Genomic and Transcriptomic Analyses Provide Insights Into Erysiphe necator Pathogenicity and Grapevine Response

Grapevine powdery mildew, caused by the fungus Erysiphe necator, is one of the most prevalent obligate biotrophic pathogens in vineyards, posing a significant threat to grape production. Despite its impact, research on E. necator pathogenicity and grapevine responses remains limited. In this study, we assembled a high-quality 69.93 Mb genome for E. necator isolate NAFU1, identifying 248 candidate-secreted effector proteins (CSEPs). RNA-Seq analysis of E. necator NAFU1 and the grapevine host during various infection stages revealed that expression of many genes, especially those encoding CSEPs, was induced in planta to facilitate host colonisation. Detailed analysis identified CSEP118 as a key highly induced effector gene, plays an important role in suppression of host defence. CSEP118 appears to interfere with the grapevine defence response to infection by targeting VviTrxz, a grapevine thioredoxin. Comparative transcriptome analysis of susceptible (Vitis vinifera cv. Cabernet Sauvignon) and resistant (Vitis piasezkii accession Baishui-40) grapevines upon infection by E. necator identified VviTCP14, encoding a transcription factor, to be a likely negative regulator of grapevine resistance against E. necator. Supporting this, VviTCP14-silenced plants exhibited increased expression of resistance-related genes such as those encoding stilbene synthases (STSs) and elevated stilbene contents when compared with the wild type grapevine. In summary, this study utilised a multi-omics approach to understand mechanisms underlying E. necator effector-triggered suppression of grapevine immunity and transcriptional regulation of host defence response during grapevine-powdery mildew interaction. The regulatory mechanisms uncovered in this study should provide valuable insights for improving grapevine resistance to powdery mildew.