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Nicotiana benthamiana phosphatidylinositol 4-kinase type II regulates chilli leaf curl virus pathogenesis.

ABSTRACT: Geminiviruses are single-stranded DNA viruses that can cause significant losses in economically important crops. In recent years, the role of different kinases in geminivirus pathogenesis has been emphasized. Although geminiviruses use several host kinases, the role of phosphatidylinositol 4-kinase (PI4K) remains obscure. We isolated and characterized phosphatidylinositol 4-kinase type II from Nicotiana benthamiana (NbPI4KII) which interacts with the replication initiator protein (Rep) of a geminivirus, chilli leaf curl virus (ChiLCV). NbPI4KII-mGFP was localized into cytoplasm, nucleus or both. NbPI4KII-mGFP was also found to be associated with the cytoplasmic endomembrane systems in the presence of ChiLCV. Furthermore, we demonstrated that Rep protein directly interacts with NbPI4KII protein and influenced nuclear occurrence of NbPI4KII. The results obtained in the present study revealed that NbPI4KII is a functional protein kinase lacking lipid kinase activity. Downregulation of NbPI4KII expression negatively affects ChiLCV pathogenesis in N. benthamiana. In summary, NbPI4KII is a susceptible factor, which is required by ChiLCV for pathogenesis.

SUBMITTER: Mansi

PROVIDER: S-EPMC6792133 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Nicotiana benthamiana phosphatidylinositol 4-kinase type II regulates chilli leaf curl virus pathogenesis.

Mansi Kushwaha Nirbhay Kumar NK Singh Ashish Kumar AK Karim Mir Jishan MJ Chakraborty Supriya S

Molecular plant pathology 20190902 10

Geminiviruses are single-stranded DNA viruses that can cause significant losses in economically important crops. In recent years, the role of different kinases in geminivirus pathogenesis has been emphasized. Although geminiviruses use several host kinases, the role of phosphatidylinositol 4-kinase (PI4K) remains obscure. We isolated and characterized phosphatidylinositol 4-kinase type II from Nicotiana benthamiana (NbPI4KII) which interacts with the replication initiator protein (Rep) of a gemi ...[more]

PMID: 31475785

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Project description:BACKGROUND:In Oman tobacco (Nicotiana tabacum; family Solanaceae) is a minor crop, which is produced only for local consumption. In 2015, tobacco plants exhibiting severe downward leaf curling, leaf thickening, vein swelling, yellowing and stunting were identified in fields of tobacco in Suhar Al-Batina region, Oman. These symptoms are suggestive of begomovirus (genus Begomovirus, family Geminiviridae) infection. METHODS:Circular DNA molecules were amplified from total DNA extracted from tobacco plants by rolling circle amplification (RCA). Viral genomes were cloned from RCA products by restriction digestion and betasatellites were cloned by PCR amplification from RCA product, using universal primers. The sequences of full-length clones were obtained by Sanger sequencing and primer walking. Constructs for the infectivity of virus and betasatellite were produced and introduced into plants by Agrobacterium-mediated inoculation. RESULTS:The full-length sequences of 3 begomovirus and 3 betasatellite clones, isolated from 3 plants, were obtained. Analysis of the full-length sequences determined showed the virus to be a variant of Chilli leaf curl virus (ChiLCV) and the betasatellite to be a variant of Tomato leaf curl betasatellite (ToLCB). Both the virus and the betasatellite isolated from tobacco show the greatest levels of sequence identity to isolates of ChiLCV and ToLCB identified in other hosts in Oman. Additionally clones of ChiLCV and ToLCB were shown, by Agrobacterium-mediated inoculation, to be infectious to 3 Nicotiana species, including N. tabacum. In N. benthamiana the betasatellite was shown to change the upward leaf rolling symptoms to a severe downward leaf curl, as is typical for many monopartite begomoviruses with betasatellites. CONCLUSIONS:The leaf curl disease of tobacco in Oman was shown to be caused by ChiLCV and ToLCB. This is the first identification of ChiLCV with ToLCB infecting tobacco. The study shows that, despite the low diversity of begomoviruses and betasatellites in Oman, the extant viruses/betasatellites are able to fill the niches that present themselves.

