Phosphorylation of TGB1 by protein kinase CK2 promotes barley stripe mosaic virus movement in monocots and dicots

Hu, Yingzhe; Li, Zhenggang; Cheng, Yuan; Jin, Xuejiao; Yan, Li; Zhao, Xiaofei; Zhang, Yong Liang; Jackson, Andrew O.; Wang, Xianbing; Han, Chenggui; Yu, Jialin; Li, Dawei

doi:10.1093/jxb/erv237

Cited by 42 publications

(50 citation statements)

References 64 publications

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“…S8). Although phosphorylation of some viral proteins does not appear to affect RNA binding (Hu et al ., ; Zhao et al ., ), in other cases, the ability to bind RNA is conditioned by the phosphorylation status (Hoover et al ., ; Hung et al ., ; Stork et al ., ; Vijayapalani et al ., ); finally, both circumstances can coexist in the same protein (Makarov et al ., ). Phosphorylation at Thr‐242 down‐regulates PVA CP RNA‐binding activity (Ivanov et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Phosphorylation coexists with O‐GlcNAcylation in a plant virus protein and influences viral infection

Martínez-Turiño

Pérez

Hervás

et al. 2018

Molecular Plant Pathology

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Phosphorylation and O-GlcNAcylation are two widespread post-translational modifications (PTMs), often affecting the same eukaryotic target protein. Plum pox virus (PPV) is a member of the genus Potyvirus which infects a wide range of plant species. O-GlcNAcylation of the capsid protein (CP) of PPV has been studied extensively, and some evidence of CP phosphorylation has also been reported. Here, we use proteomics analyses to demonstrate that PPV CP is phosphorylated in vivo at the N-terminus and the beginning of the core region. In contrast with the 'yin-yang' mechanism that applies to some mammalian proteins, PPV CP phosphorylation affects residues different from those that are O-GlcNAcylated (serines Ser-25, Ser-81, Ser-101 and Ser-118). Our findings show that PPV CP can be concurrently phosphorylated and O-GlcNAcylated at nearby residues. However, an analysis using a differential proteomics strategy based on iTRAQ (isobaric tags for relative and absolute quantitation) showed a significant enhancement of phosphorylation at Ser-25 in virions recovered from O-GlcNAcylation-deficient plants, suggesting that crosstalk between O-GlcNAcylation and phosphorylation in PPV CP takes place. Although the preclusion of phosphorylation at the four identified phosphotarget sites only had a limited impact on viral infection, the mimicking of phosphorylation prevents PPV infection in Prunus persica and weakens infection in Nicotiana benthamiana and other herbaceous hosts, prompting the emergence of potentially compensatory second mutations. We postulate that the joint action of phosphorylation and O-GlcNAcylation in the N-proximal segment of CP allows a fine-tuning of protein stability, providing the amount of CP required in each step of viral infection.

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Section: Discussionmentioning

confidence: 99%

Phosphorylation coexists with O‐GlcNAcylation in a plant virus protein and influences viral infection

Martínez-Turiño

Pérez

Hervás

et al. 2018

Molecular Plant Pathology

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“…In vitro transcription followed by viral RNA inoculation was performed as previously described (Lee et al ., ; Hu et al ., ). Briefly, transcripts of RNA α, β and γ were mixed at a molar ratio of 1 : 1 : 1, added with equal amounts of FES inoculation buffer (0.06 M potassium phosphate, 0.1 M glycine, 1% bentonite, 1% sodium pyrophosphate decahydrate, 1% celite, pH 8.5), and then inoculated onto the leaves of 7‐ to 10‐d‐old barley and wheat seedlings.…”

Section: Methodsmentioning

confidence: 97%

“…The pET‐30a‐γb plasmid or its derivatives were transformed into Escherichia coli strain BL21 (DE3). The recombinant proteins were purified as described previously (Hu et al ., ; Zhao et al ., ). Briefly, the transformed bacteria were resuspended in T buffer containing 20 mM Tris‐HCl (pH 9.0), 500 mM NaCl, 10% glycerol, 0.1% Triton X‐100 and 1 mM PMSF, then disrupted by ultrasonication.…”

