MaHog1, a Hog1-type mitogen-activated protein kinase gene, contributes to stress tolerance and virulence of the entomopathogenic fungus Metarhizium acridum

Abstract

Fungal biocontrol agents have great potential in integrated pest management. However, poor efficacy and sensitivity to various adverse factors have hampered their wide application. In eukaryotic cells, Hog1 kinase plays a critical role in stress responses. In this study, MaHog1 (GenBank accession no. EFY85878), encoding a member of the Hog1/Sty1/p38 mitogenactivated protein kinase family in Metarhizium (Me.) acridum, was identified. Targeted gene disruption was used to analyse the role of MaHog1 in virulence and tolerance of adverse factors. Mutants with MaHog1 depletion showed increased sensitivity to high osmotic stress, high temperature and oxidative stress, and exhibited remarkable resistance to cell wall-disturbing agents. These results suggest that Hog1 kinase has a conserved function in regulating multistress responses among fungi, and that MaHog1 might influence cell wall biogenesis in Me. acridum. Bioassays conducted with topical inoculation and intrahaemocoel injection revealed that MaHog1 is required for both penetration and postpenetration development of Me. acridum. MaHog1 disruption resulted in a significant reduction in virulence, likely due to the combination of a decrease in conidial germination, a reduction in appressorium formation and a decline in growth rate in insect haemolymph, which might be caused by impairing fungal tolerance of various stresses during infection.

Agrobacterium tumefaciens-Mediated Transformation of Pseudocercospora fijiensis to Determine the Role of PfHog1 in Osmotic Stress Regulation and Virulence Modulation

“…Our results indicated that PfHog1 is an important regulator of osmotic tolerance in P. fijiensis , similar to previous reports on other filamentous fungi and yeasts (Beever and Laracy, 1986; Schuller et al, 1994; Jin et al, 2012; Babazadeh et al, 2013; Wang et al, 2016). The growth and development of mycelia fragments of Δ PfHog1 mutants were suppressed on PDA medium supplemented with 1 M NaCl; whereas WT P. fijiensis showed normal growth and development of mycelia.…”

“…For example, HOG1 pathway was found critical in regulating colonization of mouse gastrointestinal tract in Candida albicans (Prieto et al, 2014). In the entomopathogenic fungus Metarhizium acridum , MaHog1 , a member of the Hog1/Sty1/ p38 MAP-kinase gene family, has been shown to be critical for adaptation to hyper osmolarity, high temperature and oxidative stress (Jin et al, 2012). It is also an important virulence factor as disruption of MaHog1 results in reduced infectivity and growth of the fungus on its insect hosts (Jin et al, 2012).…”

“…In the entomopathogenic fungus Metarhizium acridum , MaHog1 , a member of the Hog1/Sty1/ p38 MAP-kinase gene family, has been shown to be critical for adaptation to hyper osmolarity, high temperature and oxidative stress (Jin et al, 2012). It is also an important virulence factor as disruption of MaHog1 results in reduced infectivity and growth of the fungus on its insect hosts (Jin et al, 2012). In a similar way, Hog1 is also activated in response to high osmolarity, oxidative stress, and other stress stimuli in S. cerevisiae and the human pathogenic yeast C. albicans (Alonso-Monge et al, 2001; Winkler et al, 2002), whereas in the wheat pathogen Zymoseptoria tritici (synonym M. graminicola ), Hog1 regulates dimorphism and pathogenicity (Mehrabi et al, 2006).…”

Stress response signaling and virulence: insights from entomopathogenic fungi

“…These central pathways in turn regulate, typically via phosphorylation, downstream effectors including transcription factors that can be either activated or repressed by the incoming signal. The transcription factors affect the expression of genes in response to the original signal phenotype seen in B. bassiana, disruption of the Mahog1 gene resulted in increased sensitivity to osmotic and oxidative stress, with a counterbalance of decreased sensitivity to cell wall perturbing reagents such as calcofluor white and Congo red (Jin et al 2012). As seen in B. bassiana, the ΔMahog1 strain displayed reduced conidial germination, appressorium formation, and virulence.…”

Enhanced virulence of Fusarium species associated with spear rot of oil palm following recovery from osmotic stress

“…The osmoregulation MAPK pathway is well conserved in fungi. The inactivation of Hog1 orthologs increases sensitivity to osmotic stress and attenuates the virulence of Beauveria bassiana (Zhang et al 2009), Cryphonectria parasitica (Park et al 2004), Fusarium graminearum (Zheng et al 2012) and Metarhizium acridum (Jin et al 2012), and Ustilaginoidea virens (Zheng et al 2016). The osmoadaptative response of F. verticillioides is also coupled to the marked induction of FUM1 gene expression, a gene required for fumonisin biosynthesis (Marín et al 2010).…”