The novel bZIP transcription factor Fpo1 negatively regulates perithecial development by modulating carbon metabolism in the ascomycete fungus Fusarium graminearum

Abstract

Summary Fungal sexual reproduction requires complex cellular differentiation processes of hyphal cells. The plant pathogenic fungus Fusarium graminearum produces fruiting bodies called perithecia via sexual reproduction, and perithecia forcibly discharge ascospores into the air for disease initiation and propagation. Lipid metabolism and accumulation are closely related to perithecium formation, yet the molecular mechanisms that regulate these processes are largely unknown. Here, we report that a novel fungal specific bZIP transcription factor, F. graminearum perithecium overproducing 1 (Fpo1), plays a role as a global transcriptional repressor during perithecium production and maturation in F. graminearum. Deletion of FPO1 resulted in reduced vegetative growth, asexual sporulation and virulence and overproduced perithecium, which reached maturity earlier, compared with the wild type. Intriguingly, the hyphae of the fpo1 mutant accumulated excess lipids during perithecium production. Using a combination of molecular biological, transcriptomic and biochemical approaches, we demonstrate that repression of FPO1 after sexual induction leads to reprogramming of carbon metabolism, particularly fatty acid production, which affects sexual reproduction of this fungus. This is the first report of a perithecium‐overproducing F. graminearum mutant, and the findings provide comprehensive insight into the role of modulation of carbon metabolism in the sexual reproduction of fungi.

Genome‐wide analysis of bZIP gene family members in Pleurotus ostreatus, and potential roles of PobZIP3 in development and the heat stress response

“…The bZIP TFs, which are prevalent among and exclusive to eukaryotes, are among the largest and most versatile TF families (Wen et al, 2021). They are required for numerous vital biological processes in fungi, including several types of stress responses, mycelial growth, and primary and secondary metabolism (Shin et al, 2020;Wang, Zha, et al, 2020;Wen et al, 2021).…”

Genome-Wide Identification and Functional Analysis of the bZIP Transcription Factor Family in Rice Bakanae Disease Pathogen, Fusarium fujikuroi

“…According to the published literature, a large number of bZIP TFs have been found in the genomes of many fungi such as Alternaria sp. [ 26 ], Phytophthora sojae [ 27 ], Sclerotinia sclerotiorum [ 28 ], Aspergillus niger [ 29 ], F. graminearum [ 30 , 31 ] and F. pseudograminearum [ 32 ]. Only a few bZIP TFs in fungi have been systematically identified, such as those in M. oryzae [ 9 ] and F. graminearum [ 33 ].…”

The bZIP transcription factor UvbZIP6 mediates fungal growth, stress response, and false smut formation in Ustilaginoidea virens

“…Overexpressing DKM, a bZIP gene in Arabidopsis, causes defects in vegetative and reproductive development, whereas DKM deletion mutants have more floral buds and longer fruits (Lozano-Sotomayor et al 2016). In addition to reducing vegetative growth, asexual sporulation, and virulence, the deletion of Fpo1 in F. graminearum increases the production and maturation of perithecia (Shin et al 2020). In this study, although UvbZIP6-knockout mutants caused a successful infection, they lost the ability to form false smut balls, indicating that UvbZIP6 plays a critical role in the formation of false smut balls.…”

“…In Fusarium graminearum, Fpo1, a negative regulator of perithecium development, is crucial for vegetative growth, asexual sporulation, and virulence. Deletion of Fpo1 results in reprogramming of the carbon metabolism, including fatty acid production, which is essential for sexual reproduction (Shin et al 2020). Mrap1 regulates fungal morphology, virulence, and microsclerotia formation in Metarhizium rileyi (Song et al 2018).…”