The prolific ATL family of RING-H2 ubiquitin ligases

Guzmán, Plinio

doi:10.4161/psb.20851

Cited by 64 publications

(56 citation statements)

References 53 publications

(52 reference statements)

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“…The ubiquitin ligase ATL is a plant-specific multigene family and widely conserved in basal and higher plants, including mosses, monocots, and dicots (21). The Arabidopsis genome contains 91 members of the ATL proteins (22). Recently, several ATL proteins have been reported to function in multiple environmental stress adaptation (22).…”

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confidence: 99%

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Phosphorylation of Arabidopsis Ubiquitin Ligase ATL31 Is Critical for Plant Carbon/Nitrogen Nutrient Balance Response and Controls the Stability of 14-3-3 Proteins

Yasuda

Sato

Maekawa

et al. 2014

Journal of Biological Chemistry

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Background: Ubiquitin ligase ATL31 and the target, 14-3-3 proteins, function in plant nutrient response. Results: ATL31 binds to 14-3-3 proteins via phosphorylation of specific residues. These residues are essential for the function of ATL31. Conclusion: ATL31 targets 14-3-3 proteins for degradation in a phosphorylation-dependent manner to regulate nutrient response. Significance: Phosphorylation of ubiquitin ligase ATL31 controls plant nutrient response.

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confidence: 99%

“…The Arabidopsis genome contains 91 members of the ATL proteins (22). Recently, several ATL proteins have been reported to function in multiple environmental stress adaptation (22). ATL2, ATL9, and ATL55/RING1 are involved in plant defense response, and ATL78 mediates adaptation to cold stress (23)(24)(25)(26).…”

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confidence: 99%

Phosphorylation of Arabidopsis Ubiquitin Ligase ATL31 Is Critical for Plant Carbon/Nitrogen Nutrient Balance Response and Controls the Stability of 14-3-3 Proteins

Yasuda

Sato

Maekawa

et al. 2014

Journal of Biological Chemistry

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“…Although EDR1 accumulated very poorly in these assays, we were able to immunoprecipitate EDR1 and observed a clear coimmunoprecipitation with ATL1 (Supplemental Figure 1A). ATL1 belongs to a family of RING finger E3 ubiquitin ligases that consists of 91 members in Arabidopsis (Salinas- Mondragón et al, 1999;Morris et al, 2010;Aguilar-Hernández et al, 2011;Guzmán, 2012). Members of the ATL family all contain an N-terminal transmembrane domain followed by a RING-H2 type E3 ligase domain (Aguilar-Hernández et al, 2011;Guzmán, 2012).…”

Section: Edr1 Physically Associates With Atl1 In the Tgn/eementioning

confidence: 99%

“…ATL1 belongs to a family of RING finger E3 ubiquitin ligases that consists of 91 members in Arabidopsis (Salinas- Mondragón et al, 1999;Morris et al, 2010;Aguilar-Hernández et al, 2011;Guzmán, 2012). Members of the ATL family all contain an N-terminal transmembrane domain followed by a RING-H2 type E3 ligase domain (Aguilar-Hernández et al, 2011;Guzmán, 2012). Functional analyses of several ATL family members in Arabidopsis indicate that they play important roles in diverse biological processes, including defense responses, growth phase transitions, endosperm development, regulation of cell death during root development, and photoperiod response (Serrano and Guzmán, 2004;Pagnussat et al, 2005;Lin et al, 2008;Sato et al, 2009;Berrocal-Lobo et al, 2010;Morris et al, 2010;Guzmán, 2012).…”

Section: Edr1 Physically Associates With Atl1 In the Tgn/eementioning

confidence: 99%

TheArabidopsisEDR1 Protein Kinase Negatively Regulates the ATL1 E3 Ubiquitin Ligase to Suppress Cell Death

