Cell Wall Carbohydrate Dynamics during the Differentiation of Infection Structures by the Apple Scab Fungus, Venturia inaequalis

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dc.citation.issue3
dc.citation.volume11
dc.contributor.authorRocafort M
dc.contributor.authorSrivastava V
dc.contributor.authorBowen J
dc.contributor.authorDíaz-Moreno SM
dc.contributor.authorGuo Y
dc.contributor.authorBulone V
dc.contributor.authorPlummer KM
dc.contributor.authorSutherland PW
dc.contributor.authorAnderson MA
dc.contributor.authorBradshaw RE
dc.contributor.authorMesarich CH
dc.contributor.editorWang Y
dc.date.accessioned2023-12-15T01:34:21Z
dc.date.accessioned2024-07-25T06:43:54Z
dc.date.available2022-09-21
dc.date.available2023-12-15T01:34:21Z
dc.date.available2024-07-25T06:43:54Z
dc.date.issued2023-06-15
dc.description.abstractScab, caused by the biotrophic fungal pathogen Venturia inaequalis, is the most economically important disease of apples. During infection, V. inaequalis colonizes the subcuticular host environment, where it develops specialized infection structures called runner hyphae and stromata. These structures are thought to be involved in nutrient acquisition and effector (virulence factor) delivery, but also give rise to conidia that further the infection cycle. Despite their importance, very little is known about how these structures are differentiated. Likewise, nothing is known about how these structures are protected from host defenses or recognition by the host immune system. To better understand these processes, we first performed a glycosidic linkage analysis of sporulating tubular hyphae from V. inaequalis developed in culture. This analysis revealed that the V. inaequalis cell wall is mostly composed of glucans (44%) and mannans (37%), whereas chitin represents a much smaller proportion (4%). Next, we used transcriptomics and confocal laser scanning microscopy to provide insights into the cell wall carbohydrate composition of runner hyphae and stromata. These analyses revealed that, during subcuticular host colonization, genes of V. inaequalis putatively associated with the biosynthesis of immunogenic carbohydrates, such as chitin and b-1,6-glucan, are downregulated relative to growth in culture, while on the surface of runner hyphae and stromata, chitin is deacetylated to the less-immunogenic carbohydrate chitosan. These changes are anticipated to enable the subcuticular differentiation of runner hyphae and stromata by V. inaequalis, as well as to protect these structures from host defenses and recognition by the host immune system. IMPORTANCE Plant-pathogenic fungi are a major threat to food security. Among these are subcuticular pathogens, which often cause latent asymptomatic infections, making them difficult to control. A key feature of these pathogens is their ability to differentiate specialized subcuticular infection structures that, to date, remain largely understudied. This is typified by Venturia inaequalis, which causes scab, the most economically important disease of apples. In this study, we show that, during subcuticular host colonization, V. inaequalis downregulates genes associated with the biosynthesis of two immunogenic cell wall carbohydrates, chitin and b-1,6-glucan, and coats its subcuticular infection structures with a less-immunogenic carbohydrate, chitosan. These changes are anticipated to enable host colonization by V. inaequalis and provide a foundation for understanding subcuticular host colonization by other plant-pathogenic fungi. Such an understanding is important, as it may inform the development of novel control strategies against subcuticular plant-pathogenic fungi.
dc.description.confidentialfalse
dc.edition.editionJune 2023
dc.identifier.citationRocafort M, Srivastava V, Bowen J, Díaz-Moreno S, Bulone V, Plummer K, Sutherland P, Anderson M, Bradshaw R, Mesarich C. (2022). Cell wall carbohydrate dynamics during the differentiation of infection structures by the apple scab fungus, <i>Venturia inaequalis</i>. Microbiology Spectrum. 11. 3.
dc.identifier.doi10.1101/2022.09.21.508768
dc.identifier.eissn2165-0497
dc.identifier.elements-typejournal-article
dc.identifier.numbere04219-22
dc.identifier.urihttps://mro.massey.ac.nz/handle/10179/70762
dc.languageEnglish
dc.publisherAmerican Society for Microbiology
dc.publisher.urihttps://journals.asm.org/doi/10.1128/spectrum.04219-22
dc.relation.isPartOfMicrobiology Spectrum
dc.rights(c) 2023 The Author/s
dc.rightsCC BY 4.0
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.subjectapple scab
dc.subjectcell wall
dc.subjectmorphological differentiation
dc.subjectsubcuticular infection structures
dc.subjectVenturia inaequalis
dc.titleCell Wall Carbohydrate Dynamics during the Differentiation of Infection Structures by the Apple Scab Fungus, Venturia inaequalis
dc.typeJournal article
pubs.elements-id456961
pubs.organisational-groupOther
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