13 Act in Circadian Clock and Photoperiodic Flowering Regulation in Arabidopsis

Cui, Xia; Lu, Falong; Li, Yue; Xue, Yongming; Kang, Yongshui; Zhang, Shuaibin; Qiu, Qi; Cui, Xiekui; Zheng, Shuzhi; Liu, Bin; Xu, Xiaodong; Cao, Xiaofeng

doi:10.1104/pp.112.213009

Cited by 111 publications

(144 citation statements)

References 58 publications

(77 reference statements)

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“…In particular, UBP12 and UBP13, which are circadian-regulated genes, play a role in the control of circadian period. Consistently, the rhythmic oscillation of LHY and TOC1 transcripts is shortened in ubp12-deficient and ubp12 ubp13 double mutants (Cui et al, 2013). Taken together, these studies show that dynamic and reversible modulation of ubiquitin attachment to clock proteins fine-tunes circadian oscillation and facilitates daylength measurement.…”

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confidence: 56%

Multiple Layers of Posttranslational Regulation Refine Circadian Clock Activity in Arabidopsis

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2014

Plant Cell

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The circadian clock is a cellular time-keeper mechanism that regulates biological rhythms with a period of ;24 h. The circadian rhythms in metabolism, physiology, and development are synchronized by environmental cues such as light and temperature. In plants, proper matching of the internal circadian time with the external environment confers fitness advantages on plant survival and propagation. Accordingly, plants have evolved elaborated regulatory mechanisms that precisely control the circadian oscillations. Transcriptional feedback regulation of several clock components has been well characterized over the past years. However, the importance of additional regulatory mechanisms such as chromatin remodeling, protein complexes, protein phosphorylation, and stability is only starting to emerge. The multiple layers of circadian regulation enable plants to properly synchronize with the environmental cycles and to fine-tune the circadian oscillations. This review focuses on the diverse posttranslational events that regulate circadian clock function. We discuss the mechanistic insights explaining how plants articulate a high degree of complexity in their regulatory networks to maintain circadian homeostasis and to generate highly precise waveforms of circadian expression and activity. INTRODUCTIONThe circadian clock is a cellular time-keeper mechanism able to perceive external synchronizing inputs to generate endogenous rhythmic outputs with a period of ;24 h. In many plant species, synchronization of the clock with the environment confers fitness advantages by controlling key essential processes, such as photosynthetic activity, hypocotyl elongation, and the floral transition (Doyle et al., 2002;Green et al., 2002;Imaizumi et al., 2003;Dodd et al., 2005;Zhang et al., 2008;Niwa et al., 2009;Resco et al., 2009;Yerushalmi and Green, 2009;Nusinow et al., 2011). A large fraction of the plant transcriptome is clock controlled, suggesting that the circadian clock globally modulates diverse signals and metabolic pathways that mediate development and environmental adaptation responses (Nagel and Kay, 2012).The transcriptional regulation of several clock components has been well characterized at a molecular level over the past years (reviewed in Carré and Veflingstad, 2013). Multiple intertwined regulatory networks define the basic architecture of the Arabidopsis thaliana circadian clock. Two single MYB transcription factors, CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) (Schaffer et al., 1998), and TIMING OF CAB EXPRESSION1/ PSEUDO-RESPONSE REGULATOR1 (TOC1/PRR1) (Strayer et al., 2000;Makino et al., 2002) comprise a central regulatory module (Alabadí et al., 2001). CCA1 and LHY repress TOC1 expression that in turn represses the transcription of CCA1 and LHY (Gendron et al., 2012;Huang et al., 2012). This regulatory module is interlocked with a morning loop and an evening loop (Locke et al., 2006). In the morning loop, members of the PRR family (PRR5, PRR7, and PRR9) bind to promoters of CCA1 and LHY ...

