Exploring the potential beneficial effects of persistent virus infection in plants

Key Message Recent exciting results suggest that certain plant viruses transmitted exclusively through seeds and pollen, but which cause no obvious disease ‘pay back’ their hosts by, among other things, improving growth or protection from insect pests. We will test the limits of this hypothesis by determining the extent to which these 'persistent' viruses benefit plants of three species. Context With respect to their effects on hosts, viruses are more ambiguous than generally considered. For example, several erstwhile disease-causing (pathogenic) viruses benefit plants under specific circumstances; for example, by increasing host resistance to drought, cold temperatures or heavy metal toxicity. Remarkably, certain viruses inferred to have descended from ancestors that caused disease in plants or that were pathogenic to plant-associated fungi, appear to have followed an evolutionary road towards becoming benign plant symbionts. Challenge Among viruses that appear to have evolved furthest away from pathogenicity the best studied are ‘partitiviruses’ and ‘endornaviruses’. In recent literature these RNA viruses are often referred to as persistent since they are inherited via seed and pollen and so persist between generations. Persistent viruses are not infectious in a conventional sense, i.e., they are not transmitted by invertebrate vectors or wounding, as are most plant viruses. Persistent viruses are common in wild plants and occur in certain lines of major crops, but infected plants show no symptoms typical of viral disease e.g., developmental abnormalities or mosaics (discolouration patterns). Importantly, both partitiviruses and endornaviruses are reported to have beneficial effects, leading to the hypothesis that these viruses are mutualists rather than pathogens. However, that work used non-identical host backgrounds in a limited range of bean and pepper varieties, making it impossible to distinguish definitively between viral and host influences. Aims and objectives We produced genetically identical (‘isogenic’) lines of pepper (Capsicum) plants that are infected or cured of specific persistent viruses. We found that partitiviruses and endornaviruses can exert significant effects on seed size and mass and plant growth, but that these effects are not identical in all host backgrounds. The results are important because they point to persistent viruses influencing competitiveness in wild plants and to potential effects on crop yield and vigour. We will investigate how persistent viruses exert their effects, and how conserved these effects are in different plants through three objective-based work-packages. Further characterise persistent viruses’ effects in pepper In the important legume crop, common bean, develop isogenic persistent virus-infected/non-infected lines to characterise the effect(s) of persistent viruses on yield and resilience Introduce a persistent virus into a model plant background Potential applications and benefits Persistent viruses occur in lines of many crops including cereals and legumes. If persistent viruses improve plant productivity and/or resilience, even conventional crossing will provide breeders with a simple, environmentally friendly crop enhancement approach. In contrast, if they are problematic in some crops or genotypes, they can be screened for to avoid incorporation into new lines. The work addresses BBSRC’s strategic objectives of World-Class Ideas by improving understanding of fundamental ‘rules of life’ governing symbiosis in virus-host interactions, World-Class Innovation via fundamental research with potential to underpin future commercial applications leading to World-Class Impact through sustainable bio-based solutions to enhance crop characteristics and food security. Work addresses recent Spotlight areas: ‘Plant Health’, ‘Novel crop protection strategies’, ‘Better understanding of… symbionts in resilient crops’.