SnRK1 Phosphorylation of AL2 Delays Cabbage Leaf Curl Virus Infection in Arabidopsis

Shen, Wei; Dallas, Mary Beth; Goshe, Michael B.; Hanley‐Bowdoin, Linda

doi:10.1128/jvi.00761-14

Cited by 53 publications

(56 citation statements)

References 60 publications

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“…For example, the begomovirus nuclear shuttle protein (NSP)-interacting kinase 1 (NIK1) is able to activate antiviral immunity against cabbage leaf curl virus (CaLCuV) (25,26). Besides the above-mentioned defense mechanisms, host factors such as SNF1-related protein kinase 1 (SnRK1) have also been involved in defense against geminiviruses (27)(28)(29).…”

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confidence: 99%

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

Zhong

Wang

Xiao

et al. 2017

J Virol

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Phosphorylation of the ␤C1 protein encoded by the betasatellite of tomato yellow leaf curl China virus (TYLCCNB-␤C1) by SNF1-related protein kinase 1 (SnRK1) plays a critical role in defense of host plants against geminivirus infection in Nicotiana benthamiana. However, how phosphorylation of TYLCCNB-␤C1 impacts its pathogenic functions during viral infection remains elusive. In this study, we identified two additional tyrosine residues in TYLCCNB-␤C1 that are phosphorylated by SnRK1. The effects of TYLCCNB-␤C1 phosphorylation on its functions as a viral suppressor of RNA silencing (VSR) and a symptom determinant were investigated via phosphorylation mimic mutants in N. benthamiana plants. Mutations that mimic phosphorylation of TYLCCNB-␤C1 at tyrosine 5 and tyrosine 110 attenuated disease symptoms during viral infection. The phosphorylation mimics weakened the ability of TYLCCNB-␤C1 to reverse transcriptional gene silencing and to suppress posttranscriptional gene silencing and abolished its interaction with N. benthamiana ASYMMETRIC LEAVES 1 in N. benthamiana leaves. The mimic phosphorylation of TYLCCNB-␤C1 had no impact on its protein stability, subcellular localization, or self-association. Our data establish an inhibitory effect of phosphorylation of TYLCCNB-␤C1 on its pathogenic functions as a VSR and a symptom determinant and provide a mechanistic explanation of how SnRK1 functions as a host defense factor. IMPORTANCE Tomato yellow leaf curl China virus (TYLCCNV), which causes a severe yellow leaf curl disease in China, is a monopartite geminivirus associated with the betasatellite (TYLCCNB). TYLCCNB encodes a single pathogenicity protein, ␤C1 (TYLCCNB-␤C1), which functions as both a viral suppressor of RNA silencing (VSR) and a symptom determinant. Here, we show that mimicking phosphorylation of TYLCCNB-␤C1 weakens its ability to reverse transcriptional gene silencing, to suppress posttranscriptional gene silencing, and to interact with N. benthamiana ASYMMETRIC LEAVES 1. To our knowledge, this is the first report establishing an inhibitory effect of phosphorylation of TYLCCNB-␤C1 on its pathogenic functions as both a VSR and a symptom determinant and to provide a mechanistic explanation of how SNF1-related protein kinase 1 acts as a host defense factor. These findings expand the scope of phosphorylation-mediated defense mechanisms and contribute to further understanding of plant defense mechanisms against geminiviruses.KEYWORDS TYLCCNB-␤C1, Nicotiana benthamiana, SnRK1, geminivirus, host defense factor, posttranscriptional gene silencing, protein phosphorylation, transcriptional gene silencing

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confidence: 99%

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

Zhong

Wang

Xiao

et al. 2017

J Virol

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“…A further control experiment with a frameshift mutant of HA:AC2 completely excluded promoter and RNA effects as the relevant causes. Although AC2 expression was improved by the avoidance of PTGS, the level of protein was still very low, an experience which was also mentioned recently by other authors (18). Therefore, we believe that this is a more general problem, which is solved for the first time in this study.…”

Section: Discussionmentioning

confidence: 47%

“…The charge parameter can be further modulated by posttranscriptional modifications such as phosphorylation. Interestingly, Shen et al (18) found a differential phosphorylation of AC2 by SnRK, a signaling kinase involved in regulating sugar metabolism (76,77), dependent on the geminivirus species. This implies a change of the AC2 charge in the dependence of the carbohydrate level and a fine-tuning of its effect on replication.…”

