Plant breeding for resistance to disease is mainly focused on dominant plant genes, known as resistance or R-genes, which enable the recognition of would-be pathogens and the activation of opportune defense pathway s. However, resistance mediated by R-genes is frequently rapidly overcome in the field by the onset of new pathogen genetic variants. Furthermore, the loss of genetic biodiversity often hampers the identification of new R-genes to be used for breeding of species of agronomic importance. In this review, an alternative breeding strategy is proposed by looking at resistance as a condition originated by the lack of plant genes necessary for pathogenesis, here referred to as susceptibility genes or Sgenes. In the last few years, several S-genes have been identified, following both classic phenotypic screenings in natural germplasm and reverse genetic approaches, such as targeted mutagenesis or gene silencing/overexpression. Their molecular characterization revealed for most of them a role as: 1) virulence targets, which are used by pathogen effector molecules to alter cell metabolism and promote disease; 2) negative regulators of defense responses activated by the plant immune system. Although they are necessary for pathogenesis, S-genes have not been excluded by evolution, thus indicating that they are likely important for plant evolutionary fitness. However, resistance due to the loss of S-genes is sometimes devoid of pleiotropic effects undesirable for agricultural purposes, and thus could be conveniently exploited in plant breeding. Indeed, some Sgene loss-of-function mutations, the most famous being mlo in barley, have been successfully introduced in commercial cultivars. In contrast with R-gene mediated resistance and similarly to non-host resistance (i.e. the immunity of a plant species towards pathogens evolved to cause disease in other plant species), resistance due to the loss of S-genes is race-non-specific and durable. Likely, these two kind of immunity are originated by similar molecular mechanisms, as suggested by a series of genetic, biochemical, histological evidence reported in the last few years. In addition, both of them are referable to the lack of interaction between pathogen effectors and their cognate plant virulence targets. The availability of large genomic database can allow the detection of S-genes orthologues across species, whose inactivation could be fulfilled in order to identify new resistant sources. Advances in genomics and in reverse genetics techniques, such as targeted mutagenesis and silencing, together with a better understanding of molecular mechanisms underlying plant-pathogen interactions are likely to increase the importance of susceptibility genes in future plant breeding.
Keywords: plant-pathogen interactions, plant immune system, disease resistance, loss of susceptibility, virulence targets