Rice dwarf virus infection alters green rice leafhopper host preference and feeding behavior

Authors: WANG, QIANJIN - Zhejian University; LI, JINGJING - Zhejian University; DANG, CONG - Zhejian University; CHANG, XUEFEI - Zhejian University; FANG, QI - Zhejian University; Stanley, David; YE, GONG-YIN - Zhejian University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/20/2018
Publication Date: 9/7/2018
Citation: Wang, Q., Li, J., Dang, C., Chang, X., Fang, Q., Stanley, D.W., Ye, G. 2018. Rice dwarf virus infection alters green rice leafhopper host preference and feeding behavior. Frontiers in Plant Science. https://doi.org/10.1371/journal.pone.0203364.
DOI: https://doi.org/10.1371/journal.pone.0203364

Interpretive Summary: Successful insect pest management programs are essential to sustainable large-scale production of safe and affordable foods globally. A crucial problem in rice agroecosystems is insect transmission of plant pathogenic viruses. Rice is one of the three leading food crops in the world, providing about 21% of global human energy and about 15% of protein, on a per capita basis. Rice plant pathogens, such as rice dwarf virus (RDV), exert devastating damage to rice crops and they are major threat to sustainable agriculture. Research into mechanisms of insect transmission of plant pathogens is necessary to generate broad principles and models that can be applied to improve crop pest management. In this paper, we report that a rice plant pathogen, RDV, influences infected plants to change their volatile chemicals in a manner that makes them more attractive to insects that acquire the virus by feeding on them. The insects then transmit the viruses to other plants. This process increases the transmission and spread of the plant pathogenic viruses. This new information will be used by other scientists researching insect transmission of plant viruses. Ultimately, the information will lead to novel technologies to reduce this dangerous problem and benefit most consumers who rely on rice as their principle food source.

Technical Abstract: Host plants, pathogens and their herbivore vectors systems are characterized by complex interactions. Although there are substantial gaps in understanding these systems, the dynamics of the relationships may affect the process of virus transmission and plant disease epidemics. Rice dwarf virus (RDV; genus Phytoreovirus, Reoviridae) is a persistently transmitted circulative virus mainly vectored by green rice leafhoppers (GRLHs), Nephotettix cincticeps (Uhler) (Hemiptera: Cicadellidae). On the background idea that some disease organisms manipulate their vectors to expand their own biogeographic ranges, we considered the hypothesis that RDV infection manipulates the behaviors of its vector. Here, we analyzed the host plant selection preference of RDV-free or -infected GRLHs between RDV-free and -infected host plants. RDV-free GRLHs were attracted to RDV-infected rice plants, and viruliferous ones preferred RDV-free rice plants. Similarly, non-viruliferous GRLHs preferred the volitiles of RDV-infected rice plants over RDV-free plants, while viruliferous GRLHs preferred the volatiles of healthy plants over RDV-infected ones. Using an electrical penetration graph (EPG), we determined that RDV infection in the vector and in rice led to altered feeding behavior. During 6 h recording periods, non-viruliferous GRLHs spent shorter times in non-penetration, much longer times in xylem feeding on RDV-infected rice plants, compared to RDV-free rice plants. Viruliferous GRLHs exhibited more salivation and stylet movement on RDV-free rice plants than on RDV-infected plants. These findings strongly support our hypothesis that RDV manipulates its GRLH vector. This may confer adaptive advantages for RDV transmission.