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Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus.

ABSTRACT: Botryosphaeria dothidea is an important pathogenic fungus causing fruit rot, leaf and stem ring spots and dieback, stem canker, stem death or stool mortality, and decline of pear trees. Seven double-stranded RNAs (dsRNAs; dsRNAs 1 to 7 with sizes of 3,654, 2,773, 2,597, 2,574, 1,823, 1,623, and 511 bp, respectively) were identified in an isolate of B. dothidea exhibiting attenuated growth and virulence and a sectoring phenotype. Characterization of the dsRNAs revealed that they belong to two dsRNA mycoviruses. The four largest dsRNAs (dsRNAs 1 to 4) are the genomic components of a novel member of the family Chrysoviridae (tentatively designated Botryosphaeria dothidea chrysovirus 1 [BdCV1]), a view supported by the morphology of the virions and phylogenetic analysis of the putative RNA-dependent RNA polymerases (RdRps). Two other dsRNAs (dsRNAs 5 and 6) are the genomic components of a novel member of the family Partitiviridae (tentatively designated Botryosphaeria dothidea partitivirus 1 [BdPV1]), which is placed in a clade distinct from other established partitivirus genera on the basis of the phylogenetic analysis of its RdRp. The smallest dsRNA, dsRNA7, seems to be a noncoding satellite RNA of BdPV1 on the basis of the conservation of its terminal sequences in BdPV1 genomic segments and its cosegregation with BdPV1 after horizontal transmission. This is the first report of a chrysovirus and a partitivirus infecting B. dothidea and of a chrysovirus associated with the hypovirulence of a phytopathogenic fungus.Our studies identified and characterized two novel mycoviruses, Botryosphaeria dothidea chrysovirus 1 (BdCV1) and Botryosphaeria dothidea partitivirus 1 (BdPV1), associated with the hypovirulence of an important fungus pathogenic to fruit trees. This is the first report of a chrysovirus and a partitivirus infecting B. dothidea and of a chrysovirus associated with the hypovirulence of a phytopathogenic fungus. BdCV1 appears to be a good candidate for the biological control of the serious disease induced by B. dothidea. Additionally, BdPV1 is placed in a clade distinct from the established genera. The BdCV1 capsid has two major structural proteins, and the capsid is distinct from that made up by a single polypeptide of the typical chrysoviruses. BdPV1 is the second partitivirus in which the putative capsid protein shares no significant identity with any mycovirus protein. A small accompanying dsRNA that is presumed to be a noncoding satellite RNA of BdPV1 is the first of its kind reported for a partitivirus.

SUBMITTER: Wang L

PROVIDER: S-EPMC4054428 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus.

Wang LiPing L Jiang JingJing J Wang YanFen Y Hong Ni N Zhang Fangpeng F Xu WenXing W Wang GuoPing G

Journal of virology 20140423 13

<h4>Unlabelled</h4>Botryosphaeria dothidea is an important pathogenic fungus causing fruit rot, leaf and stem ring spots and dieback, stem canker, stem death or stool mortality, and decline of pear trees. Seven double-stranded RNAs (dsRNAs; dsRNAs 1 to 7 with sizes of 3,654, 2,773, 2,597, 2,574, 1,823, 1,623, and 511 bp, respectively) were identified in an isolate of B. dothidea exhibiting attenuated growth and virulence and a sectoring phenotype. Characterization of the dsRNAs revealed that the ...[more]

