Carbon acquisition and metabolism changes during fungal biotrophic plant pathogenesis: insights from<i>Ustilago maydis</i>

Goulet, Kristi M.; Saville, Barry J.

doi:10.1080/07060661.2017.1354330

Cited by 20 publications

(13 citation statements)

References 122 publications

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“…Furthermore, recent studies in U. maydis suggested that intracellular changes of metabolism influence virulence, and therefore the underlying proteins could be targets of positive selection ( Kretschmer et al. 2012 ; Goulet and Saville 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Positively Selected Effector Genes and Their Contribution to Virulence in the Smut Fungus Sporisorium reilianum

Schweizer

Münch

Mannhaupt

et al. 2018

Genome Biology and Evolution

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Plants and fungi display a broad range of interactions in natural and agricultural ecosystems ranging from symbiosis to parasitism. These ecological interactions result in coevolution between genes belonging to different partners. A well-understood example is secreted fungal effector proteins and their host targets, which play an important role in pathogenic interactions. Biotrophic smut fungi (Basidiomycota) are well-suited to investigate the evolution of plant pathogens, because several reference genomes and genetic tools are available for these species. Here, we used the genomes of Sporisorium reilianum f. sp. zeae and S. reilianum f. sp. reilianum, two closely related formae speciales infecting maize and sorghum, respectively, together with the genomes of Ustilago hordei, Ustilago maydis, and Sporisorium scitamineum to identify and characterize genes displaying signatures of positive selection. We identified 154 gene families having undergone positive selection during species divergence in at least one lineage, among which 77% were identified in the two investigated formae speciales of S. reilianum. Remarkably, only 29% of positively selected genes encode predicted secreted proteins. We assessed the contribution to virulence of nine of these candidate effector genes in S. reilianum f. sp. zeae by deleting individual genes, including a homologue of the effector gene pit2 previously characterized in U. maydis. Only the pit2 deletion mutant was found to be strongly reduced in virulence. Additional experiments are required to understand the molecular mechanisms underlying the selection forces acting on the other candidate effector genes, as well as the large fraction of positively selected genes encoding predicted cytoplasmic proteins.

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Section: Discussionmentioning

confidence: 99%

Positively Selected Effector Genes and Their Contribution to Virulence in the Smut Fungus Sporisorium reilianum

Schweizer

Münch

Mannhaupt

et al. 2018

Genome Biology and Evolution

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“…In addition, homologues to CRE1 were found in 27 of the 31 basidiomycete genomes assessed [ 54 ]. Yet, no functional studies regarding the effect of CRE1 on the regulation of cell wall degrading enzyme was conducted in the basidiomycetes until now [ 55 ].…”

Section: Discussionmentioning

confidence: 99%

Effects of cre1 modification in the white-rot fungus Pleurotus ostreatus PC9: altering substrate preference during biological pretreatment

