Transmission modes affect the population structure of potato virus Y in potato

Authors: DA SILVA, WASHINGTON - Cornell University; KUTNJAK, DENIS - National Institute Of Biology; XU, YI - Cornell University; XU, YIMIN - Boyce Thompson Institute; Giovannoni, James; SANTIAGO, ELENA - University Of Valencia; Gray, Stewart

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/6/2020
Publication Date: 6/23/2020
Citation: Da Silva, W., Kutnjak, D., Xu, Y., Xu, Y., Giovannoni, J.J., Santiago, E., Gray, S.M. 2020. Transmission modes affect the population structure of potato virus Y in potato. PLoS Pathogens. 16(6). https://doi.org/10.1371/journal.ppat.1008608.
DOI: https://doi.org/10.1371/journal.ppat.1008608

Interpretive Summary: Viruses can be transmitted between hosts via different modes, that can differently shape the population of transmitted viruses and thus have important implications for their biology and evolution. Potato virus Y, a damaging potato pathogen, can be transmitted between potato plants by aphid feeding, by wounding, or via tubers (mother to daughter plants). In this study, we have investigated how these three transmission modes directly affect the structure of the virus populations within the potato plants. We discovered that the mode of virus transmission significantly affected the population of the virus transmitted to the new plant. For example, virus populations transmitted by aphids were the least diverse while the ones transmitted vertically through tubers were the most diverse. To fully understand the effect of transmission modes on virus populations we needed to consider the events following the transmission, such as viral movement within a plant. Understanding the role that transmission modes play on the diversity and evolution of virus populations helps us to elucidate the mechanisms shaping the diversity of the virus in the field, and provides valuable information for future plant virus epidemiological studies that could promote the development of novel management strategies.

Technical Abstract: Transmission is a crucial part of a viral life cycle and transmission mode can have an important impact on virus biology. It was demonstrated that transmission mode can influence the virulence and evolution of a virus; however, few empirical data are available to describe the direct underlying changes in virus population structure dynamics within the host. Potato virus Y (PVY) is an RNA virus and one of the most damaging pathogens of potato. It comprises several genetically variable strains that are transmitted between plants via different transmission modes. To investigate how transmission modes affect the within-plant viral population structure, we have used a deep sequencing approach to examine the changes in the genetic structure of populations (in leaves and tubers) of three PVY strains after successive passages by horizontal (aphid and mechanical) and vertical (via tubers) transmission modes. Nucleotide diversities of viral populations were significantly influenced by transmission modes; lineages transmitted by aphids were the least diverse, whereas lineages transmitted by tubers were the most diverse. Differences in nucleotide diversities of viral populations between leaves and tubers were transmission mode-dependent, with higher diversities in tubers than in leaves for aphid and mechanically transmitted lineages. Furthermore, aphid and tuber transmissions were shown to impose stronger genetic bottlenecks than mechanical transmission. To better understand the structure of virus populations within the host, transmission mode, movement of the virus within the host, and the number of replication cycles after transmission event need to be considered. Collectively, our results suggest a significant impact of virus transmission modes on the within-plant diversity of virus populations and provide quantitative fundamental data for understanding how transmission can shape virus diversity in the natural ecosystems, where different transmission modes are expected to affect virus population structure and consequently its evolution.