Plant viruses transmitted in two different modes produce differing effects on small rna-mediated processes in their aphid vector

Authors: PINHEIRO, PATRICIA - Brazilian Agricultural Research Corporation (EMBRAPA); WILSON, JENNIFER - Cornell University; XU, YI - Cornell University; ZHENG, YI - Boyce Thompson Institute; REBELO, ANA RITA - Boyce Thompson Institute; FATTAH-HOUSEINI, SOMAYEH - Boyce Thompson Institute; KRUSE, ANGELA - Cornell University; SANTOS DOS SILVA, ROGERIO - Boyce Thompson Institute; XU, YIMIN - Boyce Thompson Institute; Kramer, Matthew; Giovannoni, James; FEI, ZHANGJUN - Boyce Thompson Institute; Gray, Stewart; Heck, Michelle

Submitted to: Phytobiomes Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/27/2018
Publication Date: 3/20/2019
Citation: Pinheiro, P.V., Wilson, J.R., Xu, Y., Zheng, Y., Rebelo, A., Fattah-Houseini, S., Kruse, A., Santos Dos Silva, R., Xu, Y., Kramer, M.H., Giovannoni, J.J., Fei, Z., Gray, S.M., Heck, M.L. 2019. Plant viruses transmitted in two different modes produce differing effects on small rna-mediated processes in their aphid vector. Phytobiomes Journal. 3(1):71-81. https://doi.org/10.1094/PBIOMES-10-18-0045-R.
DOI: https://doi.org/10.1094/PBIOMES-10-18-0045-R

Interpretive Summary: Many plant viruses are spread in a crop by insects. Plant viruses are known to manipulate insects to promote their own spread between plants. This study shows that potato leafroll virus, a plant virus that is spread by tiny plant feeding insects called aphids, suppresses the immune system of the aphid. The weakened aphid immune system makes the aphid more susceptible to an aphid-infecting virus, called a densovirus. The effect on the aphid immune system is mediated by a single potato leafroll virus protein called P0. In plants, P0 is known to suppress the plant immune system but a function for P0 in suppressing the aphid immune system was not known before. In other aphids, densoviruses induce the formation of winged forms of the insect, which would enable the aphid to move long distances. In this study, aphids with wings also had higher levels of the densovirus. Thus, the results lead to a new hypothesis on how potato leafroll virus manipulates aphids for spreading within a crop: the increase in densovirus in aphids caused by the suppression of the aphid’s immune system by potato leafroll virus may serve to enhance the spread of both viruses. Potato leafroll virus also caused other changes in aphids at the molecular level, including the regulation of gene expression and interactions with the beneficial bacterial partner in aphids, suggesting that potato leafroll virus can no longer be considered a silent hitchhiker in its aphid vector, but must now be considered a noisy back seat driver.

Technical Abstract: Transmission of plant viruses by aphids involves multi-trophic interactions among host plants, aphid vectors, and plant viruses. Here, we used small RNA (sRNA) sequencing to visualize the sRNA response of Myzus persicae to two plant viruses that M. persicae transmits in different modes: the nonpersistent Potato virus Y (PVY) versus the persistent Potato leafroll virus (PLRV). Aphids exposed to PLRV produced significantly less 22mers aligned to the aphid genome, and an abundance of 26-27mers, many of which were predicted to be piRNA. Additionally, expression of Buchnera aphidicola tRNA-derived sRNAs was influenced by PLRV and, to a lesser extent, PVY, suggesting that plant viruses alter the aphid-endosymbiont relationship. Finally, aphids exposed to PLRV-infected plants generated an abundance of unusually long sRNAs and a reduced number of 22mers against an aphid virus, Myzus persicae densovirus (MpDNV) and had higher MpDNV titer. Expression of the PLRV silencing suppressor P0 in plants recapitulated the increase in MpDNV titer in the absence of PLRV infection. Our results show that plant viruses transmitted in two different modes cause distinct effects on their vector with regards to post-transcriptional gene regulation, symbiosis with Buchnera, and the antiviral immune response of aphids to an aphid-infecting densovirus.