Transcription factor control of virulence in phytopathogenic fungi

John, Evan; Singh, Karam B.; Oliver, Richard P.; Tan, Kar‐Chun

doi:10.1111/mpp.13056

Cited by 54 publications

(20 citation statements)

References 360 publications

(661 reference statements)

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“…TFs are often the downstream effectors of signalling cascades and initiate the transcription and expression of specific genes, finally regulating responses to internal and external signals through the effect of gene products and playing an important regulatory role in environmental responses such as growth and development, morphogenesis, and biological and abiotic stress (Cho et al, 2012 ; van der Does et al, 2016 ; John et al, 2021 ). TFs have been widely used as novel antifungal drug targets (Bahn, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Transcription factor SsFoxE3 activating SsAtg8 is critical for sclerotia, compound appressoria formation, and pathogenicity in Sclerotinia sclerotiorum

Jiao

Cong

et al. 2021

Molecular Plant Pathology

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Sclerotinia sclerotiorum, the notorious necrotrophic phytopathogenic fungus with wide distribution, is responsible for sclerotium disease in more than 600 plant species, including many economic crops such as soybean, oilseed rape, and sunflower. The compound appressorium is a crucial multicellular infection structure that is a prerequisite for infecting healthy tissues. Previously, the Forkhead‐box family transcription factors (FOX TFs) SsFoxE2 and SsFKH1 were shown to play a key regulatory role in the hyphae growth, sexual reproduction, and pathogenicity of S. sclerotiorum. However, little is known about the roles of SsFoxE3 regulating growth and development and pathogenicity. Here, we report SsFoxE3 contributes to sclerotium formation and deletion of SsFoxE3 leads to reduced formation of compound appressoria and developmental delays. Transcripts of SsFoxE3 were greatly increased during the initial stage of infection and SsFoxE3 deficiency reduced virulence on the host, while stabbing inoculation could partially restore pathogenicity. The SsFoxE3 mutant showed sensitivity to H2O2, and the expression of reactive oxygen species detoxification and autophagy‐related genes were reduced. Moreover, expression of SsAtg8 was also decreased during the infection process of the SsFoxE3 mutant. Yeast 1‐hybrid tests suggested that SsFoxE3 interacted with the promoter of SsAtg8. Disruption of SsAtg8 resulted in a phenotype similar to that of the SsFoxE3 mutant. Comparative analysis of the level of autophagy in the wild type and SsFoxE3 mutant showed that N starvation‐induced autophagy was reduced in the SsFoxE3 mutant. Taken together, our findings indicate that SsFoxE3 plays an important role in compound appressorium formation and is involved in transcriptional activation of SsAtg8 during infection by S. sclerotiorum.

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Section: Discussionmentioning

confidence: 99%

Transcription factor SsFoxE3 activating SsAtg8 is critical for sclerotia, compound appressoria formation, and pathogenicity in Sclerotinia sclerotiorum

Jiao

Cong

et al. 2021

Molecular Plant Pathology

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“…Specific TFs associated with a given stage or with a given host plant can be identified. Interestingly, nearly 80% of the TFs with the highest expression levels were previously reported as regulators of key virulence pathways in phytopathogenic fungi (John et al, 2021). During time course infection of the poplar host, preferential expression of TF genes can also be associated with early colonization, biotrophic growth or sporulation.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the comparison across more than 200 fungal genomes determined the presence of approximatively 80 DBD families in fungi, including four fungal-specific families (Shelest, 2017). Several DBD families were associated to regulatory functions of fungal pathogenesis in plant-pathogen interactions, such as sporulation or virulence effector expression (John et al, 2021). Other TFs can be associated to abiotic stress responses; those responsible for temperature stresses are characterized by heat shock (HSDs) or cold shock domains (CSDs).…”

Section: Introductionmentioning

confidence: 99%

Expert annotation and life-cycle transcriptomics of transcription factors in rust fungi (Pucciniales) highlight the role of cold shock proteins in dormancy exit

