Characterization of the Arabidopsis thaliana E3 Ubiquitin-Ligase AtSINAL7 and Identification of the Ubiquitination Sites

Peralta, Diego A.; Araya, Alejandro; Nardi, Cristina Fernanda; Busi, María V.; Gómez-Casati, Diego F.

doi:10.1371/journal.pone.0073104

Cited by 11 publications

(7 citation statements)

References 42 publications

(49 reference statements)

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“…The conserved SINA proteins possess two characteristic domains, an N‐terminal RING‐type zinc finger domain and a C‐terminal TRAF‐like substrate‐binding domain (Hu and Fearon, ; Polekhina et al ., ). Plant SINA‐related proteins were reported to have E3 ubiquitin ligase activity (Xie et al ., ; Ning et al ., ; Peralta et al ., ) and are involved in the regulation of stress responses (Kim et al ., ; Ning et al ., ; Bao et al ., ). Because of the high sequence similarity between RAP2.12 and the SINAT2‐interacting RAP2.2 protein, we decided to test whether SINAT2 may influence RAP2.12 protein levels.…”

Section: Resultsmentioning

confidence: 99%

“…A number of RING domain proteins were reported to be responsible for polyubiquitination and subsequent degradation of key transcriptional regulators of stress and ABA responses (Qin et al ., ; Bu et al ., ; Cheng et al ., ; Liu and Stone, ). In Arabidopsis, the SINA group of putative E3 ubiquitin ligases includes 18 proteins: SINAT1–5, SINA‐like 1–11, SINA and PEX14 (Peralta et al ., ). These proteins carry conserved RING‐finger and TNF RECEPTOR ASSOCIATED FACTOR (TRAF)‐like domains, the latter is necessary for substrate binding and dimerization (Hu and Fearon, ; Polekhina et al ., ).…”

Section: Discussionmentioning

confidence: 97%

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The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12,RAP2.2 and RAP2.3

et al. 2015

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SUMMARYThe ethylene response factor VII (ERF-VII) transcription factor RELATED TO APETALA2.12 (RAP2.12) was previously identified as an activator of the ALCOHOL DEHYDROGENASE1 promoter::luciferase (ADH1-LUC) reporter gene. Here we show that overexpression of RAP2.12 and its homologues RAP2.2 and RAP2.3 sustains ABA-mediated activation of ADH1 and activates hypoxia marker genes under both anoxic and normoxic conditions. Inducible expression of all three RAP2s conferred tolerance to anoxia, oxidative and osmotic stresses, and enhanced the sensitivity to abscisic acid (ABA). Consistently, the rap2.12-2 rap2.3-1 double mutant showed hypersensitivity to both submergence and osmotic stress. These findings suggest that the three ERF-VII-type transcription factors play roles in tolerance to multiple stresses that sequentially occur during and after submergence in Arabidopsis. Oxygen-dependent degradation of RAP2.12 was previously shown to be mediated by the N-end rule pathway. During submergence the RAP2.12, RAP2.2 and RAP2.3 are stabilized and accumulates in the nucleus affecting the transcription of stress response genes. We conclude that the stabilized RAP2 transcription factors can prolong the ABA-mediated activation of a subset of osmotic responsive genes (e.g. ADH1). We also show that RAP2.12 protein level is affected by the REALLY INTERESTING GENE (RING) domain containing SEVEN IN ABSENTIA of Arabidopsis thaliana 2 (SINAT2). Silencing of SINAT1/2 genes leads to enhanced RAP2.12 abundance independently of the presence or absence of its N-terminal degron. Taken together, our results suggest that RAP2.12 and its homologues RAP2.2 and RAP2.3 act redundantly in multiple stress responses. Alternative protein degradation pathways may provide inputs to the RAP2 transcription factors for the distinct stresses.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 97%

The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12,RAP2.2 and RAP2.3

et al. 2015

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“…SINAT5 ubiquitinates the NAC1 transcription factor promoting its degradation, thereby attenuating the auxin‐induced lateral root formation (Xie et al ., ); SINAT5 may also play a role in the regulation of flowering time through controlling the stability of late elongated hypocotyl and flowering locus C (Park et al ., ; Park et al ., ). In addition, a SINA‐like protein SINAL7 has been shown to play an important role in flower development (Peralta, Araya, Nardi, Busi, & Gomez‐Casati, ). In rice, six SINA genes are predicted in the genome, but only one, termed OsDIS1 , is found to play a negative role in drought stress tolerance, presumably through ubiquitination of the kinase OsNek6 (Ning et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Functional analysis of the seven in absentia ubiquitin ligase family in tomato

