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- Title
Oxaloacetate anaplerosis differently contributes to pathogenicity in plant pathogenic fungi Fusarium graminearum and F. oxysporum.
- Authors
Shin, Soobin; Bong, Seonghun; Moon, Heeji; Jeon, Hosung; Kim, Hun; Choi, Gyung Ja; Lee, Do Yup; Son, Hokyoung
- Abstract
Anaplerosis refers to enzymatic reactions or pathways replenishing metabolic intermediates in the tricarboxylic acid (TCA) cycle. Pyruvate carboxylase (PYC) plays an important anaplerotic role by catalyzing pyruvate carboxylation, forming oxaloacetate. Although PYC orthologs are well conserved in prokaryotes and eukaryotes, their pathobiological functions in filamentous pathogenic fungi have yet to be fully understood. Here, we delve into the molecular functions of the ortholog gene PYC1 in Fusarium graminearum and F. oxysporum, prominent fungal plant pathogens with distinct pathosystems, demonstrating variations in carbon metabolism for pathogenesis. Surprisingly, the PYC1 deletion mutant of F. oxysporum exhibited pleiotropic defects in hyphal growth, conidiation, and virulence, unlike F. graminearum, where PYC1 deletion did not significantly impact virulence. To further explore the species-specific effects of PYC1 deletion on pathogenicity, we conducted comprehensive metabolic profiling. Despite shared metabolic changes, distinct reprogramming in central carbon and nitrogen metabolism was identified. Specifically, alpha-ketoglutarate, a key link between the TCA cycle and amino acid metabolism, showed significant down-regulation exclusively in the PYC1 deletion mutant of F. oxysporum. The metabolic response associated with pathogenicity was notably characterized by S-methyl-5-thioadenosine and S-adenosyl-L-methionine. This research sheds light on how PYC1-mediated anaplerosis affects fungal metabolism and reveals species-specific variations, exemplified in F. graminearum and F. oxysporum. Author summary: Pyruvate carboxylase plays a crucial role in replenishing oxaloacetate in the tricarboxylic acid cycle, a fundamental carbon metabolic pathway. While PYC is present in both prokaryotes and eukaryotes, its specific contribution to the development and pathogenesis of fungal pathogens remains poorly understood. Our study focuses on elucidating the function of PYC, particularly investigating the effects of deleting the ortholog gene PYC1 in two important fungal plant pathogens, Fusarium graminearum and F. oxysporum, which have distinct pathosystems. By conducting comprehensive genetic and metabolic profiling, we observed different impacts on fungal developmental processes and pathogenicity between the two species. In particular, the deletion of the PYC1 gene in F. oxysporum led to a unique metabolic profile and the subsequent loss of pathogenicity. This research provides valuable insights into the distinct effects of PYC1-mediated anaplerosis on fungal metabolism in pathogenic fungi, contributing to a more profound understanding of the molecular mechanisms governing fungal pathogenesis.
- Subjects
KREBS cycle; PHYTOPATHOGENIC microorganisms; PHYTOPATHOGENIC fungi; FUNGAL metabolism; PYRUVATE carboxylase; FUSARIUM oxysporum
- Publication
PLoS Pathogens, 2024, Vol 20, Issue 9, p1
- ISSN
1553-7366
- Publication type
Article
- DOI
10.1371/journal.ppat.1012544