The Maize Pathogen Ustilago maydis Secretes Glycoside Hydrolases and Carbohydrate Oxidases Directed toward Components of the Fungal Cell Wall

Reyre, Jean‐Lou; Grisel, Sacha; Haon, Mireille; Navarro, David; Ropartz, David; Gall, Sophie Le; Record, Éric; Sciara, Giuliano; Tranquet, Olivier; Berrin, Jean‐Guy; Bissaro, Bastien

doi:10.1128/aem.01581-22

Cited by 11 publications

(9 citation statements)

References 56 publications

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“…In our study, we predicted 495 CAZymes coding genes in the genome of F. zanthoxyli, a hemibiotrophic pathogen (Fig. 3A; Table S6), which was dramatically larger than those in biotrophic phytopathogenic fungi, such as Melampsora laricis-populina [46], Blumeria graminis [47] and Ustilago maydis [48], etc. This finding is consistent with the previous viewpoint that hemibiotrophic phytopathogenic fungi have more CAZymes than biotrophic pathogens [49].…”

Section: Discussionmentioning

confidence: 95%

Genome sequencing and comparative genomics reveal insights into pathogenicity and evolution of Fusarium zanthoxyli, the causal agent of stem canker in prickly ash

Ruan,

Jiao,

Zhao

et al. 2024

BMC Genomics

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Background Fusarium zanthoxyli is a destructive pathogen causing stem canker in prickly ash, an ecologically and economically important forest tree. However, the genome lack of F. zanthoxyli has hindered research on its interaction with prickly ash and the development of precise control strategies for stem canker. Results In this study, we sequenced and annotated a relatively high-quality genome of F. zanthoxyli with a size of 43.39 Mb, encoding 11,316 putative genes. Pathogenicity-related factors are predicted, comprising 495 CAZymes, 217 effectors, 156 CYP450s, and 202 enzymes associated with secondary metabolism. Besides, a comparative genomics analysis revealed Fusarium and Colletotrichum diverged from a shared ancestor approximately 141.1 ~ 88.4 million years ago (MYA). Additionally, a phylogenomic investigation of 12 different phytopathogens within Fusarium indicated that F. zanthoxyli originated approximately 34.6 ~ 26.9 MYA, and events of gene expansion and contraction within them were also unveiled. Finally, utilizing conserved domain prediction, the results revealed that among the 59 unique genes, the most enriched domains were PnbA and ULP1. Among the 783 expanded genes, the most enriched domains were PKc_like kinases and those belonging to the APH_ChoK_Like family. Conclusion This study sheds light on the genetic basis of F. zanthoxyli’s pathogenicity and evolution which provides valuable information for future research on its molecular interactions with prickly ash and the development of effective strategies to combat stem canker.

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Section: Discussionmentioning

confidence: 95%

Genome sequencing and comparative genomics reveal insights into pathogenicity and evolution of Fusarium zanthoxyli, the causal agent of stem canker in prickly ash

Ruan,

Jiao,

Zhao

et al. 2024

BMC Genomics

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“…However, to date the role of oxidative enzymes in FCW modification has not been deeply investigated in a chitinolytic context. Of note, we recently characterized two CAZymes from U. maydis that act in synergy on β-glucans, namely a glucanase ( Um GH16_1A) active on β-1,3-glucans branched with short β-1,6 substitutions and a dehydrogenase ( Um AA3_2A) active on β-1,3 and β-1,6-gluco-oligosaccharides released by the former ( 37 ). As these substrates are also FCW components, we believe these enzymes could play a role in FCW remodeling.…”

Section: Discussionmentioning

confidence: 99%

“…Compared to fungal saprotrophs and some plant pathogens, the U. maydis genome contains a small set of CAZymes ( 35 ) with 107 GHs and 23 AAs. While studying CAZymes from U. maydis ( 36 , 37 ), we noted the unusual presence of a unique AA10-encoding gene in its genome ( Um AA10), the function of which remains unknown. Interestingly, digging into transcriptomic data collected during U. maydis plant infection cycle ( 38 ), we noted that this Um AA10-encoding gene is overexpressed.…”

