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Survival factor 1 contributes to the oxidative stress response and is required for full virulence of Sclerotinia sclerotiorum.

ABSTRACT: Sclerotinia sclerotiorum is a devastating necrotrophic fungal pathogen that infects over 400 species of plants worldwide. Reactive oxygen species (ROS) modulations are critical for the pathogenic development of S. sclerotiorum. The fungus applies enzymatic and non-enzymatic antioxidants to cope with the oxidative stress during the infection processes. Survival factor 1 was identified and characterized to promote survival under conditions of oxidative stress in Saccharomyes cerevisiae. In this research, a gene named SsSvf1 was predicted to encode a survival factor 1 homologue in S. sclerotiorum. SsSvf1 transcripts showed high expression levels in hyphae under oxidative stress. Silencing of SsSvf1 resulted in increased sensitivity to oxidative stress in culture and increased levels of intracellular ROS. Transcripts of SsSvf1 showed a dramatic increase during the initial stage of infection and the gene-silenced strains displayed reduced virulence on oilseed rape and Arabidopsis thaliana. Inhibition of plant ROS production partially restores virulence of SsSvf1 gene-silenced strains. SsSvf1 gene-silenced strains exhibited normal oxalate production, but were impaired in compound appressorium formation and cell wall integrity. The results suggest that SsSvf1 is involved in coping with ROS during fungal-host interactions and plays a crucial role in the pathogenicity of S. sclerotiorum.

SUBMITTER: Yu Y

PROVIDER: S-EPMC6589728 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Survival factor 1 contributes to the oxidative stress response and is required for full virulence of Sclerotinia sclerotiorum.

Yu Yang Y Du Jiao J Wang Yabo Y Zhang Mengyao M Huang Zhiqiang Z Cai Junsong J Fang Anfei A Yang Yuheng Y Qing Ling L Bi Chaowei C Cheng Jiasen J

Molecular plant pathology 20190509 7

Sclerotinia sclerotiorum is a devastating necrotrophic fungal pathogen that infects over 400 species of plants worldwide. Reactive oxygen species (ROS) modulations are critical for the pathogenic development of S. sclerotiorum. The fungus applies enzymatic and non-enzymatic antioxidants to cope with the oxidative stress during the infection processes. Survival factor 1 was identified and characterized to promote survival under conditions of oxidative stress in Saccharomyes cerevisiae. In this re ...[more]

PMID: 31074170

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Project description:Sclerotinia sclerotiorum is a plant-pathogenic ascomycete fungus and infects over 400 host plants, including pea (Pisum sativum L.). The fungus causes white mold on pea, and substantial yield loss is attributed to the disease. To improve white mold management, further understanding of S. sclerotiorum pathogenicity is crucial. In this study, 389 transcription factors (TFs) were mined from the complete genome sequence of S. sclerotiorum and their in planta expression patterns were determined in susceptible and partially resistant pea lines and compared to in vitro expression patterns on culture medium. One of the transcription factors was significantly induced in planta at 24 and 48 h postinfection compared to the expression in vitro This putative C6 transcription factor of S. sclerotiorum (SsC6TF1) was knocked down using a gene-silencing approach to investigate its functions in vegetative growth and sclerotial development as well as its virulence and pathogenicity in pea. While the SsC6TF1 knockdown mutants had hyphal growth rates identical to those of the wild-type strain and were capable of infection, the knockdown mutants produced no sclerotia or significantly fewer and smaller sclerotia on the culture medium and exhibited reduced virulence on both pea lines. This study profiled genome-wide expression for S. sclerotiorum transcription factors in planta and in vitro and functionally characterized a novel transcription factor, SsC6TF1, which positively regulates sclerotial development and virulence on pea. The finding provides molecular insights into S. sclerotiorum biology and interaction with pea and other economically important crops.IMPORTANCE White mold, caused by Sclerotinia sclerotiorum, is a destructive disease on important legume species such as soybean, dry bean, and pea. This study investigated expression levels of transcription factors in S. sclerotiorumin planta (pea lines) and in vitro (culture medium). One transcription factor displaying high expression in planta was found to be involved in sclerotial development and virulence on pea. This report provides a new understanding regarding transcription factors of S. sclerotiorum in development and virulence.

Project description:UnlabelledA recombinant strain of Sclerotinia sclerotiorum hypovirus 2 (SsHV2) was identified from a North American Sclerotinia sclerotiorum isolate (328) from lettuce (Lactuca sativa L.) by high-throughput sequencing of total RNA. The 5'- and 3'-terminal regions of the genome were determined by rapid amplification of cDNA ends. The assembled nucleotide sequence was up to 92% identical to two recently reported SsHV2 strains but contained a deletion near its 5' terminus of more than 1.2 kb relative to the other SsHV2 strains and an insertion of 524 nucleotides (nt) that was distantly related to Valsa ceratosperma hypovirus 1. This suggests that the new isolate is a heterologous recombinant of SsHV2 with a yet-uncharacterized hypovirus. We named the new strain Sclerotinia sclerotiorum hypovirus 2 Lactuca (SsHV2L) and deposited the sequence in GenBank with accession number KF898354. Sclerotinia sclerotiorum isolate 328 was coinfected with a strain of Sclerotinia sclerotiorum endornavirus 1 and was debilitated compared to cultures of the same isolate that had been cured of virus infection by cycloheximide treatment and hyphal tipping. To determine whether SsHV2L alone could induce hypovirulence in S. sclerotiorum, a full-length cDNA of the 14,538-nt viral genome was cloned. Transcripts corresponding to the viral RNA were synthesized in vitro and transfected into a virus-free isolate of S. sclerotiorum, DK3. Isolate DK3 transfected with SsHV2L was hypovirulent on soybean and lettuce and exhibited delayed maturation of sclerotia relative to virus-free DK3, completing Koch's postulates for the association of hypovirulence with SsHV2L.ImportanceA cosmopolitan fungus, Sclerotinia sclerotiorum infects more than 400 plant species and causes a plant disease known as white mold that produces significant yield losses in major crops annually. Mycoviruses have been used successfully to reduce losses caused by fungal plant pathogens, but definitive relationships between hypovirus infections and hypovirulence in S. sclerotiorum were lacking. By establishing a cause-and-effect relationship between Sclerotinia sclerotiorum hypovirus Lactuca (SsHV2L) infection and the reduction in host virulence, we showed direct evidence that hypoviruses have the potential to reduce the severity of white mold disease. In addition to intraspecific recombination, this study showed that recent interspecific recombination is an important factor shaping viral genomes. The construction of an infectious clone of SsHV2L allows future exploration of the interactions between SsHV2L and S. sclerotiorum, a widespread fungal pathogen of plants.

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Dataset Information

Survival factor 1 contributes to the oxidative stress response and is required for full virulence of Sclerotinia sclerotiorum.

Publications

Survival factor 1 contributes to the oxidative stress response and is required for full virulence of Sclerotinia sclerotiorum.

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