Secreted proteins produced by fungi associated with Botryosphaeria dieback trigger distinct defense responses in Vitis vinifera and Vitis rupestris cells

Abstract

Grapevine trunk diseases (Eutypa dieback, esca and Botryosphaeria dieback) are caused by a complex of xylem-inhabiting fungi, which severely reduce yields in vineyards. Botryosphaeria dieback is associated with Botryosphaeriaceae. In order to develop effective strategies against Botryosphaeria dieback, we investigated the molecular basis of grapevine interactions with a virulent species, Neofusicoccum parvum, and a weak pathogen, Diplodia seriata. We investigated defenses induced by purified secreted fungal proteins within suspension cells of Vitis (Vitis rupestris and Vitis vinifera cv. Gewurztraminer) with putative different susceptibility to Botryosphaeria dieback. Our results show that Vitis cells are able to detect secreted proteins produced by Botryosphaeriaceae, resulting in a rapid alkalinization of the extracellular medium and the production of reactive oxygen species. Concerning early defense responses, N. parvum proteins induced a more intense response compared to D. seriata. Early and late defense responses, i.e., extracellular medium alkalinization, cell death, and expression of PR defense genes were stronger in V. rupestris compared to V. vinifera, except for stilbene production. Secreted Botryosphaeriaceae proteins triggered a high accumulation of δ-viniferin in V. vinifera suspension cells. Artificial inoculation assays on detached canes with N. parvum and D. seriata showed that the development of necrosis is reduced in V. rupestris compared to V. vinifera cv. Gewurztraminer. This may be related to a more efficient induction of defense responses in V. rupestris, although not sufficient to completely inhibit fungal colonization. Overall, our work shows a specific signature of defense responses depending on the grapevine genotype and the fungal species.

Comparison of the Molecular Responses of Tolerant, Susceptible and Highly Susceptible Grapevine Cultivars During Interaction With the Pathogenic Fungus Eutypa lata

“…We took advantage of the millicell system, which imposes strictly controlled conditions of elicitation, to compare general defenses of Merlot, Cabernet Sauvignon, and Ugni Blanc cultivars, previously described as differentially affected by E. lata (Figure 1). We analyzed the relative expression levels of seven genes encoding PR proteins in leaves, chosen as representative of different defense signaling pathways in grapevine (Jacobs et al, 1999; Robert et al, 2001; Aziz et al, 2003, 2004; Liu and Ekramoddoullah, 2006; Chong et al, 2008; Giacomelli et al, 2012; Spagnolo et al, 2017; Stempien et al, 2017).…”

Fungal canker pathogens trigger carbon starvation by inhibiting carbon metabolism in poplar stems

“…The change of gene expression was likely induced by the secondary metabolites (such as toxins, secreted proteins, etc.) 37,38 , and so might occur at all stages of canker disease. Therefore, in addition to inhibiting photosynthesis, the two canker pathogens directly modulated carbon metabolism around the inoculation sites.…”

Transcriptional response of grapevine to infection with the fungal pathogen Lasiodiplodia theobromae

“…Most studies on woody tissues responding to pathogen infection have focused on the plant’s physical responses or metabolic changes, such as formation of tyloses and gels in xylem 24 , cell wall modifications with suberin 25 , production of resins 26 , and accumulation of peroxidases, superoxide dismutases, glutathione S-transferases, phenolic compounds, stilbenes, and phytoalexins 20,27–32 . Recently, defense responses, for example, cell death, expression of pathogenesis-related (PR) genes, and alkalinization of extracellular medium, were observed to be induced by purified secreted proteins isolated from two Botryosphaeriaceae species, Neofusicoccum parvum and Diplodia seriata , in Vitis suspension cells 33 . In recent decades, RNA sequencing (RNA-seq) has enabled the study of the transcriptional responses of woody plants to phytopathogens, revealing that genes involved in cell wall biosynthesis, hormone signal transduction and secondary metabolism processes play important roles 34–37 .…”