Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in Fusarium graminearum

Abstract

Autophagy is a conserved cellular recycling and trafficking pathway in eukaryotic cells and has been reported to be important in the virulence of a number of microbial pathogens. Here, we report genome-wide identification and characterization of autophagy-related genes (ATGs) in the wheat pathogenic fungus Fusarium graminearum. We identified twenty-eight genes associated with the regulation and operation of autophagy in F. graminearum. Using targeted gene deletion, we generated a set of 28 isogenic mutants. Autophagy mutants were classified into two groups by differences in their growth patterns. Radial growth of 18 Group 1 ATG mutants was significantly reduced compared to the wild-type strain PH-1, while 10 Group 2 mutants grew normally. Loss of any of the ATG genes, except FgATG17, prevented the fungus from causing Fusarium head blight disease. Moreover, subsets of autophagy genes were necessary for asexual/sexual differentiation and deoxynivalenol (DON) production, respectively. FgATG1 and FgATG5 were investigated in detail and showed severe defects in autophagy. Taken together, we conclude that autophagy plays a critical role in growth, asexual/sexual sporulation, deoxynivalenol production and virulence in F. graminearum.

Independent losses and duplications of autophagy‐related genes in fungal tree of life

“…Autophagy is known to be important for sexual reproduction in fungi (Wang et al, 2011;Voigt and Poggeler, 2013;Lv et al, 2017). Recently, it has been reported that A-to-I RNA editing occurs specifically during sexual reproduction in F. graminearum, N. crassa and other filamentous ascomycetes (Liu et al, , 2017.…”

“…In plants, autophagy is important for seedling establishment, plant development, senescence, stress resistance, metabolism and reproduction (Liu et al, 2005;Bassham et al, 2006;Avila-Ospina et al, 2014;Michaeli et al, 2016). In fungi, autophagy affects growth, morphology, development, lipid turnover and sexual reproduction (Kershaw and Talbot, 2009;Pollack et al, 2009;Nguyen et al, 2011;Josefsen et al, 2012;Liu et al, 2012;Duan et al, 2013;Voigt and Poggeler, 2013;Lv et al, 2017). In fungal pathogens, autophagy is also known to be important for plant or animal infection.…”

“…For example, deletion any of the 16 ATG genes required for nonselective autophagy in the rice blast fungus Magnaporthe oryzae affected its virulence (Kershaw and Talbot, 2009). Mutants of many ATG genes were defective in toxin production and plant infection (Nguyen et al, 2011;Wang et al, 2011;Josefsen et al, 2012;Lv et al, 2017) in another ascomycete Fusarium graminearum, the main causal agent of Fusarium head blight (FHB). In human pathogen Cryptococcus neoformans, knockdown of ATG8 results in attenuated virulence in a mouse model of infection (Hu et al, 2008).…”

Current opinions on autophagy in pathogenicity of fungi

“…The second category consists of Atg6, Vps38, Vps34 and Vps15, which are mainly involved in the endocytic pathway. It was recently reported that in nematodes, Atg6 regulates the processes of endocytosis Fusarium graminearum Reduced Reduced [27] and autophagy through the competitive binding of Vps38 and Atg14, and crosstalk exists between these two pathways, i.e., the autophagy pathway is promoted if the endocytic pathway is inhibited. This phenomenon has also been observed in fungi [19].…”

Fusarium diseases: biology and management perspectives

“…This suggests that the shift of infection mechanisms may be regulated by nutrient deprivation during the biotrophic phase (Brown et al 2017). Indeed, autophagy mechanisms used to maintain homeostasis in fungal cells and recycle nutrients were shown to be necessary for growth and pathogenicity (Lv et al 2017). Furthermore, Brown et al (2017) found that the expression of several effector genes were upregulated during infection and interestingly, this secreted protein cocktail appears to be specific for each phase and their location in the genome aligns with high recombination regions.…”