Section: Discussionmentioning

confidence: 99%

“…The detection of AC2 proteins in plants is a challenge. So far, AC2 proteins have been investigated by using samples expressed ectopically in vitro (64), in insect cells (17), or in bacteria (18,50,65). Most authors have observed an anomalous migration behavior of the respective proteins.…”

Section: Fig 4 Systemic Agroinfection Of Gfpexpress Plants With Wt Abmentioning

confidence: 99%

“…Phosphorylation of AC2 proteins from cabbage leaf curl virus (CaLCuV) and tomato mottle virus (ToMoV), both New World begomoviruses, was recently shown to be important for infection (18). C2 of tomato yellow leaf curl virus-China (TYLCV-C) (19) was localized to nuclei, whereas TGMV AC2 was found in nuclei and the cytoplasm (20), by using different techniques and cells.…”

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confidence: 99%

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Early Function of the Abutilon Mosaic Virus AC2 Gene as a Replication Brake

Krenz

Deuschle

Deigner

et al. 2015

J Virol

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The C2/AC2 genes of monopartite/bipartite geminiviruses of the genera Begomovirus and Curtovirus encode important pathogenicity factors with multiple functions described so far. A novel function of Abutilon mosaic virus (AbMV) AC2 as a replication brake is described, utilizing transgenic plants with dimeric inserts of DNA B or with a reporter construct to express green fluorescent protein (GFP). Their replicational release upon AbMV superinfection or the individual and combined expression of epitope-tagged AbMV AC1, AC2, and AC3 was studied. In addition, the effects were compared in the presence and in the absence of an unrelated tombusvirus suppressor of silencing (P19). The results show that AC2 suppresses replication reproducibly in all assays and that AC3 counteracts this effect. Examination of the topoisomer distribution of supercoiled DNA, which indicates changes in the viral minichromosome structure, did not support any influence of AC2 on transcriptional gene silencing and DNA methylation. The geminiviral AC2 protein has been detected here for the first time in plants. The experiments revealed an extremely low level of AC2, which was slightly increased if constructs with an intron and a hemagglutinin (HA) tag in addition to P19 expression were used. AbMV AC2 properties are discussed with reference to those of other geminiviruses with respect to charge, modification, and size in order to delimit possible reasons for the different behaviors. IMPORTANCEThe (A)C2 genes encode a key pathogenicity factor of begomoviruses and curtoviruses in the plant virus family Geminiviridae. This factor has been implicated in the resistance breaking observed in agricultural cotton production. AC2 is a multifunctional protein involved in transcriptional control, gene silencing, and regulation of basal biosynthesis. Here, a new function of Abutilon mosaic virus AC2 in replication control is added as a feature of this protein in viral multiplication, providing a novel finding on geminiviral molecular biology.

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AKIN10, a representative Arabidopsis SNF1‐related protein kinase 1 (SnRK1), phosphorylates and downregulates plant HMG‐CoA reductase

et al. 2017

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HMG-CoA reductase (HMGR) is a key enzyme in the mevalonate pathway for sterols and cytosolic isoprenoid production. Although HMGR kinases from spinach, barley, and cauliflower tissues have been strongly suggested as members of SNF1-related protein kinases 1 (SnRK1), the phosphorylation and inactivation of HMGR by plant SnRK1s has not been demonstrated. In this study, we elucidated that AKIN10, an Arabidopsis SnRK1, acts as an HMGR kinase. The recombinant AKIN10 phosphorylates and inactivates AtHMGR1S using recombinant GRIK1 as the AKIN10 activator. In contrast, AKIN10-GRIK1 fails to inactivate AtHMGR1S-S577A, suggesting that this is achieved through Ser577 phosphorylation. Moreover, phosphorylation is detected not only in AtHMGR1S but also in AtHMGR1S-S577A, suggesting the presence of a novel regulatory mechanism of plant HMGR.

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SnRK1 Phosphorylation of AL2 Delays Cabbage Leaf Curl Virus Infection in Arabidopsis

Cited by 53 publications

References 60 publications

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant

Early Function of the Abutilon Mosaic Virus AC2 Gene as a Replication Brake

AKIN10, a representative Arabidopsis SNF1‐related protein kinase 1 (SnRK1), phosphorylates and downregulates plant HMG‐CoA reductase

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