Potato leafroll virus reduces Buchnera aphidocola titer and alters vector transcriptome responses.

Viruses in the Luteoviridae family, such as Potato leafroll virus (PLRV), are transmitted by aphids in a circulative and nonpropagative mode. This means the virions enter the aphid body through the gut when they feed from infected plants and then the virions circulate through the hemolymph to enter the salivary glands before being released into the saliva. Although these viruses do not replicate in their insect vectors, previous studies have demonstrated viruliferous aphid behavior is altered and the obligate symbiont of aphids, Buchnera aphidocola, may be involved in transmission. Here we provide the transcriptome of green peach aphids (Myzus persicae) carrying PLRV and virus-free control aphids using Illumina sequencing. Over 150 million paired-end reads were obtained through Illumina sequencing, with an average of 19 million reads per library. The comparative analysis identified 134 differentially expressed genes (DEGs) between the M. persicae transcriptomes, including 64 and 70 genes that were up- and down-regulated in aphids carrying PLRV, respectively. Using functional classification in the GO databases, 80 of the DEGs were assigned to 391 functional subcategories at category level 2. The most highly up-regulated genes in aphids carrying PLRV were cytochrome p450s, genes related to cuticle production, and genes related to development, while genes related to heat shock proteins, histones, and histone modification were the most down-regulated. PLRV aphids had reduced Buchnera titer and lower abundance of several Buchnera transcripts related to stress responses and metabolism. These results suggest carrying PLRV may reduce both aphid and Buchnera genes in response to stress. This work provides valuable basis for further investigation into the complicated mechanisms of circulative and nonpropagative transmission.

A polerovirus, Potato leafroll virus, alters plant-vector interactions using three viral proteins.

Potato leafroll virus (PLRV), genus Polerovirus, family Luteoviridae, is a major pathogen of potato worldwide. PLRV is transmitted among host plants by aphids in a circulative-nonpropagative manner. Previous studies have demonstrated that PLRV infection increases aphid fecundity on, and attraction to, infected plants as compared to controls. However, the molecular mechanisms mediating this relationship are still poorly understood. In this study, we measured the impact of PLRV infection on plant-aphid interactions and plant chemistry in two hosts: Solanum tuberosum and Nicotiana benthamiana. Our study demonstrates that PLRV infection attenuates the induction of aphid-induced jasmonic acid and ethylene in S. tuberosum and N. benthamiana. Using transient expression experiments, insect bioassays and chemical analysis, we show that expression of three PLRV proteins (P0, P1, and P7) mediate changes in plant-aphid interactions and inhibition of aphid-induced jasmonic acid and ethylene in N. benthamiana. This study enhances our understanding of the plant-vector-pathogen interface by elucidating new mechanisms by which plant viruses transmitted in a circulative manner can manipulate plant hosts.

Ethylene signaling mediates potyvirus spread by aphid vectors.

Plant pathogens can influence host characteristics such as volatile emissions, nutrient composition or plant color, modulating vector and non-vector insect dynamics in the ecosystem. While previous research has focused on insect attraction and dispersal to infected plants, little is known about mechanisms mediating these interactions. Here, we investigate the role of ethylene in green peach aphid (Myzus persicae) attraction to potyvirus-infected plants. In our experiments, we utilized two different potyviruses, Potato virus Y (PVY) and Turnip mosaic virus, in lab and field experiments. Consistent with previous studies, we show that greater numbers of aphids settle on potyvirus-infected plants in the lab and greater numbers of aphids are found in PVY-infected potato (Solanum tuberosum) fields compared to controls. In laboratory experiments, inhibition of ethylene signaling in plants either chemically or genetically prevented aphids from preferentially settling on potyvirus-infected plants. Virus spread was reduced in lab arenas by over 80% when ethylene signaling was inhibited chemically. Despite this, ethylene inhibition had no significant impact on virus spread in field mesocosms. Our results indicate that induction of ethylene signaling by potyviruses mediates aphid attraction to infected plants and virus spread; however, additional factors may contribute to plant-vector dynamics in complex communities. Specific components of ethylene signaling may be important targets for future management of vector-borne viruses and research on mechanisms mediating plant-vector-virus interactions.