Molecular aspects of potato virus Y transmission by aphids (Myzus persicae)

Potato virus Y (PVY), is a plant virus causing important damage in a number of important crops, particularly in potato. Several PVY strains have been differentiated, all of them causing different symptoms and disease levels on numerous commercial potato cultivars. In Belgium, strains belonging to the N group had been reported as the most prevalent, but no detailed information on the relative importance of the PVY strains in Belgium was published.
PVY is transmitted in a non-persistent manner by many aphid species and the green peach aphid (Myzus persicae) is the most efficient known vector. Aphid species, host plants and environmental conditions are the main factors that influence transmission efficiency. In addition to these main factors, the host plants that are used to rear the aphids prior to the virus acquisition, can affect the PVY transmission efficiency and this aspect has been paid less attention. Furthermore, the quantification of potyviruses in individual vectors has mainly focused on the whole aphid body and not the stylet alone, whereas an even more precise indicator that could correlate with vector efficiency in non-persistently transmitted viruses is the quantity of the virus in the stylet.
Variation in virus transmission by aphid species is another essential question that needs to be better understood. The important role of the distal part of the aphid’s stylet in PVY transmission is known, but the molecular aspects still need to be further elucidated. PVY transmission relays on receptors and aphid-virus protein interaction and understanding the molecular components that are involved, would provide useful opportunities for virus management. PVY receptors have been localized in the tip of the stylet, however, the nature of the receptors is in obscurity. Cuticle proteins (CuP), being the most likely receptors in non/semi-persistent virus transmission, including PVY transmission, need to be characterized much better. Based on the above-mentioned gaps, this project aimed to provide and elucidate the relative importance of the PVY strains in Belgium, the correlation between host plants in aphid rearing before PVY acquisition, as well as the transmission efficiency, and finally, the relevance of the PVY concentration in the stylet of aphid vectors related to the transmission efficiency. We also evaluated the impact of five CuPs on the transmission of PVY by M. persicae using an RNA interference (RNAi) gene-silencing assay.
The PVY survey in Belgian seed potatoes was performed in 2700 individual tubers from 54 seed potato lots originating from 54 production units in 2010. The results revealed a high PVY incidence and substantial strain diversity in some farms. The dominance of the N group in Belgian seed potatoes was confirmed, while the O strain was only found in a few locations. Further characterization using a multiplex PCR identified 75% of the isolates as belonging to the NTN strain group and surprisingly, 7.5% as the mild Wilga strain (N-Wi). The presence of the N-Wi strain was confirmed and further characterized for the first time in Belgian seed potato production.
When evaluating the correlation between the host and PVY quantity, the study revealed that M. persicae, when reared on broad bean and then exposed to acquire PVY, transmitted PVY less efficiently (50%), compared to when the aphid was reared on Brussels sprout (81%). Additionally, the transmission percentage was directly correlated with the virus concentration in the stylet (r = 0.7), yet not with the concentration in the intact whole aphid body (r = 0.06). Hence, the virus quantity in the stylet could be exploited as a useful index for virus transmission efficiency in epidemiological studies or predictive schemes.
Using an oral RNAi bioassay where the aphids pierce-suck in an artificial diet that was supplemented with gene-specific dsRNA, the expression of two CuPs, mpcp2 (DQ108935) and mpcp1 (AF435075.1), could be decreased by 63% and 75%, respectively. Expression of three other CuPs was not affected. Subsequently, we investigated what the effect is of the RNAi-mediated gene silencing on the transmission of PVY from potato to tobacco plants. These results showed with a high certainty of 99.5%, for the first time in vivo, a significant involvement of MPCP2 with a reduction of 47% (compared to the dsGFP-control) in the transmission of PVY. For MPCP1, the effect was smaller with a reduction of 19% and lower certainty of 86%. These findings as useful information and can be used in PVY epidemiology and management.