How the Pathogenic Fungus Alternaria alternata Copes with Stress via the Response Regulators SSK1 and SHO1

Abstract

The tangerine pathotype of Alternaria alternata is a necrotrophic fungal pathogen causing brown spot disease on a number of citrus cultivars. To better understand the dynamics of signal regulation leading to oxidative and osmotic stress response and fungal infection on citrus, phenotypic characterization of the yeast SSK1 response regulator homolog was performed. It was determined that SSK1 responds to diverse environmental stimuli and plays a critical role in fungal pathogenesis. Experiments to determine the phenotypes resulting from the loss of SSK1 reveal that the SSK1 gene product may be fulfilling similar regulatory roles in signaling pathways involving a HOG1 MAP kinase during ROS resistance, osmotic resistance, fungicide sensitivity and fungal virulence. The SSK1 mutants display elevated sensitivity to oxidants, fail to detoxify H2O2 effectively, induce minor necrosis on susceptible citrus leaves, and displays resistance to dicarboximide and phenylpyrrole fungicides. Unlike the SKN7 response regulator, SSK1 and HOG1 confer resistance to salt-induced osmotic stress via an unknown kinase sensor rather than the “two component” histidine kinase HSK1. SSK1 and HOG1 play a moderate role in sugar-induced osmotic stress. We also show that SSK1 mutants are impaired in their ability to produce germ tubes from conidia, indicating a role for the gene product in cell differentiation. SSK1 also is involved in multi-drug resistance. However, deletion of the yeast SHO1 (synthetic high osmolarity) homolog resulted in no noticeable phenotypes. Nonetheless, our results show that A. alternata can sense and react to different types of stress via SSK1, HOG1 and SKN7 in a cooperative manner leading to proper physiological and pathological functions.

The high osmotic response and cell wall integrity pathways cooperate to regulate morphology, microsclerotia development, and virulence in Metarhizium rileyi

“…Moreover, similar phenotypic changes have been observed in other fungi26272840, in which the single-gene disruptions increased sensitivity to cell wall damage, high osmolarity, and oxidative stress, as well as showing convoluted colonies. As in other fungi, these results indicated that the CWI and HOG pathways in M. rileyi could functionally overlap in responding to cell wall damage, osmoregulation, and oxidative stress171924.…”

“…Although fungi have mechanisms that guarantee the specificity of MAPK signalling pathways and that insulate other pathways, the pathways respond to many stress in a coordinated manner1719. In some fungi, the HOG and CWI pathways interact in responses the cell wall202122 and oxidative stresses2324.…”

“…However, the two MAPKs are not restricted to individual stimuli, but their responses can be elicited by various environmental stresses303132. Furthermore, there is some evidence of collaboration between the two MAPKs to counteract various antifungal drugs and environmental stresses202122232433. However, there is no evidence of such a role in regulating MS differentiation.…”

Histone Deacetylase HDA-2 Regulates Trichoderma atroviride Growth, Conidiation, Blue Light Perception, and Oxidative Stress Responses

“…In this regard, similar results for light-regulated genes were published for T. atroviride and Aspergillus nidulans mutants in the tmk3 and sakA genes that code for a mitogen-activated protein kinase (MAPK) orthologous to Hog1p of S. cerevisiae. Importantly, Tmk3 and SakA integrate several stress factors, such as light sensing, stress sensing, and osmosensing (35,36). It is worth noting that in yeast under hyperosmotic stress the repressor Sko1 is phosphorylated by Hog1 and converted to an activator that recruits Hog1 itself as well as the SAGA histone acetyltransferase complex (coactivator) at the promoter of target genes to activate transcription (37).…”

A Major Facilitator Superfamily Transporter-Mediated Resistance to Oxidative Stress and Fungicides Requires Yap1, Skn7, and MAP Kinases in the Citrus Fungal Pathogen Alternaria alternata

“…A . alternata mutant strains lacking the Yap1 transcription activator, the Hog1 mitogen-activated protein (MAP) kinase, the Ssk1 regulator, the Skn7 response regulator, the NADPH oxidase (Nox), or the Gpx3 glutathione peroxidase all displayed hypersensitivity to oxidants and reduced lesion formation on citrus [11,12,14–18]. Exogenous addition of iron partially rescued H 2 O 2 sensitivity seen for Yap1 , Hog1 , Skn7 , and Nox mutants [19], indicating the important role of iron uptake in ROS resistance.…”