Ubiquitin carboxyl-terminal hydrolases are required for period maintenance of the circadian clock at high temperature in Arabidopsis

Ryosuke Hayama,George Coupland,Federico Valverde,Tsuyoshi Mizoguchi,Peizhen Yang,Richard D Vierstra,Ikuyo Furutani-Hayama

doi:10.1038/s41598-019-53229-8

Ryosuke Hayama, George Coupland + Show 5 more

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https://doi.org/10.1038/s41598-019-53229-8

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Protein ubiquitylation participates in a number of essential cellular processes including signal transduction and transcription, often by initiating the degradation of specific substrates through the 26S proteasome. Within the ubiquitin-proteasome system, deubiquitylating enzymes (DUBs) not only help generate and maintain the supply of free ubiquitin monomers, they also directly control functions and activities of specific target proteins by modulating the pool of ubiquitylated species. Ubiquitin carboxyl-terminal hydrolases (UCHs) belong to an enzymatic subclass of DUBs, and are represented by three members in Arabidopsis, UCH1, UCH2 and UCH3. UCH1 and UCH2 influence auxin-dependent developmental pathways in Arabidopsis through their deubiquitylation activities, whereas biological and enzymatic functions of UCH3 remain unclear. Here, we demonstrate that Arabidopsis UCH3 acts to maintain the period of the circadian clock at high temperatures redundantly with UCH1 and UCH2. Whereas single uch1, uch2 and uch3 mutants have weak circadian phenotypes, the triple uch mutant displays a drastic lengthening of period at high temperatures that is more extreme than the uch1 uch2 double mutant. UCH3 also possesses a broad deubiquitylation activity against a range of substrates that link ubiquitin via peptide and isopeptide linkages. While the protein target(s) of UCH1-3 are not yet known, we propose that these DUBs act on one or more factors that control period length of the circadian clock through removal of their bound ubiquitin moieties, thus ensuring that the clock oscillates with a proper period even at elevated temperatures.

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Selective attachment of ubiquitin is a critical post-translational modification that regulates diverse cellular processes and signaling pathways
This screen was performed in CO overexpressor plants and this role for UCH3 could not be confirmed in wild-type plants, but we found that UCH3, together with UCH1 and UCH2, strongly influences the period of circadian rhythms especially at high temperature
UCH3 was originally identified in a mutant screen as a candidate gene that controls photoperiodic flowering in Arabidopsis thaliana

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Selective attachment of ubiquitin is a critical post-translational modification that regulates diverse cellular processes and signaling pathways. Within the UCH subfamily, Arabidopsis uch[1] and uch[2] mutants exhibit altered shoot architecture[17] These two UCHs impact the turnover of AXR3, a major regulator in the auxin response pathway, implying their direct role for de-ubiquitylation of one or more ubiquitin substrates that modulate auxin signaling[17]. UCH3 was originally identified through a mutant screen as a candidate gene necessary for activation of A. thaliana CONSTANS (CO), a key transcription factor that promotes flowering under long-day (LD) conditions This screen was performed in CO overexpressor plants and this role for UCH3 could not be confirmed in wild-type plants, but we found that UCH3, together with UCH1 and UCH2, strongly influences the period of circadian rhythms especially at high temperature. We propose that this set of Arabidopsis DUBs helps maintain the period of the circadian clock at high temperature, sustaining appropriate period length at elevated temperatures

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