Yoav

Salame

Feldman

et al. 2018

Biotechnol Biofuels

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BackgroundDuring the process of bioethanol production, cellulose is hydrolyzed into its monomeric soluble units. For efficient hydrolysis, a chemical and/or mechanical pretreatment step is required. Such pretreatment is designed to increase enzymatic digestibility of the cellulose chains inter alia by de-crystallization of the cellulose chains and by removing barriers, such as lignin from the plant cell wall. Biological pretreatment, in which lignin is decomposed or modified by white-rot fungi, has also been considered. One disadvantage in biological pretreatment, however, is the consumption of the cellulose by the fungus. Thus, fungal species that attack lignin with only minimal cellulose loss are advantageous. The secretomes of white-rot fungi contain carbohydrate-active enzymes (CAZymes) including lignin-modifying enzymes. Thus, modification of secretome composition can alter the ratio of lignin/cellulose degradation.ResultsPleurotus ostreatus PC9 was genetically modified to either overexpress or eliminate (by gene replacement) the transcriptional regulator CRE1, known to act as a repressor in the process of carbon catabolite repression. The cre1-overexpressing transformant demonstrated lower secreted cellulolytic activity and slightly increased selectivity (based on the chemical composition of pretreated wheat straw), whereas the knockout transformant demonstrated increased cellulolytic activity and significantly reduced residual cellulose, thereby displaying lower selectivity. Pretreatment of wheat straw using the wild-type PC9 resulted in 2.8-fold higher yields of soluble sugar compared to untreated wheat straw. The overexpression transformant showed similar yields (2.6-fold), but the knockout transformant exhibited lower yields (1.2-fold) of soluble sugar. Based on proteomic secretome analysis, production of numerous CAZymes was affected by modification of the expression level of cre1.ConclusionsThe gene cre1 functions as a regulator for expression of fungal CAZymes active against plant cell wall lignocelluloses, hence altering the substrate preference of the fungi tested. While the cre1 knockout resulted in a less efficient biological pretreatment, i.e., less saccharification of the treated biomass, the converse manipulation of cre1 (overexpression) failed to improve efficiency. Despite the inverse nature of the two genetic alterations, the expected “mirror image” (i.e., opposite regulatory response) was not observed, indicating that the secretion level of CAZymes, was not exclusively dependent on CRE1 activity.Electronic supplementary materialThe online version of this article (10.1186/s13068-018-1209-6) contains supplementary material, which is available to authorized users.

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“…Many CAZymes play a role in plant cell-wall degradation and can be important virulence factors in necrotrophic fungi. Reductions in CAZymes genes have been observed in biotrophic pathogens and are thought to be an adaptation to reduce the exposure of molecular patterns, which can trigger host defenses (Duplessis et al, 2014;Goulet and Saville, 2017). Moreover, CAZyme loss can occur during host shifts, such as from plant to animal or insect hosts (Zhang et al, 2018).…”

Section: Distinct Cazyme Gene Loss In a Pathogenic Speciesmentioning

confidence: 99%

Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genusCryphonectria

Stauber

Prospero

Croll

2020

Preprint

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Emerging fungal pathogens are a threat to forest and agroecosystems, as well as animal and human health. How pathogens evolve from non-pathogenic ancestors is still poorly understood making the prediction of future outbreaks challenging. Most pathogens have evolved lifestyle adaptations, which were enabled by specific changes in the gene content of the species. Hence, understanding transitions in the functions encoded by genomes gives valuable insight into the evolution of pathogenicity. Here, we studied lifestyle evolution in the genus Cryphonectria, including the prominent invasive pathogen C. parasitica, the causal agent of chestnut blight on Castanea species. We assembled and compared the genomes of pathogenic and putatively non-pathogenic Cryphonectria species, as well as sister group pathogens in the family Cryphonectriaceae (Diaporthales, Ascomycetes) to investigate the evolution of genome size and gene content. We found a striking loss of genes associated with carbohydrate metabolism (CAZymes) in C. parasitica compared to other Cryphonectriaceae. Despite substantial CAZyme gene loss, experimental data suggests that C. parasitica has retained wood colonization abilities shared with other Cryphonectria species. Putative effectors substantially varied in number, cysteine content and protein length among species. In contrast, secondary metabolite gene clusters show a high degree of conservation within the genus. Overall, our results underpin the recent lifestyle transition of C. parasitica towards a more pathogenic lifestyle. Our findings suggest that a CAZyme loss may have promoted pathogenicity of C. parasitica on chestnuts. Analyzing gene complements underlying key nutrition modes can facilitate the detection of species with the potential to emerge as pathogens.

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Carbon acquisition and metabolism changes during fungal biotrophic plant pathogenesis: insights fromUstilago maydis

Cited by 20 publications

References 122 publications

Positively Selected Effector Genes and Their Contribution to Virulence in the Smut Fungus Sporisorium reilianum

Positively Selected Effector Genes and Their Contribution to Virulence in the Smut Fungus Sporisorium reilianum

Effects of cre1 modification in the white-rot fungus Pleurotus ostreatus PC9: altering substrate preference during biological pretreatment

Comparative genomics analyses of lifestyle transitions at the origin of an invasive fungal pathogen in the genusCryphonectria

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