S genes for disease resistance in wheat using Arabidopsis as a model

In their millennia-long coexistence, plants and pathogens have coevolved diverse arrays of biochemicals against each other to survive. The arms race between them is a complex process and involves multiple defence and signalling pathways. Pathogens with superior virulence arms often cause substantial yield loss and compromise quality in numerous plant species. In response, plants are equipped with resistance genes ( R genes) to overcome pathogen-associated losses. However, the use of R genes in breeding is often hindered by their short durability and limited specificity against a pathogen race. Besides using their resources for pathogenicity, pathogens usually ‘trick’ the host defence system and involve the host genes in favour of their entry and colonisation of the host, so-called susceptibility genes ( S genes). In contrast to R genes, S genes serve as host factors to establish host-pathogen compatibility by facilitating nutrient acquisition, suppressing defence signalling, or modifying host cellular structures. Unlike the recognition-based mechanism of R genes, resistance derived from S genes typically results from a loss-of-function of these required targets. In the last two decades, S genes have been used to improve resistance against various pathogens. However, the use of mutant S genes to develop resistant crops is often hampered by their potential pleiotropic effects. To overcome these challenges, New Genomic Techniques (NGTs) provide tools and platforms to fine-tune target S gene expression without pleiotropic effects. NGTs also enable simultaneous targeting of multiple S genes to achieve broad-spectrum resistance. Compared to classical breeding, NGTs significantly shorten the breeding cycles and facilitate the rapid integration of resistance traits into elite cultivars. Here, we summarise the functional diversity of S genes in the model plant Arabidopsis and the cereal crop wheat against various plant pathogens. In addition, we also highlight the potential challenges to translate S gene functional studies from Arabidopsis to polyploid crop species, like wheat. Furthermore, we discuss potential targets in the S genes for NGTs-mediated modification and the generation of resilient crops against various pathogens. • S genes play central roles in diverse physiological processes underlying plant growth and development. • S genes are required for host-pathogen compatibility and facilitate successful colonization of the host by pathogens. • S gene-mediated resistance is more durable than R gene-based resistance but is often impeded by pleiotropic effects. • Translational insights from the Arabidopsis model accelerate precision breeding approaches in polyploid wheat. • New genomic techniques offer opportunities to reduce S gene pleiotropy and improve their application in resistance breeding