Viruses as Manipulative Agents of Host Plants and Vectors

Pathogens, including some plant viruses have the potential to induce changes in host or vector biology that enhance their fitness. Evidence continues to accumulate indicating that plant viruses may act as manipulative agents of their host plants and vectors. Plant virus infection can alter the suitability of host plants for their arthropod vectors. For example, most reports indicate that virus-infected plants are superior hosts for arthropod vectors compared to noninfected plants with respect to vector growth rates, fecundity, longevity and/or enhanced production of winged forms of the vector. Some arthropod vectors preferentially respond to virus-infected plants compared to noninfected ones. Thus, it appears arthropod vectors can exploit changes in host plant quality associated with viral infection. Enhanced vector performance and preference for virus-infected plants might be advantageous for viruses by promoting their spread and possibly enhancing their fitness. We have proposed the Vector Manipulation Hypothesis to explain the emergence of strategies in plant pathogens that enhance their spread to new hosts via their vectors. Our research has focused on one of the most important viruses that infect wheat, a major food staple around the world. Through studies utilizing the model system of Barley yellow dwarf virus and its vector, the bird-cherry oat aphid, we have demonstrated that virus infection alters the concentration and relative composition of volatile organic compounds in wheat plants. Such virus-infection-mediated alterations of the host plant can affect vector behavior. In this pathosystem, noninfective vectors are attracted to virus-infected host plants, while infective vectors prefer non-infected plants. Such a shift in preference from infected to noninfected plants following acquisition of the virus could accelerate the rate of virus spread under field conditions. Further, our research has provided evidence that a plant virus can directly manipulate its vector in a manner that is likely to maximize virus transmission potential between plant hosts. Recent work by other researchers with Cucumber mosaic virus (CMV) demonstrated that arthropod vectors are initially attracted to virus-infected squash plants but subsequently prefer to colonize noninfected plants. Since the virus can be acquired rapidly by an aphid probing on an infected plant these behaviors can enhance virus spread, further illustrating manipulation of an arthropod vector by a plant virus. In addition to manipulating vectors, CMV also may manipulate plant defenses with the potential for enhancing vector survival. Greater understanding of such host plant-virus-vector interactions has the potential to improve management of vectors and plant diseases in agricultural settings and enhance our understanding of the role plant viruses play in natural settings, including their effects on ecological processes. Recent research findings will be presented and their significance discussed.