Submitted to: Journal of Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/29/2006
Publication Date: 4/19/2007
Citation: Gray, S.M., Caillaud, M., Burrows, M.E., Smith, D. 2007. Transmission of viruses that cause barley yellow dwarf is controlled by different loci in the aphid, schizaphis graminum. Journal of Insect Science. 24:53-78. Interpretive Summary: The Barley yellow dwarf viruses are the most economically important group of plant viruses affecting many of the world’s staple cereal crops. Natural host plant resistance or engineered resistance is limited and other control measures, such as chemical control of vectors or adjusting planting times to avoid peak aphid vector flights, are generally ineffective or economically prohibitive. Another type of control strategy, and the underlying goal of this research, is to disrupt the ability of the virus to be transmitted by its vector. If viruses are inefficiently transmitted between hosts, then disease epidemics are unlikely to develop or at least will develop more slowly and be less damaging. This research examines the genetics of plant virus vectors relative to their ability to transmit viruses. We identified vector and nonvector populations of a single species of aphid and used them to make a genetic cross to examine the inheritance of the trait of virus transmission. Transmission was controlled by multiple genes and was inherited in a dominant manner. Furthermore, there are unique genes in the aphid that regulate the transmission of each virus that causes Barley yellow dwarf disease. The segregating population of aphids provides a tool to identify aphid genes responsible for virus transmission and a means to differential vector and nonvector populations. This knowledge could eliminate unnecessary efforts to control insects, often by pesticide applications that are not a threat as disease vectors. The mechanisms of transmission of luteoviruses have many similarities to the transmission mechanisms of numerous other arthropod-borne plant and animal viruses. The fundamental knowledge gained from this system and the techniques developed to study these interactions are likely to be applicable to other systems allowing a more rapid advancement in the development of strategies to control other arthropod-borne viruses.
Technical Abstract: Clonal populations of the aphid, Schizaphis graminum, have been separated into biotypes bases on host preference and their ability to overcome resistance genes in wheat. Recently, the biotypes were found to differ in their ability to transmit one or more of the viruses that cause barley yellow dwarf disease in grain crops and vector competence was linked to host preference. The genetics of host preference has been studied in S. graminum, but the genetics of vector competency of plant virus transmission are unknown. Sexual morphs of a vector and nonvector S. graminum genotype were induced from parthenogenetic females and reciprocal crosses made. Eighty-nine hybrids were generated and maintained by parthenogenetic reproduction. Each hybrid was evaluated for its ability to colonize wheat expressing two different resistance genes to S. graminum and for its ability to transmit Barley yellow dwarf virus-PAV (BYDV-PAV) and Cereal yellow dwarf virus-RPV (CYDV-RPV). The F1 hybrids were genetically variable for their ability to colonize the aphid resistant wheat, but this phenotype was not correlated with vector competence which also segregated in the F1 generation. Individual hybrids ranged in transmission efficiency from 0-100% for both viruses; however there was directional dominance for transmission of CYDV-RPV and BYDV-PAV. The F1 hybrids had an overall mean transmission efficiency similar to the transmission competent parent. The direction of the cross did not affect the vector competency for either virus indicating that maternally inherited cytoplasmic factors or bacterial endosymbionts did not contribute significantly to the inheritance of vector competency in S. graminum. Importantly, there was no genetic correlation between the ability to transmit BYDV-PAV and CYDV-RPV in the F1 hybrids. These results taken together indicate that multiple loci are involved in the circulative transmission, but the successful transmission of these closely related viruses is regulated an overlapping but not identical set of aphid genes.