Serrano

Dong

et al. 2014

Plant Cell

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Loss-of-function mutations in the Arabidopsis thaliana ENHANCED DISEASE RESISTANCE1 (EDR1) gene confer enhanced programmed cell death under a variety of abiotic and biotic stress conditions. All edr1 mutant phenotypes can be suppressed by missense mutations in the KEEP ON GOING gene, which encodes a trans-Golgi network/early endosome (TGN/EE)-localized E3 ubiquitin ligase. Here, we report that EDR1 interacts with a second E3 ubiquitin ligase, ARABIDOPSIS TOXICOS EN LEVADURA1 (ATL1), and negatively regulates its activity. Overexpression of ATL1 in transgenic Arabidopsis induced severe growth inhibition and patches of cell death, while transient overexpression in Nicotiana benthamiana leaves induced cell death and tissue collapse. The E3 ligase activity of ATL1 was required for both of these processes. Importantly, we found that ATL1 interacts with EDR1 on TGN/EE vesicles and that EDR1 suppresses ATL1-mediated cell death in N. benthamiana and Arabidopsis. Lastly, knockdown of ATL1 expression suppressed cell death phenotypes associated with the edr1 mutant and made Arabidopsis hypersusceptible to powdery mildew infection. Taken together, our data indicate that ATL1 is a positive regulator of programmed cell death and EDR1 negatively regulates ATL1 activity at the TGN/EE and thus controls stress responses initiated by ATL1-mediated ubiquitination events.

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“…The Arabidopsis Tóxicos en Levadura (ATL) gene family encodes plant-specific putative RING-type ubiquitin ligases with a transmembrane domain and is composed of 91 and 121 members in Arabidopsis and rice, respectively (Aguilar-Hernández et al 2011;Guzmán 2012;Koiwai et al 2007). ATL31 and its closest homolog ATL6 have been reported to play important roles in the carbon/nitrogen (C/N)-nutrient response by regulating the stability of 14-3-3 proteins through ubiquitination (Sato et al 2009(Sato et al , 2011.…”

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confidence: 99%

The <i>Arabidopsis</i> ubiquitin ligase <i>ATL31</i> is transcriptionally controlled by WRKY33 transcription factor in response to pathogen attack

Reyes

Maekawa

Sato

et al. 2015

Plant Biotechnology

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ATL31, an Arabidopsis RING-type ubiquitin ligase, plays a critical role in plant carbon/nitrogen (C/N)-nutrient responses during post-germinative growth and in defense responses to pathogen attack. ATL31 expression under these stress conditions suggested the presence of transcriptional regulators mediated by these stress signals. We recently reported that the expression pattern of WRKY33, a transcription factor involved in plant defense responses, is highly correlated with that of ATL31. In this study, we investigated the detailed relationship between the ATL31 gene and WRKY33. Using transient reporter analysis, we found that WRKY33 could significantly activate ATL31 transcription in plant cells. Transcript analysis of stable transgenic Arabidopsis plants overexpressing WRKY33 confirmed that the expression of ATL31 in response to the PAMPs flg22 and chitin was enhanced compared with wild-type plants, while expression was repressed in wrky33 mutants. Further detailed transient reporter analysis revealed that transactivation by WRKY33 is required and mediated through a specific W-box cis-acting element in the promoter region of the ATL31 gene. In contrast, WRKY33 did not regulate ATL31 expression during the C/N response. Taken together, these results demonstrate that WRKY33 acts as a transcription factor of ATL31 and positively regulates its expression during activation of plant defense responses.

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The prolific ATL family of RING-H2 ubiquitin ligases

Cited by 64 publications

References 53 publications

Phosphorylation of Arabidopsis Ubiquitin Ligase ATL31 Is Critical for Plant Carbon/Nitrogen Nutrient Balance Response and Controls the Stability of 14-3-3 Proteins

Phosphorylation of Arabidopsis Ubiquitin Ligase ATL31 Is Critical for Plant Carbon/Nitrogen Nutrient Balance Response and Controls the Stability of 14-3-3 Proteins

TheArabidopsisEDR1 Protein Kinase Negatively Regulates the ATL1 E3 Ubiquitin Ligase to Suppress Cell Death

The <i>Arabidopsis</i> ubiquitin ligase <i>ATL31</i> is transcriptionally controlled by WRKY33 transcription factor in response to pathogen attack

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