Section: Methodsmentioning

confidence: 97%

“…Nicotiana benthamiana Domin plants were grown in a climate chamber with a 14 h : 10 h, light : dark photoperiod at 23–25°C as described previously (Yuan et al ., ). Barley ( Hordeum vulgare L.) (Yangfu 4056) and wheat ( Triticum aestivum L.) (Yangmai 158) were grown in a glasshouse until the two‐leaf stage and then transferred to a climate chamber after inoculation with BSMV (Lee et al ., ; Hu et al ., ).…”

Section: Methodsmentioning

confidence: 99%

“…For example, early studies on Tobacco mosaic virus (TMV) showed that its movement protein (MP) is phosphorylated by a cell wall‐associated kinase that facilitates viral cell‐to‐cell transport through plasmodesmata (Citovsky et al ., ; Karpova et al ., ; Waigmann et al ., ). Phosphorylation of viral movement proteins was then shown to be a common strategy that enables plant viruses to spread (Modena et al ., ; Link et al ., ; Samuilova et al ., ; Hu et al ., ). Various viral proteins with distinct functions are phosphorylated during viral infection, including RNA‐dependent RNA polymerase (RdRp) (Kim et al ., ; Jakubiec et al ., ; Jakubiec & Jupin, ), coat protein (CP) (Ivanov et al ., ; Hung et al ., ; Zhao et al ., ), and proteins that suppress RNA silencing and symptom development (Lewsey et al ., ; Shen et al ., , ; Zhong et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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Barley stripe mosaic virus infection requires PKA‐mediated phosphorylation of γb for suppression of both RNA silencing and the host cell death response

Zhang

Dong

et al. 2018

New Phytologist

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The Barley stripe mosaic virus (BSMV) γb protein is a viral suppressor of RNA silencing (VSR) and symptom determinant. However, it is unclear how post-translational modification affects the different functions of γb. Here, we demonstrate that γb is phosphorylated at Ser-96 by a PKA-like kinase in vivo and in vitro. Mutant viruses containing a nonphosphorylatable substitution (BSMV or BSMV ) exhibited reduced viral accumulation in Nicotiana benthamiana due to transient induction of the cell death response that constrained the virus to necrotic areas. By contrast, a BSMV mutant virus that mimics γb phosphorylation spread similarly to the wild-type virus. Furthermore, the S96A mutant had reduced local and systemic γb VSR activity due to having compromised its binding activity to 21-bp dsRNA. However, overexpression of other VSRs in trans or in cis failed to rescue the necrosis induced by BSMV , demonstrating that suppression of cell death by γb phosphorylation is functionally distinct from its RNA silencing suppressor activities. These results provide new insights into the function of γb phosphorylation in regulating RNA silencing and the BSMV-induced host cell death response, and contribute to our understanding of how the virus optimizes the balance between viral replication and virus survival in the host plants during virus infection.

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Identification and manipulation of host factors for the control of plant viruses

Tang

Bernards

Wang

2020

Applied Plant Virology

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Phosphorylation of TGB1 by protein kinase CK2 promotes barley stripe mosaic virus movement in monocots and dicots

Abstract: HighlightCK2 phosphorylation of the TGB1 protein has a critical role in promoting barley stripe mosaic virus movement in monocots and dicots by affecting the interactions between TGB1 and TGB3 proteins.

Cited by 42 publications

References 64 publications

Phosphorylation coexists with O‐GlcNAcylation in a plant virus protein and influences viral infection

Phosphorylation coexists with O‐GlcNAcylation in a plant virus protein and influences viral infection

Barley stripe mosaic virus infection requires PKA‐mediated phosphorylation of γb for suppression of both RNA silencing and the host cell death response

Identification and manipulation of host factors for the control of plant viruses

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