Cytoplasmic Degradation of the Arabidopsis Transcription Factor ABSCISIC ACID INSENSITIVE 5 Is Mediated by the RING-type E3 Ligase KEEP ON GOING

Liu, Hongxia; Stone, Sophia L.

doi:10.1074/jbc.m113.465369

Cited by 113 publications

(112 citation statements)

References 33 publications

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“…A. tumefaciens strain GV3101 transformed with the appropriate binary plasmids was grown and prepared for transient expression as described previously (Sparkes et al, 2006;Liu and Stone, 2013). Briefly, A. tumefaciens cultures were resuspended in infiltration solution (5 mg mL 21 D-Glc, 50 mM MES, 2 mM Na 3 PO 4 , and 0.1 mM acetosyringone) at an optical density at 600 nm of 0.8.…”

Section: Transient Protein Expression In Tobaccomentioning

confidence: 99%

The RING-Type E3 Ligase XBAT35.2 Is Involved in Cell Death Induction and Pathogen Response

et al. 2017

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XBAT35 belongs to a subfamily of Arabidopsis (Arabidopsis thaliana) RING-type E3s that are similar in domain architecture to the rice (Oryza sativa) XA21 Binding Protein3, a defense protein. The XBAT35 transcript undergoes alternative splicing to produce two protein isoforms, XBAT35.1 and XBAT35.2. Here, we demonstrate that XBAT35.2 localizes predominantly to the Golgi and is involved in cell death induction and pathogen response. XBAT35.2, but not XBAT35.1, was found to trigger cell death when overexpressed in tobacco (Nicotiana benthamiana) leaves and does so in a manner that requires its RING domain. Loss of XBAT35 gene function disrupts the plant's ability to defend against pathogen attack, whereas overexpression of XBAT35.2 enhances resistance to pathogens. XBAT35.2 was found to be unstable and promotes its own degradation, suggesting self-regulation. Inoculation with virulent and avirulent strains of the bacterial pathogen Pseudomonas syringae pv tomato DC3000 results in a drastic reduction in the levels of ubiquitinated XBAT35.2 and an increase in the abundance of the E3. This implies that pathogen infection prohibits XBAT35.2 self-regulation and stabilizes the E3. In agreement with a role in defending against pathogens, XBAT35.2 interacts with defense-related Accelerated Cell Death11 (ACD11) in planta and promotes the proteasome-dependent turnover of ACD11 in cell-free degradation assays. In accordance with regulation by a stabilized XBAT35.2, the levels of ubiquitinated ACD11 increased considerably, and the abundance of ACD11 was reduced following pathogen infection. In addition, treatment of transgenic seedlings with a proteasome inhibitor results in the accumulation of ACD11, confirming proteasome-dependent degradation. Collectively, these results highlight a novel role for XBAT35.2 in cell death induction and defense against pathogens.Posttranslational modification (PTM) via ubiquitination plays essential regulatory roles in all eukaryotic cells. The selective attachment of ubiquitin serves as a versatile modification that regulates protein activity, abundance, sorting, and localization (Deshaies and Joazeiro, 2009;Komander and Rape, 2012). This versatility places ubiquitination at the center of numerous cellular processes and allows for the regulation of growth, development, and responses to various environmental stimuli. Ubiquitination is accomplished through the sequential action of three enzymes: E1 (ubiquitin-activating enzyme), E2 (ubiquitin-conjugating enzyme), and E3 (ubiquitin ligase). Ubiquitin conjugation begins with the activation of ubiquitin molecules by E1, which is then transferred to E2, forming a thioester-linked E2-ubiquitin intermediate. Finally, E3 mediates the transfer of ubiquitin from the E2-ubiquitin intermediate to the substrate. The covalent attachment of ubiquitin to the substrate is usually accomplished via the formation of an isopeptide bond between the C-terminal Gly of ubiquitin and an internal lysine (Lys) of the substrate. Substrate modifications include the

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Section: Transient Protein Expression In Tobaccomentioning

confidence: 99%

The RING-Type E3 Ligase XBAT35.2 Is Involved in Cell Death Induction and Pathogen Response

et al. 2017

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“…The Arabidopsis genome is predicted to contain more than 460 RING-containing proteins (Stone et al, 2005). Although the function of several RING proteins has been studied extensively (Dong et al, 2006;Stone et al, 2006;Lau and Deng, 2012;Lazaro et al, 2012Lazaro et al, , 2015Liu and Stone, 2013;Lee and Seo, 2015;Pauwels et al, 2015;Wang et al, 2015a), the E3 ligase activity and the targets of most RING proteins in Arabidopsis have yet to be elucidated.…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis RING-Type E3 Ligase TEAR1 Controls Leaf Development by Targeting the TIE1 Transcriptional Repressor for Degradation

et al. 2017

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The developmental plasticity of leaf size and shape is important for leaf function and plant survival. However, the mechanisms by which plants form diverse leaves in response to environmental conditions are not well understood. Here, we identified TIE1-ASSOCIATED RING-TYPE E3 LIGASE1 (TEAR1) and found that it regulates leaf development by promoting the degradation of TCP INTERACTOR-CONTAINING EAR MOTIF PROTEIN1 (TIE1), an important repressor of CINCINNATA (CIN)-like TEOSINTE BRANCHED1/CYCLOIDEA/PCF (TCP) transcription factors, which are key for leaf development. TEAR1 contains a typical C3H2C3-type RING domain and has E3 ligase activity. We show that TEAR1 interacts with the TCP repressor TIE1, which is ubiquitinated in vivo and degraded by the 26S proteasome system. We demonstrate that TEAR1 is colocalized with TIE1 in nuclei and negatively regulates TIE1 protein levels. Overexpression of TEAR1 rescued leaf defects caused by TIE1 overexpression, whereas disruption of TEAR1 resulted in leaf phenotypes resembling those caused by TIE1 overexpression or TCP dysfunction. Deficiency in TEAR partially rescued the leaf defects of TCP4 overexpression line and enhanced the wavy leaf phenotypes of jaw-5D. We propose that TEAR1 positively regulates CIN-like TCP activity to promote leaf development by mediating the degradation of the TCP repressor TIE1.

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“…KEG is a RING-finger E3 ligase that has been previously shown to regulate abscisic acid signaling through mediating degradation of the transcription factors ABSCISIC ACID INSENSITIVE5 (ABI5), ABA BINDING FACTOR1 (ABF1), and ABF3 (Stone et al, 2006;Liu and Stone, 2010;Chen et al, 2013). We have previously shown that KEG physically associates with the kinase domain of EDR1 on trans-Golgi network/early endosome (TGN/EE) vesicles , while Liu and Stone (2013) have recently shown that KEG physically associates with ABI5 on TGN/EE vesicles. Together, these data suggest that EDR1 may function at the TGN/EE and regulate the E3 ligase activity of KEG.…”

Section: Introductionmentioning

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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Cytoplasmic Degradation of the Arabidopsis Transcription Factor ABSCISIC ACID INSENSITIVE 5 Is Mediated by the RING-type E3 Ligase KEEP ON GOING

Cited by 113 publications

References 33 publications

The RING-Type E3 Ligase XBAT35.2 Is Involved in Cell Death Induction and Pathogen Response

The RING-Type E3 Ligase XBAT35.2 Is Involved in Cell Death Induction and Pathogen Response

The Arabidopsis RING-Type E3 Ligase TEAR1 Controls Leaf Development by Targeting the TIE1 Transcriptional Repressor for Degradation

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

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