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Plant Viruses Transmitted in Two Different Modes Produce Differing Effects on Small RNA-Mediated Processes in Their Aphid Vector

Transmission of plant viruses by aphids involves multitrophic 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)

Patricia V. Pinheiro, Jennifer R. Wilson, Yi Xu, Yi Zheng, Ana Rita Rebelo, Somayeh Fattah-Hosseini, Angela Kruse, Rogerio Santos Dos Silva, Yimin Xu, Matthew Kramer, James Giovannoni, Zhangjun Fei, Stewart Gray, and Michelle Heck

APS Publications; Published Online: 20 Mar 2019  https://doi.org/10.1094/PBIOMES-10-18-0045-R

Abstract

Transmission of plant viruses by aphids involves multitrophic 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 22 mers aligned to the aphid genome, and an abundance of 26 to 27 mers, 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 22 mers 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.

 

See: https://apsjournals.apsnet.org/doi/full/10.1094/PBIOMES-10-18-0045-R

Figure 2: Small RNA (sRNA) mapping to the most abundant Buchnera aphidicola aminoacyl-tRNAs in aphid samples. Myzus persicae aphids (∼700 aphids/replicate, three to four replicates/treatment) were given a 72 h acquisition access period on Potato leafroll virus(PLRV)-infected plants, purified PLRV in 30% sucrose, Potato virus Y (PVY)-infected potato plants, 30% sucrose, or mock-inoculated potato plants, followed by 72 h gut clearing on turnip plants for all treatments. Aphid sRNA was extracted, sequenced, and analyzed as described in the methods. Values presented as percent of the total Buchnera-derived sRNA generated in aphids, averaged across biological replicates. Shown are the abundance of sRNA reads mapping to the aminoacyl-tRNAs A, asparagine, B, tyrosine, C, threonine, D,methionine, E, serine, F, leucine, and G, glutamine, in descending order of abundance. Error bars represent ± one standard error. Letters represent significantly different treatments (P < 0.05).

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