Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity

Abstract

Taxonomy: Potato virus Y (PVY) is the type member of the genus Potyvirus in the family Potyviridae. VIRION AND GENOME PROPERTIES: PVY virions have a filamentous, flexuous form, with a length of 730 nm and a diameter of 12 nm. The genomic RNA is single stranded, messenger sense, with a length of 9.7 kb, covalently linked to a viral-encoded protein (VPg) at the 5' end and to a 3' polyadenylated tail. The genome is expressed as a polyprotein of approximately 3062 amino acid residues, processed by three virus-specific proteases into 11 mature proteins.

Hosts: PVY is distributed worldwide and has a broad host range, consisting of cultivated solanaceous species and many solanaceous and nonsolanaceous weeds. It is one of the most economically important plant pathogens and causes severe diseases in cultivated hosts, such as potato, tobacco, tomato and pepper, as well as in ornamental plants.

Transmission: PVY is transmitted from plant to plant by more than 40 aphid species in a nonpersistent manner and, in potato, by planting contaminated seed tubers. DIVERSITY: Five major clades, named C1, C2, Chile, N and O, have been described within the PVY species. In recent decades, a strong increase in prevalence of N × O recombinant isolates has been observed worldwide. A correlation has been observed between PVY phylogeny and certain pathogenicity traits. GENETIC CONTROL OF PVY: Resistance genes against PVY have been used widely in breeding programmes and deployed in the field. These resistance genes show a large diversity of spectrum of action, durability and genetic determinism. Notably, recessive and dominant major resistance genes show highly contrasting patterns of interaction with PVY populations, displaying rapid co-evolution or stable relationships, respectively.

Figure 1

Symptoms induced by Potato virus Y (PVY). (a) Vein necrosis in potato leaf (courtesy of Nikon Vassilakos). (b) Necrotic rings on potato tubers (courtesy of the Laboratory of Virology, Benaki Phytopathological Institute). (c) Leaf mosaic on pepper [courtesy of Alain Palloix, INRA, Provence Alpes Côte d'Azur, Génétique et Amélioration des Fruits et Légumes (GAFL)]. (d) Electron micrograph of PVY virions [courtesy of Isabelle Bornard, INRA, Provence Alpes Côte d'Azur (PACA), Pathologie Végétale]. The scale bar corresponds to 200 nm.

Figure 2

Determinants of pathogenicity mapped in the Potato virus Y (PVY) genome and recombination pattern of PVY^NTN and PVY^N‐W isolates. (a) PVY factors and/or mutations involved in resistance breakdown are indicated below the genome scheme. The dominant genes are specified with a capital letter and the host is indicated n parentheses. Above the genome scheme, PVY determinants of virulence or aphid transmission are noted. (b) Schematic representation of the different recombination patterns between PVY^O (light grey) and PVY^N (dark grey) clades (modified from Hu et al., 2009). *The tobacco Rk gene confers a nematode resistance and it (or a very tightly linked gene) induces leaf necrosis on PVY inoculation.

Figure 3

Simplified Potato virus Y (PVY) phylogeny (excluding the recombinant isolates) and infectivity of PVY isolates from the five major clades in crop plants of the family Solanaceae.