The triglyceride catabolism regulated by a serine/threonine protein phosphatase, Smek1, is required for development and plant infection in Magnaporthe oryzae

Abstract

Magnaporthe oryzae is a pathogenic fungus that seriously harms rice production. Phosphatases and carbon metabolism play crucial roles in the growth and development of eukaryotes. However, it remains unclear how serine/threonine phosphatases regulate the catabolism of triglycerides, a major form of stored lipids. In this study, we identified a serine/threonine protein phosphatase regulatory subunit, Smek1, which is required for the growth, conidiation, and virulence of M. oryzae. Deletion of SMEK1 led to defects in the utilization of lipids, arabinose, glycerol, and ethanol. In glucose medium, the expression of genes involved in lipolysis, long‐chain fatty acid degradation, β‐oxidation, and the glyoxylate cycle increased in the Δsmek1 mutant, which is consistent with ΔcreA in which a carbon catabolite repressor CREA was deleted. In lipid medium, the expression of genes involved in long‐chain fatty acid degradation, β‐oxidation, the glyoxylate cycle, and utilization of arabinose, ethanol, or glycerol decreased in the Δsmek1 mutant, which is consistent with Δcrf1 in which a transcription activator CRF1 required for carbon metabolism was deleted. Lipase activity, however, increased in the Δsmek1 mutant in both glucose and lipid media. Moreover, Smek1 directly interacted with CreA and Crf1, and dephosphorylated CreA and Crf1 in vivo. The phosphatase Smek1 is therefore a dual‐function regulator of the lipid and carbohydrate metabolism, and controls fungal development and virulence by coordinating the functions of CreA and Crf1 in carbon catabolite repression (CCR) and derepression (CCDR).

The Methylcitrate Cycle and Its Crosstalk with the Glyoxylate Cycle and Tricarboxylic Acid Cycle in Pathogenic Fungi

“…In S. cerevisiae , the expression of ICL2 (encoding 2-methylisocitrate lyase) and ICL1 (encoding isocitrate lyase with a low 2-methylisocitrate lyase activity) is repressed by glucose and induced by ethanol or threonine [ 41 , 53 ]. In M. oryzae , the expression of MoICL1 and MoMCL1 was repressed by glucose and induced by lipid [ 54 ]. When glucose is used as the carbon source, the phosphatase Smek1 activates the carbon catabolite repressor CreA and inhibits the expression of MoICL1 and MoMCL1 ; while lipid is used as the carbon source, Smek1 activates the transcription activator Crf1 and promotes the expression of MoICL1 and MoMCL1 [ 34 , 54 ].…”

“…In M. oryzae , the expression of MoICL1 and MoMCL1 was repressed by glucose and induced by lipid [ 54 ]. When glucose is used as the carbon source, the phosphatase Smek1 activates the carbon catabolite repressor CreA and inhibits the expression of MoICL1 and MoMCL1 ; while lipid is used as the carbon source, Smek1 activates the transcription activator Crf1 and promotes the expression of MoICL1 and MoMCL1 [ 34 , 54 ].…”