Section: Introductionmentioning

confidence: 99%

The Ustilago maydis AA10 LPMO is active on fungal cell wall chitin

Yao,

Reyre,

Tamburrini

et al. 2023

Appl Environ Microbiol

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Lytic polysaccharide monooxygenases (LPMOs) can perform oxidative cleavage of glycosidic bonds in carbohydrate polymers (e.g., cellulose, chitin), making them more accessible to hydrolytic enzymes. While most studies have so far mainly explored the role of LPMOs in a (plant) biomass conversion context, alternative roles and paradigms begin to emerge. The AA10 LPMOs are active on chitin and/or cellulose and mostly found in bacteria and in some viruses and archaea. Interestingly, AA10-encoding genes are also encountered in some pathogenic fungi of the Ustilaginomycetes class, such as Ustilago maydis , responsible for corn smut disease. Transcriptomic studies have shown the overexpression of the AA10 gene during the infectious cycle of U. maydis . In fact, U. maydis has a unique AA10 gene that codes for a catalytic domain appended with a C-terminal disordered region. To date, there is no public report on fungal AA10 LPMOs. In this study, we successfully produced the catalytic domain of this LPMO ( Um AA10_cd) in Pichia pastoris and carried out its biochemical characterization. Our results show that Um AA10_cd oxidatively cleaves α- and β-chitin with C1 regioselectivity and boosts chitin hydrolysis by a GH18 chitinase from U. maydis ( Um GH18A). Using a biologically relevant substrate, we show that Um AA10_cd exhibits enzymatic activity on U. maydis fungal cell wall chitin and promotes its hydrolysis by Um GH18A. These results represent an important step toward the understanding of the role of LPMOs in the fungal cell wall remodeling process during the fungal life cycle. IMPORTANCE Lytic polysaccharide monooxygenases (LPMOs) have been mainly studied in a biotechnological context for the efficient degradation of recalcitrant polysaccharides. Only recently, alternative roles and paradigms begin to emerge. In this study, we provide evidence that the AA10 LPMO from the phytopathogen Ustilago maydis is active against fungal cell wall chitin. Given that chitin-active LPMOs are commonly found in microbes, it is important to consider fungal cell wall as a potential target for this enigmatic class of enzymes.

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“…cinnabarinus proteins were predicted secreted if they fulfilled three conditions: (i) presence of a secretion signal peptide, (ii) absence of endoplasmic reticulum retention motif and (iii) absence of transmembrane helix outside the signal peptide, as described (26). Experimentally validated fungal secreted proteins were retrieved from proteomics analyses (7,(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49), from Uniprot (www.uniprot.org) and FunSecKB2 (50). Metazoans experimentally validated secreted were retrieved from Uniprot, MetazSecKB (51) and the Human Protein Atlas (52,53).…”

Section: Analysis Of Met Content In P Cinnabarinus Fungi Metazoans An...mentioning

confidence: 99%

Methionine oxidation of Carbohydrate-Active enZymes during white-rot wood decay

Molinelli,

Drula,

Gaillard

et al. 2023

Preprint

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White-rot fungi employ secreted carbohydrate-active enzymes (CAZymes) along with reactive oxygen species (ROS), like hydrogen peroxide (H2O2), to degrade lignocellulose in wood. H2O2 serves as a co-substrate for key oxidoreductases during the initial decay phase. While the degradation of lignocellulose by CAZymes is well-documented, the impact of ROS on the oxidation of the secreted proteins remains unclear and the identity of the oxidized proteins is largely unknown. Methionine (Met) can be oxidized to Met sulfoxide (MetO) or Met sulfone (MetO2) with potential deleterious, antioxidant, or regulatory effects. Other residues, like proline (Pro), can undergo carbonylation. Using the white-rot model Pycnoporus cinnabarinus grown on aspen wood, we analyzed the Met content of the secreted proteins and their susceptibility to oxidation combining labelled H218O2 with proteomics. Strikingly, their overall Met content was significantly lower (1.4%) compared to intracellular proteins (2.1%), a feature conserved in fungi but not in other eukaryotes. We also evidenced that a catalase, widespread in white-rot fungi, protects the secreted proteins from oxidation. Our redox proteomics approach allowed identification of 49 oxidizable Met and 40 oxidizable Pro residues within few secreted proteins, mostly CAZymes. Interestingly, many of them had several oxidized residues localized in hotspots. Some Met, including those in GH7 cellobiohydrolases, were oxidized up to 47%, with a substantial percentage of sulfone (13%). These Met are conserved in fungal homologs, suggesting important functional roles. Our findings reveal that white-rot fungi safeguard their secreted proteins by minimizing their Met content and by scavenging ROS and pinpoint redox-active residues in CAZymes.

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The Maize Pathogen Ustilago maydis Secretes Glycoside Hydrolases and Carbohydrate Oxidases Directed toward Components of the Fungal Cell Wall

Abstract: Filamentous fungi play a central regulatory role on Earth, notably in the global carbon cycle. Regardless of their lifestyle, filamentous fungi need to remodel their own cell wall (mostly composed of polysaccharides) to grow and proliferate.

Cited by 11 publications

References 56 publications

Genome sequencing and comparative genomics reveal insights into pathogenicity and evolution of Fusarium zanthoxyli, the causal agent of stem canker in prickly ash

Genome sequencing and comparative genomics reveal insights into pathogenicity and evolution of Fusarium zanthoxyli, the causal agent of stem canker in prickly ash

The Ustilago maydis AA10 LPMO is active on fungal cell wall chitin

Methionine oxidation of Carbohydrate-Active enZymes during white-rot wood decay

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