The key gluconeogenic gene PCK1 is crucial for virulence of Botrytis cinerea via initiating its conidial germination and host penetration

Abstract

The process of initiation of host invasion and survival of some foliar phytopathogenic fungi in the absence of external nutrients on host leaf surfaces remains obscure. Here, we demonstrate that gluconeogenesis plays an important role in the process and nutrient-starvation adaptation before the pathogen host invasion. Deletion of phosphoenolpyruvate carboxykinase gene BcPCK1 in gluconeogenesis in Botrytis cinerea, the causative agent of grey mould, resulted in the failure of the ΔBcpck1 mutant conidia to germinate on hard and hydrophobic surface and penetrate host cells in the absence of glucose, reduction in conidiation and slow conidium germination in a nutrient-rich medium. The wild-type and ΔBcpck1 conidia germinate similarly in the presence of glucose (higher concentration) as the sole carbon source. Conidial glucose-content should reach a threshold level to initiate germination and host penetration. Infection structure formation by the mutants displayed a glucose-dependent fashion, which corresponded to the mutant virulence reduction. Exogenous glucose or complementation of BcPCK1 completely rescued all the developmental and virulence defects of the mutants. Our findings demonstrate that BcPCK1 plays a crucial role in B. cinerea pathogenic growth and virulence, and provide new insights into gluconeogenesis mediating pathogenesis of plant fungal pathogens via initiation of conidial germination and host penetration.

Transcriptome analysis and functional validation reveal a novel gene, BcCGF1, that enhances fungal virulence by promoting infection‐related development and host penetration

“…Glucose metabolism is one of the basic characteristics of B. cinerea host infection. Glucose mediates pathogen development and pathogenesis via initiating conidial germination, mediating infection structure development, and host penetration (Liu et al, 2018). To (Table S5), suggesting that these enzymes may function in the pathogen CWD and break the plant physical barrier.…”

“…cinerea WT B05.10 and its derived mutant and complemented strains were used in this study (Table S14). All strains were maintained on potato dextrose agar (PDA) or CM as previously described (Liu et al, 2018). The plant materials used in this work included tomato, green bean, strawberry, and apple leaves or fruits.…”

“…At least three independent experiments (triplicate samples examined for each treatment in each experiment) were performed. The assays were performed as previously described (Feng et al, 2017;Cao et al, 2018;Liu et al, 2018).…”

“…Preparation of conidia and onion epidermal cells as well as sample lactophenol blue staining were performed as previously described (Liu et al, 2018(Liu et al, , 2019bHou et al, 2020). The infected samples were microscopically observed, photographically documented, and analysed at 20 hpi.…”

“…Conidia of the pathogen hardly germinate in the presence of only water. Therefore, gluconeogenesis and glucose play a crucial role in the initiation of conidial germination; gluconeogenesis allows the pathogen to cope with the limitation of glucose and/or other carbon sources in the infection niches (Liu et al, 2018). Shortly after conidial germination, the germ tubes cease their polarized cell growth and start to form swollen melanized structures called appressoria.…”