A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum

Yan Xu; Yilan Qiu; Yuelin Zhang; Xin Li

doi:10.3389/fpls.2023.1175552

A cAMP phosphodiesterase is essential for sclerotia formation and virulence in Sclerotinia sclerotiorum

Front Plant Sci. 2023 May 31:14:1175552. doi: 10.3389/fpls.2023.1175552. eCollection 2023.

Authors

Yan Xu^{1

2}, Yilan Qiu³, Yuelin Zhang², Xin Li^{1

2}

Affiliations

¹ Michael Smith Laboratories, University of British Columbia, Vancouver, BC, Canada.
² Department of Botany, University of British Columbia, Vancouver, BC, Canada.
³ Department of Life Science, Hunan Normal University, Changsha, China.

Abstract

Sclerotinia sclerotiorum is a plant pathogenic fungus that causes white mold or stem rot diseases. It affects mostly dicotyledonous crops, resulting in significant economic losses worldwide. Sclerotia formation is a special feature of S. sclerotiorum, allowing its survival in soil for extended periods and facilitates the spread of the pathogen. However, the detailed molecular mechanisms of how sclerotia are formed and how virulence is achieved in S. sclerotiorum are not fully understood. Here, we report the identification of a mutant that cannot form sclerotia using a forward genetics approach. Next-generation sequencing of the mutant's whole genome revealed candidate genes. Through knockout experiments, the causal gene was found to encode a cAMP phosphodiesterase (SsPDE2). From mutant phenotypic examinations, we found that SsPDE2 plays essential roles not only in sclerotia formation, but also in the regulation of oxalic acid accumulation, infection cushion functionality and virulence. Downregulation of SsSMK1 transcripts in Sspde2 mutants revealed that these morphological defects are likely caused by cAMP-dependent inhibition of MAPK signaling. Moreover, when we introduced HIGS construct targeting SsPDE2 in Nicotiana benthamiana, largely compromised virulence was observed against S. sclerotiorum. Taken together, SsPDE2 is indispensable for key biological processes of S. sclerotiorum and can potentially serve as a HIGS target to control stem rot in the field.

Keywords: Sclerotinia sclerotiorum; cAMP; cAMP phosphodiesterase; forward genetics; host-induced gene silencing; next-generation sequencing; oxalic acid; pathogen control.

Grants and funding

XL and YZ were financially supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery, NSERC-CREATE-PRoTECT, Canada Research Chair (CRC) to XL, and the Canadian Foundation for Innovation (CFI-JELF) programs. YX and YQ were partly supported by Chinese Scholarship Council.