PMID: 24760881

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Project description:BACKGROUND:Pear ring rot, caused by Botryosphaeria species, is responsible for substantial economic losses by causing severe recession of pear tree growth in China. Mycovirus-mediated hypovirulence in plant pathogenic fungi is a crucial biological method to control fungal diseases. METHODS:We conducted a large-scale and comprehensive transcriptome analysis to identify mRNA in B. dothidea in response to mycovirus. De novo sequencing technology from four constructed libraries of LW-C (Botryosphaeria dothidea chrysovirus 1, BdCV1), LW-P (Botryosphaeria dothidea partitivirus 1, BdPV1), LW-CP (LW-1 strain infection with BdCV1 and BdPV1), and Mock (free virus) was used to investigate and compare gene expression changes in B.dothidea strains infected with mycovirus. RESULTS:In total, 30,058 Unigenes with an average length of 2128 bp were obtained from 4 libraries of B. dothidea strains. These were annotated to specify their classified function. We demonstrate that mRNAs of B. dothidea strains in response to mycovirus are differentially expressed. In total, 5598 genes were up-regulated and 3298 were down-regulated in the LW-CP group, 4468 were up-regulated and 4291 down-regulated in the LW-C group, and 2590 were up-regulated and 2325 down-regulated in the LW-P group. RT-qPCR was used to validate the expression of 9 selected genes. The B. dothidea transcriptome was more affected by BdCV1 infection than BdPV1. We conducted GO enrichment analysis to characterize gene functions regulated by B. dothidea with mycovirus infection. These involved metabolic process, cellular process, catalytic activity, transporter activity, signaling, and other biological pathways. KEGG function analysis demonstrated that the enriched differentially expressed genes are involved in metabolism, transcription, signal transduction, and ABC transport. mRNA is therefore involved in the interaction between fungi and mycovirus. In addition, changes in differential accumulation levels of cp and RdRp of BdCV1 and BdPV1 in B. dothidea strains were evaluated, revealing that the accumulation of BdCV1 and BdPV1 is related to the phenotype and virulence of B. dothidea strain LW-1. CONCLUSIONS:The identification and analysis of mRNAs from B. dothidea was first reported at the transcriptome level. Our analysis provides further insight into the interaction of B. dothidea strains infection with chrysovirus 1 (BdCV1) and partitivirus 1 (BdPV1) at the transcriptome level.

Project description:Colletotrichum spp. are economically important phytopathogenic fungi that cause anthracnose in a variety of plant species worldwide. Hypovirulence-associated mycoviruses provide new options for the biological control of plant fungal diseases. Here, we found a novel partitivirus from Colletotrichum alienum and named it Colletotrichum alienum partitivirus 1 (CaPV1). CaPV1 contained two dsRNA segments encoding an RNA-dependent RNA polymerase and a capsid protein and was classified under the genus Gammapartitivirus of the family Partitiviridae. CaPV1 significantly decreased host virulence, mycelial growth, appressorial development, and appressorium turgor but increased conidial production with abnormal morphology. In addition, CaPV1 could be successfully transfected into other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, and caused hypovirulence, indicating the broad application potential of this virus. CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum. Notably, some genes related to vesicle transport in the CaPV1-infected strain were downregulated, consistent with the impaired endocytosis pathway in this fungus. When the Rab gene CaRab7, which is associated with endocytosis in vesicle transport, was knocked out, the virulence of the mutants was reduced. Overall, our findings demonstrated that CaPV1 has the potential to control anthracnose caused by Colletotrichum, and the mechanism by which Colletotrichum induces hypovirulence is caused by affecting vesicle transport.IMPORTANCEColletotrichum is a kind of economically important phytopathogenic fungi that cause anthracnose disease in a variety of plant species worldwide. We found a novel mycovirus of the Gammapartitivirus genus and Partitiviridae family from the phytopathogenic fungus Colletotrichum alienum and named it CaPV1. This study revealed that CaPV1 infection significantly decreased host virulence and fitness by affecting mycelial growth, appressorial development, and appressorium turgor. In addition, CaPV1 could also infect other Colletotrichum species, including C. fructicola, C. spaethianum, and C. gloeosporioides, by viral particle transfection and resulting in hypovirulence of these Colletotrichum species. Transcriptomic analysis showed that CaPV1 caused significant transcriptional rewiring of the host fungus C. alienum, especially the genes involved in vesicle transport. Moreover, endocytosis and gene knockout assays demonstrated that the mechanism underlying CaPV1-induced hypovirulence is, at least in part, caused by affecting the vesicle transport of the host fungus. This study provided insights into the mechanisms underlying the pathogenesis of Colletotrichum species and mycovirus-fungus interactions, linking the role of mycovirus and fungus vesicle transport systems in shaping fungal pathogenicity.

Dataset Information

Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus.

Publications

Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus.

Similar Datasets

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