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confidence: 56%

Multiple Layers of Posttranslational Regulation Refine Circadian Clock Activity in Arabidopsis

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2014

Plant Cell

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“…H2Bub to repress a set of genes and RING1B of the PRC1 complex to prevent its RING domain from being self-ubiquitinated (Cummins & Vogelstein, 2004;Brazhnik & Kohn, 2007;McClurg & Robson, 2015;Lecona et al, 2016;Kim & Sixma, 2017). Although the role of UBP12 and UBP13 was characterized first in plant immunity including SA response (Ewan et al, 2011) and then subsequently in circadian clock and plant development (Cui et al, 2013) the mechanisms of action of UBP12/UBP13 in these processes remain largely unexplored. Recently, direct targets of UBP12 and UBP13 in several pathways have been described.…”

Section: Multiple Functions Of Ubp12 and Ubp13mentioning

confidence: 99%

Arabidopsis ubiquitin‐specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency

et al. 2019

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Summary Nitrogen deficiency (−N) in plants triggers leaf senescence which is regulated by the transcription factor ORE1. Little is known about post‐translational regulation of ORE1 in this process. Here, we show that UBP12/UBP13 (ubiquitin‐specific protease 12/13) antagonize the action of NLA (nitrogen limitation adaptation) E3 ligase to maintain ORE1 homeostasis. In vitro pull‐down and in vivo co‐immunoprecipitation assays demonstrated specific binding between UBP12/UBP13 and ORE1. We further analyzed in various genotypes total Chl content and expression levels of senescence‐related genes under −N conditions. We found that UBP12/UBP13 can deubiquitinate polyubiquitinated ORE1 in vitro and increase the stability of ORE1 in vivo in MG132/cycloheximide‐chase experiments. Plants overexpressing UBP12/UBP13 display accelerated leaf senescence which is reversed by the ore1 mutation. By contrast, the senescence phenotype of plants overexpressing ORE1 is exacerbated by UBP12/UBP13 overexpression. The expression of senescence‐related genes tracks the senescence phenotype. ORE1 protein levels can be elevated by UBP12/UBP13 overexpression but decreased in ubp12‐2w/13‐3. In conclusion, UBP12/UBP13 deubiquitinate ORE1 to stabilize this transcription factor and promote its activity as a positive regulator for leaf senescence under −N conditions. Our study shows that UBP12/UBP13 counteracts the effect of NLA E3 ligase to accelerate leaf senescence under nitrogen starvation.

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“…Although the mechanisms communicating these cues to the circadian clock are not fully understood, they result in tissue-dependent [34] and/or cell-type-dependent [35] response-adjusted expression of output genes through the transcription factors (TFs) and repressors of its ‘morning’ and ‘evening’ loops [6,19,20]. Clock-controlled gene expression is further regulated through the modification of chromatin by ubiquitination [36,37], acetylation [38,39] and methylation [40–42]. Context-dependent stability (e.g.…”

Section: Introductionmentioning

confidence: 99%

Parallel analysis ofArabidopsiscircadian clock mutants reveals different scales of transcriptome and proteome regulation

et al. 2017

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The circadian clock regulates physiological processes central to growth and survival. To date, most plant circadian clock studies have relied on diurnal transcriptome changes to elucidate molecular connections between the circadian clock and observable phenotypes in wild-type plants. Here, we have integrated RNA-sequencing and protein mass spectrometry data to comparatively analyse the lhycca1, prr7prr9, gi and toc1 circadian clock mutant rosette at the end of day and end of night. Each mutant affects specific sets of genes and proteins, suggesting that the circadian clock regulation is modular. Furthermore, each circadian clock mutant maintains its own dynamically fluctuating transcriptome and proteome profile specific to subcellular compartments. Most of the measured protein levels do not correlate with changes in their corresponding transcripts. Transcripts and proteins that have coordinated changes in abundance are enriched for carbohydrate- and cold-responsive genes. Transcriptome changes in all four circadian clock mutants also affect genes encoding starch degradation enzymes, transcription factors and protein kinases. The comprehensive transcriptome and proteome datasets demonstrate that future system-driven research of the circadian clock requires multi-level experimental approaches. Our work also shows that further work is needed to elucidate the roles of post-translational modifications and protein degradation in the regulation of clock-related processes.

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Ubiquitin-Specific Proteases UBP12 and UBP13 Act in Circadian Clock and Photoperiodic Flowering Regulation in Arabidopsis

Cited by 111 publications

References 58 publications

Multiple Layers of Posttranslational Regulation Refine Circadian Clock Activity in Arabidopsis

Multiple Layers of Posttranslational Regulation Refine Circadian Clock Activity in Arabidopsis

Arabidopsis ubiquitin‐specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency

Parallel analysis ofArabidopsiscircadian clock mutants reveals different scales of transcriptome and proteome regulation

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