Project description:BackgroundViruses have evolved to create a cellular environment permissive for viral replication in susceptible hosts. Possibly both enabling and resulting from these virus-triggered changes, infected hosts undergo a dramatic transcriptional reprogramming, the analysis of which can shed light on the molecular processes underlying the outcome of virus-host interactions. The study of the transcriptional changes triggered by the plant DNA viruses geminiviruses is potentially hampered by the low representation of infected cells in the total population, a situation that becomes extreme in those cases, like that of Tomato yellow leaf curl virus (TYLCV), in which the virus is restricted to phloem companion cells.ResultsIn order to gain insight into how different the transcriptional landscapes of TYLCV-infected cells or whole tissues of TYLCV-infected plants might be, here we compare the transcriptional changes in leaf patches infected with TYLCV by agroinfiltration or in systemic leaves of TYLCV-infected plants in Nicotiana benthamiana. Our results show that, in agreement with previous works, infection by TYLCV induces a dramatic transcriptional reprogramming; the detected changes, however, are not equivalent in local and systemic infections, with a much larger number of genes differentially expressed locally, and some genes responding in an opposite manner. Interestingly, a transcriptional repression of the auxin signalling pathway and a transcriptional activation of the ethylene signalling pathway were detected in both local and systemically infected samples. A transcriptional activation of defence was also detectable in both cases. Comparison with the transcriptional changes induced by systemic infection by the geminivirus Tobacco curly shoot virus (TbSV) shows common subsets of up- and down-regulated genes similarly affected by both viral species, unveiling a common transcriptional repression of terpenoid biosynthesis, a process also suppressed by the geminivirus Tomato yellow leaf curl China virus.ConclusionsTaken together, the results presented here not only offer insight into the transcriptional changes derived from the infection by TYLCV in N. benthamiana, but also demonstrate that the resolution provided by local and systemic infection approaches largely differs, highlighting the urge to come up with a better system to gain an accurate view of the molecular and physiological changes caused by the viral invasion.

Project description:BackgroundTomato yellow leaf curl virus (TYLCV) is a major monopartite virus in the family Geminiviridae and has caused severe yield losses in tomato and tobacco planting areas worldwide. Wall-associated kinases (WAKs) and WAK-like kinases (WAKLs) are a subfamily of the receptor-like kinase family implicated in cell wall signaling and transmitting extracellular signals to the cytoplasm, thereby regulating plant growth and development and resistance to abiotic and biotic stresses. Recently, many studies on WAK/WAKL family genes have been performed in various plants under different stresses; however, identification and functional survey of the WAK/WAKL gene family of Nicotiana benthamiana have not yet been performed, even though its genome has been sequenced for several years. Therefore, in this study, we aimed to identify the WAK/WAKL gene family in N. benthamiana and explore their possible functions in response to TYLCV infection.ResultsThirty-eight putative WAK/WAKL genes were identified and named according to their locations in N. benthamiana. Phylogenetic analysis showed that NbWAK/WAKLs are clustered into five groups. The protein motifs and gene structure compositions of NbWAK/WAKLs appear to be highly conserved among the phylogenetic groups. Numerous cis-acting elements involved in phytohormone and/or stress responses were detected in the promoter regions of NbWAK/WAKLs. Moreover, gene expression analysis revealed that most of the NbWAK/WAKLs are expressed in at least one of the examined tissues, suggesting their possible roles in regulating the growth and development of plants. Virus-induced gene silencing and quantitative PCR analyses demonstrated that NbWAK/WAKLs are implicated in regulating the response of N. benthamiana to TYLCV, ten of which were dramatically upregulated in locally or systemically infected leaves of N. benthamiana following TYLCV infection.ConclusionsOur study lays an essential base for the further exploration of the potential functions of NbWAK/WAKLs in plant growth and development and response to viral infections in N. benthamiana.

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Nicotiana benthamiana phosphatidylinositol 4-kinase type II regulates chilli leaf curl virus pathogenesis.

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Nicotiana benthamiana phosphatidylinositol 4-kinase type II regulates chilli leaf curl virus pathogenesis.

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