Louet

Blot

Shelest

et al. 2021

Preprint

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Fungi of the order Pucciniales are obligate plant biotrophs causing rust diseases. They exhibit a complex life cycle with the production of up to five spore types, infection of two unrelated hosts and an overwintering stage. Transcription factors (TFs) are key regulators of gene expression in eukaryote cells. In order to better understand genetic programs expressed during major transitions of the rust life cycle, we surveyed the complement of TFs in fungal genomes with an emphasis on Pucciniales. We found that despite their large gene numbers, rust genomes have a reduced repertoire of TFs compared to other fungi. The proportions of C2H2 and Zinc cluster - two of the most represented TF families in fungi-indicate differences in their evolutionary relationships in Pucciniales and other fungal taxa. The cold shock protein (CSP) family showed a striking expansion in Pucciniomycotina with specific duplications in the order Pucciniales. The survey of expression profiles collected by transcriptomics along the life cycle of the poplar rust fungus revealed TF genes related to major biological transitions, e.g. response to environmental cues and host infection. Particularly, poplar rust CSPs were strongly expressed in basidia produced after the overwintering stage suggesting a possible role in dormancy exit. Expression during transition from dormant telia to basidia confirmed the specific expression of the three poplar rust CSP genes. Their heterologous expression in yeast improved cell growth after cold stress exposure, strengthening their implication in dormancy exit. This study addresses for the first time TF involved in developmental transition in the rust life cycle opening perspectives to further explore molecular regulation in the biology of the Pucciniales.

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“…In Zymoseptoria tritici, a Pf2 orthologue was essential for virulence, but also regulates dimorphic switch, axenic growth and fungal cell wall composition (Habig et al, 2020). So, while the involvement of Pf2 in pathogenicity is a common feature, its involvement in developmental processes or morphological switches is speciesdependent (John et al, 2021).…”

Section: Lmpf2 Is Involved In the Establishment Of Infection By L Maculansmentioning

confidence: 99%

Regulation of effector gene expression as concerted waves inLeptosphaeria maculans: a two-players game

Clairet

Gay

Porquier

et al. 2021

Preprint

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During infection, plant pathogenic fungi secrete a set of molecules collectively known as effectors, involved in overcoming the host immune system and in disease establishment. Effector genes are concertedly expressed as waves all along plant pathogenic fungi lifecycle. However, little is known about how coordinated expression of effector genes is regulated. Since many effector genes are located in repeat-rich regions, the role of chromatin remodeling in the regulation of effector expression was recently investigated. In Leptosphaeria maculans, causing stem canker of oilseed rape, we established that the repressive histone modification H3K9me3 (trimethylation of Lysine 9 of Histone H3), deposited by the histone methyltransferase KMT1, was involved in the regulation of expression of genes highly expressed during infection, including effectors. Nevertheless, inactivation of KMT1 did not induce expression of these genes at the same level as observed during infection of oilseed rape, suggesting that a second regulator, such as a transcription factor (TF), might be involved. Pf2, a TF belonging to the Zn2Cys6 fungal specific TF family, was described in several Dothideomycete species as essential for pathogenicity and effector gene expression. We identified the orthologue of Pf2 in L. maculans, LmPf2, and investigated the role of LmPf2 together with KMT1, by inactivating and over-expressing LmPf2 in a wild type (WT) strain and a Δkmt1 mutant. Functional analyses of the corresponding transformants highlighted an essential role of LmPf2 in the establishment of pathogenesis. Transcriptomic analyses during axenic growth showed that LmPf2 is involved in the control of effector gene expression. We observed an enhanced effect of the over-expression of LmPf2 on effector gene expression in a Δkmt1 background, suggesting an antagonist role between KMT1 and LmPf2.

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Transcription factor control of virulence in phytopathogenic fungi

Cited by 54 publications

References 360 publications

Transcription factor SsFoxE3 activating SsAtg8 is critical for sclerotia, compound appressoria formation, and pathogenicity in Sclerotinia sclerotiorum

Transcription factor SsFoxE3 activating SsAtg8 is critical for sclerotia, compound appressoria formation, and pathogenicity in Sclerotinia sclerotiorum

Expert annotation and life-cycle transcriptomics of transcription factors in rust fungi (Pucciniales) highlight the role of cold shock proteins in dormancy exit

Regulation of effector gene expression as concerted waves inLeptosphaeria maculans: a two-players game

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