A PERK-Like Receptor Kinase Interacts with the Geminivirus Nuclear Shuttle Protein and Potentiates Viral Infection

Florentino, Lilian H.; Santos, Anésia A.; Fontenelle, M. R.; Pinheiro, Guilherme L.; Zerbini, F. Murilo; Baracat‐Pereira, Maria Cristina; Fontes, Elizabeth P. B.

doi:10.1128/jvi.00173-06

Cited by 86 publications

(83 citation statements)

References 56 publications

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“…Coat proteins (CPs) of the Cauliflower mosaic virus (Martinez-Izquierdo and Hohn, 1987) and potyviruses (Ivanov et al, 2001;Fernández-Fernández et al, 2002) as well as movement protein (MP) of Tobacco mosaic virus (Atkins et al, 1991;Watanabe et al, 1992;Citovsky et al, 1993;Waigmann et al, 2000) are phosphorylated, and several functions of these proteins are affected by phosphorylation (Karpova et al, 1999;Kawakami et al, 1999;Waigmann et al, 2000). Previous studies also identified a PERK-Like Receptor Kinase, NsAK, that may regulate nuclear shuttle protein function through phosphorylation (Florentino et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

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Tomato SlSnRK1 Protein Interacts with and Phosphorylates βC1, a Pathogenesis Protein Encoded by a Geminivirus β-Satellite

et al. 2011

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The bC1 protein of tomato yellow leaf curl China b-satellite functions as a pathogenicity determinant. To better understand the molecular basis of bC1 in pathogenicity, a yeast two-hybrid screen of a tomato (Solanum lycopersicum) cDNA library was carried out using bC1 as bait. bC1 interacted with a tomato SUCROSE-NONFERMENTING1-related kinase designated as SlSnRK1. Their interaction was confirmed using a bimolecular fluorescence complementation assay in Nicotiana benthamiana cells. Plants overexpressing SnRK1 were delayed for symptom appearance and contained lower levels of viral and satellite DNA, while plants silenced for SnRK1 expression developed symptoms earlier and accumulated higher levels of viral DNA. In vitro kinase assays showed that bC1 is phosphorylated by SlSnRK1 mainly on serine at position 33 and threonine at position 78. Plants infected with bC1 mutants containing phosphorylation-mimic aspartate residues in place of serine-33 and/or threonine-78 displayed delayed and attenuated symptoms and accumulated lower levels of viral DNA, while plants infected with phosphorylation-negative alanine mutants contained higher levels of viral DNA. These results suggested that the SlSnRK1 protein attenuates geminivirus infection by interacting with and phosphorylating the bC1 protein.

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Section: Discussionmentioning

confidence: 99%

“…Recent studies indicated that they can evade the plant immune system by interfering with host antiviral pathways Wang et al, 2003;Florentino et al, 2006;Piroux et al, 2007). In response, the plant hosts have evolved diverse innate defense mechanisms to counter these challenges (Voinnet, 2001;Xie and Guo, 2006).…”

Section: Discussionmentioning

confidence: 99%

Tomato SlSnRK1 Protein Interacts with and Phosphorylates βC1, a Pathogenesis Protein Encoded by a Geminivirus β-Satellite

et al. 2011

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“…In plants, they play critical roles in pathogen recognition and the defense response (for review, see Romeis, 2001;Xing et al, 2002;Martin, 2003, 2005). They can also act in concert with pathogen proteins to facilitate infection (Florentino et al, 2006). This partnership is particularly important for viruses that have limited coding capacities.…”

mentioning

confidence: 99%

“…The BR1 protein binds to three Leurich-repeat RLKs, NIK1, NIK2, and NIK2, to inhibit their kinase and antiviral activities (Fontes et al, 2004). In contrast, interaction and phosphorylation of BR1 by a PERK-like RLK, NsAK, is necessary for efficient infection and full symptom development (Florentino et al, 2006). The AL2 protein inhibits the activity of an SNF1-related kinase (SnRK) through protein interactions, resulting in an enhanced susceptibility phenotype (Hao et al, 2003).…”

mentioning

confidence: 99%

Geminivirus Infection Up-Regulates the Expression of Two Arabidopsis Protein Kinases Related to Yeast SNF1- and Mammalian AMPK-Activating Kinases

Shen¹,

Hanley‐Bowdoin²

2006

Plant Physiol.

