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      Different pathogenicities of Rice stripe virus from the insect vector and from viruliferous plants

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          Summary

          • Persistent plant viruses usually depend on insects for their transmission; they cannot be transmitted between plants or through mechanical inoculation. However, the mechanism by which persistent viruses become pathogenic in insect vectors remains unknown. In this study, we used Rice stripe virus ( RSV), its insect vector Laodelphax striatellus and host plant ( Oryza sativa) to explore how persistent viruses acquire pathogenicity from insect vectors.

          • RSV acquired phytopathogenicity in both the alimentary tract and the salivary gland of L. striatellus.

          • We mechanically inoculated RSV into rice O. sativa leaves through midrib microinjection. Insect‐derived RSV induced a typical stripe symptom, whereas plant‐derived RSV only produced chlorosis in rice leaves. Insect‐derived RSV had higher expression of genes rdrp, ns2, nsvc2, sp and nsvc4 than plant‐derived RSV, and the latter had higher expression of genes cp and ns3 than the former in rice leaves. Different from plant‐derived RSV, insect‐derived RSV damaged grana stacks within the chloroplast and inhibited photosynthesis by suppressing the photosystem II subunit psbp.

          • This study not only presented a convenient method to mechanically inoculate RSV into plants, but also provided insights into the different pathogenic mechanisms of RSV from the insect vector and from viruliferous plants.

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          Mechanisms of plant resistance to viruses.

          Plants have evolved in an environment rich with microorganisms that are eager to capitalize on the plants' biosynthetic and energy-producing capabilities. There are approximately 450 species of plant-pathogenic viruses, which cause a range of diseases. However, plants have not been passive in the face of these assaults, but have developed elaborate and effective defence mechanisms to prevent, or limit, damage owing to viral infection. Plant resistance genes confer resistance to various pathogens, including viruses. The defence response that is initiated after detection of a specific virus is stereotypical, and the cellular and physiological features associated with it have been well characterized. Recently, RNA silencing has gained prominence as an important cellular pathway for defence against foreign nucleic acids, including viruses. These pathways function in concert to result in effective protection against virus infection in plants.
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            Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms.

            Rice stripe virus (RSV) causes severe diseases in Oryza sativa (rice) in many Eastern Asian countries. Disease-specific protein (SP) of RSV is a non-structural protein and its accumulation level in rice plant was shown to determine the severity of RSV symptoms. Here, we present evidence that expression of RSV SP alone in rice or Nicotiana benthamiana did not produce visible symptoms. Expression of SP in these two plants, however, enhanced RSV- or Potato virus X (PVX)-induced symptoms. Through yeast two-hybrid screening, GST pull-down, and bimolecular fluorescence complementation assays, we demonstrated that RSV SP interacted with PsbP, a 23-kDa oxygen-evolving complex protein, in both rice and N. benthamiana. Furthermore, our investigation showed that silencing of PsbP expression in both plants increased disease symptom severity and virus accumulation. Confocal microscopy using N. benthamiana protoplast showed that PsbP accumulated predominantly in chloroplast in wild-type N. benthamiana cells. In the presence of RSV SP, most PsbP was recruited into cytoplasm of the assayed cells. In addition, accumulation of SP during RSV infection resulted in alterations of chloroplast structure and function. Our findings shed light on the molecular mechanism underlying RSV disease symptom development.
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              Massively parallel pyrosequencing-based transcriptome analyses of small brown planthopper (Laodelphax striatellus), a vector insect transmitting rice stripe virus (RSV)

              Background The small brown planthopper (Laodelphax striatellus) is an important agricultural pest that not only damages rice plants by sap-sucking, but also acts as a vector that transmits rice stripe virus (RSV), which can cause even more serious yield loss. Despite being a model organism for studying entomology, population biology, plant protection, molecular interactions among plants, viruses and insects, only a few genomic sequences are available for this species. To investigate its transcriptome and determine the differences between viruliferous and naïve L. striatellus, we employed 454-FLX high-throughput pyrosequencing to generate EST databases of this insect. Results We obtained 201,281 and 218,681 high-quality reads from viruliferous and naïve L. striatellus, respectively, with an average read length as 230 bp. These reads were assembled into contigs and two EST databases were generated. When all reads were combined, 16,885 contigs and 24,607 singletons (a total of 41,492 unigenes) were obtained, which represents a transcriptome of the insect. BlastX search against the NCBI-NR database revealed that only 6,873 (16.6%) of these unigenes have significant matches. Comparison of the distribution of GO classification among viruliferous, naïve, and combined EST databases indicated that these libraries are broadly representative of the L. striatellus transcriptomes. Functionally diverse transcripts from RSV, endosymbiotic bacteria Wolbachia and yeast-like symbiotes were identified, which reflects the possible lifestyles of these microbial symbionts that live in the cells of the host insect. Comparative genomic analysis revealed that L. striatellus encodes similar innate immunity regulatory systems as other insects, such as RNA interference, JAK/STAT and partial Imd cascades, which might be involved in defense against viral infection. In addition, we determined the differences in gene expression between vector and naïve samples, which generated a list of candidate genes that are potentially involved in the symbiosis of L. striatellus and RSV. Conclusions To our knowledge, the present study is the first description of a genomic project for L. striatellus. The identification of transcripts from RSV, Wolbachia, yeast-like symbiotes and genes abundantly expressed in viruliferous insect, provided a starting-point for investigating the molecular basis of symbiosis among these organisms.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                20 November 2015
                April 2016
                : 210
                : 1 ( doiID: 10.1111/nph.2016.210.issue-1 )
                : 196-207
                Affiliations
                [ 1 ] State Key Laboratory of Integrated Management of Pest Insects and Rodents Institute of ZoologyChinese Academy of Sciences BeijingChina
                [ 2 ] Beijing Institutes of Life ScienceChinese Academy of Sciences BeijingChina
                Author notes
                [*] [* ] Authors for correspondence:

                Le Kang

                Tel: +86 10 64807219

                Email: lkang@ 123456ioz.ac.cn

                Feng Cui

                Tel: +86 10 64807218

                Email: cuif@ 123456ioz.ac.cn

                [†]

                These authors contributed equally to this work.

                Article
                NPH13747 2015-19477
                10.1111/nph.13747
                5063192
                26585422
                98ae5a90-4195-480c-8124-b391a4ddf2ab
                © 2015 The Authors. New Phytologist © 2015 New Phytologist Trust

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 26 March 2015
                : 06 October 2015
                Page count
                Pages: 12
                Funding
                Funded by: Strategic Priority Research Program of the Chinese Academy of Sciences
                Award ID: XDB11040200
                Funded by: Major State Basic Research Development Program of China
                Award ID: 2014CB13840402
                Categories
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                Research
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                Custom metadata
                2.0
                nph13747
                April 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:13.10.2016

                Plant science & Botany
                alimentary canal,chloroplast,mechanical inoculation,rice stripe disease,salivary gland,small brown planthopper (laodelphax striatellus)

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