O-GlcNAc modification of the coat protein of the potyvirus Plum pox virus enhances viral infection

Pérez, José de Jesús; Udeshi, Namrata D.; Shabanowitz, Jeffrey; Ciordia, Sergio; Juárez, Silvia; Scott, Cheryl L.; Olszewski, Neil E.; Hunt, Donald F.; Garcı́a, Juan Antonio

doi:10.1016/j.virol.2013.03.029

Cited by 34 publications

(41 citation statements)

References 36 publications

(64 reference statements)

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“…(B) Scheme of PPV CP and its post‐translational modifications (PTMs). Distribution of phosphorylated residues (red ellipses) and previously mapped O ‐GlcNAcylated amino acids (blue hexagons; Pérez et al ., ). Trypsin/Lys‐C peptides in which the PTMs were identified are specified beneath the PPV CP map.…”

Section: Resultsmentioning

confidence: 97%

“…Phosphorylation at Ser residues 25, 81, 101 and 118 takes place alongside the previously described O ‐GlcNAcylation, which also modifies the N‐terminal part of PPV CP at Thr residues 19, 24, 41, 50, 53, 54/58 and Ser‐65 (Kim et al ., ; Pérez et al ., ). Residues susceptible to phosphorylation differ from those that can be O ‐GlcNAcylated (Fig.…”

Section: Resultsmentioning

confidence: 97%

“…The PPV CP is O ‐GlcNAcylated by the OGT SEC (Chen et al ., ; Fernández‐Fernández et al ., ). Seven Thr residues and one Ser that are modified by O ‐GlcNAcylation or influence the modification of other residues have been identified in the N‐terminal region of PPV CP (Kim et al ., ; Pérez et al ., ; Scott et al ., ). Although O‐ GlcNAcylation of PPV CP is not essential for virus viability, it enhances viral infection (Chen et al ., ; Pérez et al ., ).…”

Section: Introductionmentioning

confidence: 98%

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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: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 98%

See 1 more Smart Citation

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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“…On the other hand, O-GlcNAcylation modifications carried out by the host protein SECRET AGENT were also found in PPV CP (59,62). Interestingly, a mutagenic approach showed that O-GlcNAcylation might have a role in virion assembly and/or stability (63). Hence, the involvement of HCPro in the regulation of virion assembly by modulation of posttranslational modifications of CP is an attractive possibility that is worthy of exploration in the future.…”

Section: Discussionmentioning

confidence: 99%

A Novel Role of the Potyviral Helper Component Proteinase Contributes To Enhance the Yield of Viral Particles

Vallí

Gallo

Calvo

et al. 2014

J Virol

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The helper component proteinase (HCPro) is an indispensable, multifunctional protein of members of the genus Potyvirus and other viruses of the family Potyviridae. This viral factor is directly involved in diverse steps of viral infection, such as aphid transmission, polyprotein processing, and suppression of host antiviral RNA silencing. In this paper, we show that although a chimeric virus based on the potyvirus Plum pox virus lacking HCPro, which was replaced by a heterologous silencing suppressor, caused an efficient infection in Nicotiana benthamiana plants, its viral progeny had very reduced infectivity. Making use of different approaches, here, we provide direct evidence of a previously unknown function of HCPro in which the viral factor enhances the stability of its cognate capsid protein (CP), positively affecting the yield of virions and consequently improving the infectivity of the viral progeny. Site-directed mutagenesis revealed that the ability of HCPro to stabilize CP and enhance the yield of infectious viral particles is not linked to any of its previously known activities and helped us to delimit the region of HCPro involved in this function in the central region of the protein. Moreover, the function is highly specific and cannot be fulfilled by the HCPro of a heterologous potyvirus. The importance of this novel requirement in regulating the sorting of the viral genome to be subjected to replication, translation, and encapsidation, thus contributing to the synchronization of these viral processes, is discussed. IMPORTANCEPotyviruses form one of the most numerous groups of plant viruses and are a major cause of crop loss worldwide. It is well known that these pathogens make use of virus-derived multitasking proteins, as well as dedicated host factors, to successfully infect their hosts. Here, we describe a novel requirement for the proper yield and infectivity of potyviral progeny. In this case, such a function is performed by the extensively studied viral factor HCPro, which seems to use an unknown mechanism that is not linked to its previously described activities. To our knowledge, this is the first time that a factor different from capsid protein (CP) has been shown to be directly involved in the yield of potyviral particles. Based on the data presented here, we hypothesize that this capacity of HCPro might be involved in the coordination of mutually exclusive activities of the viral genome by controlling correct assembly of CP in stable virions.

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“…It has also been implicated in resistance gene evasion and symptomatic development (Decroocq et al ., ; Ullah and Grumet, ), as well as functioning as a determinant of systemic infectivity for a number of potyviruses (Andersen and Johansen, ; Desbiez et al ., ; Tatineni et al ., ). Interestingly, potyviral pathogenicity determinants mapping to this region may also display host specificity in their functioning (Pérez et al ., ), and play a key role in host adaptation (Carbonell et al ., ; Salvador et al ., ).…”

Section: Primers and Annealing Conditions Used In This Investigationmentioning

confidence: 98%

A pathogenicity determinant maps to the N‐terminal coat protein region of the Pepino mosaic virus genome

Duff‐Farrier

Bailey

Boonham

et al. 2014

Molecular Plant Pathology

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O-GlcNAc modification of the coat protein of the potyvirus Plum pox virus enhances viral infection

Cited by 34 publications

References 36 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

A Novel Role of the Potyviral Helper Component Proteinase Contributes To Enhance the Yield of Viral Particles

A pathogenicity determinant maps to the N‐terminal coat protein region of the Pepino mosaic virus genome

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