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Geminivirus Rep-interacting kinase 1 (GRIK1) and GRIK2 constitute a small protein kinase family in Arabidopsis (Arabidopsis thaliana). An earlier study showed that a truncated version of GRIK1 binds to the geminivirus replication protein AL1. We show here both full-length GRIK1 and GRIK2 interact with AL1 in yeast two-hybrid studies. Using specific antibodies, we showed that both Arabidopsis kinases are elevated in infected leaves. Immunoblot analysis of healthy plants revealed that GRIK1 and GRIK2 are highest in young leaf and floral tissues and low or undetectable in mature tissues. Immunohistochemical staining showed that the kinases accumulate in the shoot apical meristem, leaf primordium, and emerging petiole. Unlike the protein patterns, GRIK1 and GRIK2 transcript levels only show a small increase during infection and do not change significantly during development. Treating healthy seedlings and infected leaves with the proteasome inhibitor MG132 resulted in higher GRIK1 and GRIK2 protein levels, whereas treatment with the translation inhibitor cycloheximide reduced both kinases, demonstrating that their accumulation is modulated by posttranscriptional processes. Phylogenetic comparisons indicated that GRIK1, GRIK2, and related kinases from Medicago truncatula and rice (Oryza sativa) are most similar to the yeast kinases PAK1, TOS3, and ELM1 and the mammalian kinase CaMKK, which activate the yeast kinase SNF1 and its mammalian homolog AMPK, respectively. Complementation studies using a PAK1/TOS3/ELM1 triple mutant showed that GRIK1 and GRIK2 can functionally replace the yeast kinases, suggesting that the Arabidopsis kinases mediate one or more processes during early plant development and geminivirus infection by activating SNF1-related kinases.

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“…It has been shown that they play role in the regulation of meristem proliferation (Clark et al 1997;DeYoung et al 2006), organ specification (Torii et al 1996;Muto et al 2004;Shpak et al 2004;Chevalier et al, 2005;Kwak et al 2005;Eyuboglu et al 2007), reproduction (Albrecht et al 2005;Colcombet et al 2005;Escobar-Restrepo et al 2007), and hormone signal transduction (Li and Chory 1997;Nam and Li 2002;Zhou et al 2004). Other RLK/Pelle members function in signaling networks involving environmental stimuli, both abiotic (Sivaguru et al 2003;Hou et al 2005) and biotic (Song et al 1995;GomezGomez and Boller 2000;Endre et al 2002;Stracke et al 2002;Fontes et al 2004;Sun et al 2004;Diener and Ausubel 2005;Florentino et al 2006;Acharya et al 2007;Miya et al 2007). In some cases, RLK/Pelle genes exhibit multifunctionality, playing roles in both development and defense (Bent and Mackey 2007).…”

Section: Functions Of Receptor-like Cytoplasmic Kinase (Rlck) Proteinsmentioning

confidence: 99%

Characterization of ROP GTPase-activated Arabidopsis receptor-like cytoplasmic kinases (RLCK class VI_A)

Manuela

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A PERK-Like Receptor Kinase Interacts with the Geminivirus Nuclear Shuttle Protein and Potentiates Viral Infection

Cited by 86 publications

References 56 publications

Tomato SlSnRK1 Protein Interacts with and Phosphorylates βC1, a Pathogenesis Protein Encoded by a Geminivirus β-Satellite

Tomato SlSnRK1 Protein Interacts with and Phosphorylates βC1, a Pathogenesis Protein Encoded by a Geminivirus β-Satellite

Geminivirus Infection Up-Regulates the Expression of Two Arabidopsis Protein Kinases Related to Yeast SNF1- and Mammalian AMPK-Activating Kinases

Characterization of ROP GTPase-activated Arabidopsis receptor-like cytoplasmic kinases (RLCK class VI_A)

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