Intracellular polyamines regulate redox homeostasis with cAMP–PKA signalling during sexual mating/filamentation and pathogenicity of Sporisorium scitamineum

Author:

Yin Kai12ORCID,Cui Guobing12,Bi Xinping12,Liang Meiling3,Hu Zhijian12,Deng Yi Zhen12ORCID

Affiliation:

1. Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources, College of Plant Protection South China Agricultural University Guangzhou China

2. Integrative Microbiology Research Centre, Guangdong Province Key Laboratory of Microbial Signals and Disease Control South China Agricultural University Guangzhou China

3. Guangdong Provincial Key Laboratory of High Technology for Plant Protection, Plant Protection Research Institute of Guangdong Academy of Agricultural Sciences Guangzhou China

Abstract

AbstractSugarcane smut caused by Sporisorium scitamineum seriously impairs sugarcane production and quality. Sexual mating/filamentation is a critical step of S. scitamineum pathogenesis, yet the regulatory mechanisms are not fully understood. In this study, we identified the SsAGA, SsODC, and SsSAMDC genes, which are involved in polyamine biosynthesis in S. scitamineum. Deletion of SsODC led to complete loss of filamentous growth after sexual mating, and deletion of SsAGA or SsSAMDC caused reduced filamentation. Double deletion of SsODC and SsSAMDC resulted in auxotrophy for putrescine (PUT) and spermidine (SPD) when grown on minimal medium (MM), indicating that these two genes encode enzymes that are critical for PUT and SPD biosynthesis. We further showed that low PUT concentrations promoted S. scitamineum filamentation, while high PUT concentrations suppressed filamentation. Disrupted fungal polyamine biosynthesis also resulted in a loss of pathogenicity and reduced fungal biomass within infected plants at the early infection stage. SPD formed a gradient from the diseased part to nonsymptom parts of the cane stem, suggesting that SPD is probably favourable for fungal virulence. Mutants of the cAMP–PKA (SsGPA3–SsUAC1–SsADR1) signalling pathway displayed up‐regulation of the SsODC gene and elevated intracellular levels of PUT. SsODC directly interacted with SsGPA3, and sporidia of the ss1uac1ΔodcΔ mutant displayed abundant pseudohyphae. Furthermore, we found that elevated PUT levels caused accumulation of intracellular reactive oxygen species (ROS), probably by suppressing transcription of ROS‐scavenging enzymes, while SPD played the opposite role. Overall, our work proves that polyamines play important roles in the pathogenic development of sugarcane smut fungus, probably by collaboratively regulating intracellular redox homeostasis with the cAMP–PKA signalling pathway.

Funder

National Natural Science Foundation of China

Publisher

Wiley

Subject

Plant Science,Soil Science,Agronomy and Crop Science,Molecular Biology

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