Wang

Fan

Niu

et al. 2018

Plant Cell & Environment

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Seven in absentia (SINA) protein is one subgroup of ubiquitin ligases possessing an N-terminal cysteine-rich really interesting new gene (RING) domain, two zinc-finger motifs, and a C-terminal domain responsible for substrate-binding and dimerization. In tomato (Solanum lycopersicum), the SINA gene family has six members, and we characterize in this study all tomato SINA (SlSINA) genes and the gene products. Our results show that SlSINA genes are differentially regulated in leaf, bud, stem, flower, and root. All SlSINA proteins possess RING-dependent E3 ubiquitin ligase activity, exhibiting similar specificity towards the E2 ubiquitin-conjugating enzyme. SlSINA1/3/4/5/6 are localized in both cytoplasm and nucleus, whereas SlSINA2 is exclusively localized in the nucleus. Moreover, all SlSINAs can interact with each other for homo- or hetero-dimerization. The functionality of SlSINA proteins has been investigated. SlSINA4 plays a positive role in defense signalling, as manifested by elicitation of E3-dependent hypersensitive response-like cell death; the other SlSINAs are negative regulator and capable to suppress hypersensitive response cell death. Transgenic tomato plants overexpressing SlSINA2 exhibit pale-green leaf phenotype, suggesting SlSINA2 regulates chlorophyll level in plant cells, whereas transgenic tomato plants overexpressing SlSINA5 have altered floral structure with exserted stigma, implicating SlSINA5 plays a role in flower development.

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“…In the nucleus, GAPDH stabilizes Siah1 facilitating its degradation activity of nuclear substrates, which leads to the induction of the cell death cascade. As in mammals, plant GAPDH interacts with an Siah1-like E3-ubiquitin ligase, namely seven in absentia-like 7 (Sinal7), also responsible for its nuclear translocation ( 137 ). When Sinal7 is lacking in a knockout line, GADPH does not appear in the nucleus, indicating that nuclear import of GAPDH is mediated indirectly by binding to Sinal7 as originally described for Siah1 in mammalian cells ( 69 ).…”

Section: Cytosolic Enzymes Take Over Multiple Roles In the Nucleusmentioning

confidence: 99%

Central Metabolism in Mammals and Plants as a Hub for Controlling Cell Fate

Selinski

Scheibe

2021

Antioxidants & Redox Signaling

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Significance: The importance of oxidoreductases in energy metabolism together with the occurrence of enzymes of central metabolism in the nucleus gave rise to the active research field aiming to understand moonlighting enzymes that undergo post-translational modifications (PTMs) before carrying out new tasks. Recent Advances: Cytosolic enzymes were shown to induce gene transcription after PTM and concomitant translocation to the nucleus. Changed properties of the oxidized forms of cytosolic glyceraldehyde 3-phosphate dehydrogenase, and also malate dehydrogenases and others, are the basis for a hypothesis suggesting moonlighting functions that directly link energy metabolism to adaptive responses required for maintenance of redox-homeostasis in all eukaryotes. Critical Issues: Small molecules, such as metabolic intermediates, coenzymes, or reduced glutathione, were shown to fine-tune the redox switches, interlinking redox state, metabolism, and induction of new functions via nuclear gene expression. The cytosol with its metabolic enzymes connecting energy fluxes between the various cell compartments can be seen as a hub for redox signaling, integrating the different signals for graded and directed responses in stressful situations. Future Directions: Enzymes of central metabolism were shown to interact with p53 or the assumed plant homologue suppressor of gamma response 1 (SOG1), an NAM, ATAF, and CUC transcription factor involved in the stress response upon ultraviolet exposure. Metabolic enzymes serve as sensors for imbalances, their inhibition leading to changed energy metabolism, and the adoption of transcriptional coactivator activities. Depending on the intensity of the impact, rerouting of energy metabolism, proliferation, DNA repair, cell cycle arrest, immune responses, or cell death will be induced. Antioxid. Redox Signal. 34, 1025–1047.

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Characterization of the Arabidopsis thaliana E3 Ubiquitin-Ligase AtSINAL7 and Identification of the Ubiquitination Sites

Cited by 11 publications

References 42 publications

The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12,RAP2.2 and RAP2.3

The low oxygen, oxidative and osmotic stress responses synergistically act through the ethylene response factor VII genes RAP2.12,RAP2.2 and RAP2.3

Functional analysis of the seven in absentia ubiquitin ligase family in tomato

Central Metabolism in Mammals and Plants as a Hub for Controlling Cell Fate

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