Metatranscriptomics and small RNA analysis revealed that viral covert coinfection resulted in disease symptoms reminiscent of rice sterility

Abstract BackgroundViral pathogens are a major threat to stable crop production. The discovery of viral diseases traditionally concerns apparent infection that shows obvious symptoms in crop plants. However, little is known about the covert infection of crop plants by viruses. In this study, we used deep metatranscriptomic sequencing and small RNA analysis to identify covert infection of rice plants by viruses.ResultsOur results showed that introgression of the dominant brown planthopper (BPH) resistance gene Bph3 into the high-yielding but BPH-susceptible indica variety Ms55 via a backcross strategy significantly enhanced resistance to BPH. However, Bph3-carrying backcross lines infested by BPH exhibited panicle enclosure and failed to produce seed at the mature stage, which are typical characteristics of sterile rice plants. Using a metatranscriptomic analysis, we identified six RNA viruses in backcross line Rby1 and eleven RNA viruses in backcross line Rby2, including eight novel viruses that fell within existing families and orders. Furthermore, our small RNA analysis revealed the biogenesis of viral small interfering RNAs that represented active virus infection in rice plants.ConclusionBph3-carrying backcross rice lines are resistant to BPH but are susceptible to viral infection. We identified viral covert coinfection in sterile rice plants by deep metatranscriptomic sequencing and small RNA analysis. Our results suggested that covert coinfection of rice plants by RNA viruses resulted in disease symptoms reminiscent of rice sterility. To develop rice varieties resistant to BPH, it is necessary to introgress genes resistant to not only BPH but also viral infection.