Dissecting the role of histidine kinase and HOG1 mitogen-activated protein kinase signalling in stress tolerance and pathogenicity of Parastagonospora nodorum on wheat

Abstract

The HOG1 mitogen-activated protein kinase (MAPK) pathway is activated through two-component histidine kinase (HK) signalling. This pathway was first characterized in the budding yeast Saccharomyces cerevisiae as a regulator of osmotolerance. The fungus Parastagonospora nodorum is the causal agent of septoria nodorum blotch of wheat. This pathogen uses host-specific effectors in tandem with general pathogenicity mechanisms to carry out its infection process. Genes showing strong sequence homology to S. cerevisiae HOG1 signalling pathway genes have been identified in the genome of P. nodorum. In this study, we examined the role of the pathway in the virulence of P. nodorum on wheat by disrupting putative pathway component genes: HOG1 (SNOG_13296) MAPK and NIK1 (SNOG_11631) hybrid HK. Mutants deleted in NIK1 and HOG1 were insensitive to dicarboximide and phenylpyrrole fungicides, but not a fungicide that targets ergosterol biosynthesis. Furthermore, both Δnik1 and Δhog1 mutants showed increased sensitivity to hyperosmotic stress. However, HOG1, but not NIK1, is required for tolerance to elevated temperatures. HOG1 deletion conferred increased tolerance to 6-methoxy-2-benzoxazolinone, a cereal phytoalexin. This suggests that the HOG1 signalling pathway is not exclusively associated with NIK1. Both Δnik1 and Δhog1 mutants retained the ability to infect and cause necrotic lesions on wheat. However, we observed that the Δhog1 mutation resulted in reduced production of pycnidia, asexual fruiting bodies that facilitate spore dispersal during late infection. Our study demonstrated the overlapping and distinct roles of a HOG1 MAPK and two-component HK signalling in P. nodorum growth and pathogenicity.

Shifts in Host Mucosal Innate Immune Function Are Associated with Ruminal Microbial Succession in Supplemental Feeding and Grazing Goats at Different Ages

“…Secondly, some species of Methanosphera , which have been reported to activate host dendritic cells, and induce release of inflammatory cytokines TNFα and IL1β ( Bang et al, 2014 ), were more abundant in the rumen of G kids due to the pectins in the forages ( Janssen and Kirs, 2008 ). Finally, Microcyclosporella and Parastagonospora are well-known fungal plant–pathogens ( Frank et al, 2010 ; John et al, 2016 ), and their greater relative abundances in the rumen of G kids suggest the notion that fungal composition is diet-driven ( Denman et al, 2008 ; Kittelmann et al, 2012 ), which provokes further consideration of their roles in modulating host immune function.…”

Spontaneous and CRISPR/Cas9-induced mutation of the osmosensor histidine kinase of the canola pathogen Leptosphaeria maculans

“…Resistance to iprodione and other dicarboximide fungicides and the underlying mechanisms have been well characterized in other plant pathogenic fungi, such as Botrytis cinerea [ 30 – 32 ]. The impact of mutation of hos1 in plant pathogens varies, in some cases impacting pathogenicity and in others having no effect [ 16 ]. Hallmarks of impairing the HOG pathway, i.e.…”

“…Studies in other plant pathogenic fungi show differing results in terms of the contribution of the histidine kinase to pathogenicity. Similar to L. maculans , disruption of the gene does not impair pathogenicity in Alternaria alternata , Parastagonospora nodorum and Pyricularia oryzae [ 16 , 33 , 34 ]. In contrast, the homolog is required for pathogenicity in Botrytis cinerea , Fusarium oxysporum , Monilinia fructicola , Sclerotinia sclerotiorum and Ustilago maydis [ 35 – 39 ].…”

“…The colony diameter was measured in two perpendicular directions and values recorded in millimeters. EC 50 values were calculated as described previously [ 16 ]. EC 50 values of wild type and complemented strains were analyzed by the Mann–Whitney U -test.…”

“…The HOG pathway features a sensing histidine kinase that transfers environmental information into a cascade of three mitogen activated protein kinases [ 12 ]. Mutations often occur in the homologs of the histidine kinase in other fungi to confer resistance to the dicarboximide fungicides [ 16 ].…”