Novel Aspects on The Interaction Between Grapevine and Plasmopara viticola: Dual-RNA-Seq Analysis Highlights Gene Expression Dynamics in The Pathogen and The Plant During The Battle For Infection

Abstract

Mgaloblishvili, a Vitis vinifera cultivar, exhibits unique resistance traits against Plasmopara viticola, the downy mildew agent. This offers the unique opportunity of exploring the molecular responses in compatible and incompatible plant-pathogen interaction. In this study, whole transcriptomes of Mgaloblishvili, Pinot noir (a V. vinifera susceptible cultivar), and Bianca (a resistant hybrid) leaves, inoculated and non-inoculated with the pathogen, were used to identify P. viticola effector-encoding genes and plant susceptibility/resistance genes. Multiple effector-encoding genes were identified in P. viticola transcriptome, with remarkable expression differences in relation to the inoculated grapevine cultivar. Intriguingly, five apoplastic effectors specifically associated with resistance in V. vinifera. Gene coexpression network analysis identified specific modules and metabolic changes occurring during infection in the three grapevine cultivars. Analysis of these data allowed, for the first time, the detection in V. vinifera of a putative P. viticola susceptibility gene, encoding a LOB domain-containing protein. Finally, the de novo assembly of Mgaloblishvili, Pinot noir, and Bianca transcriptomes and their comparison highlighted novel candidate genes that might be at the basis of the resistant phenotype. These results open the way to functional analysis studies and to new perspectives in molecular breeding of grapevine for resistance to P. viticola.

Georgian Grapevine Cultivars: Ancient Biodiversity for Future Viticulture

“…Susceptibility genes are essential for plant-pathogen interaction and their disruption leads to resistance, as with mlo gene, whose knockdown is involved in resistance to E. necator (Pessina et al, 2016). The candidate gene related to susceptibility to P. viticola in V. vinifera encodes an LOB domain-containing (LBD) protein (Toffolatti et al, 2020) that has been previously found in the interaction between Arabidopsis thaliana and Fusarium oxysporum (Thatcher et al, 2012). The new genome editing tools, providing several protocols to introduce knockout on target sequences, makes the understanding of plant pathogenresistance mechanism mediated by susceptibility genes a very attractive alternative for the development of durable diseaseresistant varieties (Zaidi et al, 2018).…”

Rpv29, Rpv30 and Rpv31: Three Novel Genomic Loci Associated With Resistance to Plasmopara viticola in Vitis vinifera

“…GWA results corroborate the involvement of these receptors in triggering the plant response. Indeed, during the infection process P. viticola has shown the expression of numerous different cytoplasmic and apoplastic effectors ( Toffolatti et al, 2020 ) and their interaction with the NB-LRR receptors of the plant should be further investigated. Since no hypersensitive response (HR) was observed in the Georgian resistant accessions, due to absence of co-evolution with the pathogen, the involvement of the effector receptor Lr10 could be associated with an effector-triggered immunity not associated with HR.…”

“…vinifera varieties ( Bitsadze et al, 2015 ; Toffolatti et al, 2016 ) coming from the first domestication center of the species: Georgia, Southern Caucasus ( Imazio et al, 2013 ). The resistance mechanism for one of these resistant cultivars, named Mgaloblishvili, has been studied in detail ( Toffolatti et al, 2018a , 2020 ). After artificial inoculation, P. viticola growth and sporulation are significantly affected in Mgaloblishvili: the mycelium degenerates, sporangiophores show an altered morphology and lower numbers of sporangia are produced, without any evidences of the hypersensitive response that occurs in American species.…”

Fungicide Resistance Evolution and Detection in Plant Pathogens: Plasmopara viticola as a Case Study

“…P. viticola is an obligate parasite of grapevine, causing the main damage to the Eurasian grapevine species ( Vitis vinifera ), which is the most cultivated species worldwide due to the high quality of its grapes. Most of the V. vinifera cultivars are highly susceptible to the pathogen, and only recently have sources of resistance been found in the center of origin of viticulture, which is located in Georgia (South Caucasus) [ 2 , 3 ]. This high susceptibility makes chemical control of the pathogen the most important measure to ensure an adequate yield.…”