Lettuce mosaic virus: from pathogen diversity to host interactors

Abstract

Taxonomy: Lettuce mosaic virus (LMV) belongs to the genus Potyvirus (type species Potato virus Y) in the family Potyviridae.

Physical properties: The virion is filamentous, flexuous with a length of 750 nm and a width of 15 nm. The particles are made of a genomic RNA of 10 080 nucleotides, covalently linked to a viral-encoded protein (the VPg) at the 5' end and with a 3' poly A tail, and encapsidated in a single type of capsid protein. The molecular weight of the capsid protein subunit has been estimated electrophoretically to be 34 kDa and estimated from the amino acid sequence to be 31 kDa.

Genome organization: The genome is expressed as a polyprotein of 3255 amino-acid residues, processed by three virus-specific proteinases into ten mature proteins.

Hosts: LMV has a worldwide distribution and a relatively broad host range among several families. Weeds and ornamentals can act as local reservoirs for lettuce crops. In particular, many species within the family Asteraceae are susceptible to LMV, including cultivated and ornamental species such as common (Lactuca sativa), prickly (L. serriola) or wild (L. virosa) lettuce, endive/escarole (Cichorium endiva), safflower (Carthamus tinctorius), starthistle (Centaurea solstitialis), Cape daisy (Osteospermum spp.) and gazania (Gazania rigens). In addition, several species within the families Brassicaceae, Cucurbitaceae, Fabaceae, Solanaceae and Chenopodiaceae are natural or experimental hosts of LMV. Genetic control of resistance to LMV: The only resistance genes currently used to protect lettuce crops worldwide are the recessive genes mo1(1) and mo1(2) corresponding to mutant alleles of the gene encoding the translation initiation factor eIF4E in lettuce. It is believed that at least one intact copy of eIF4E must be present to ensure virus accumulation.

Transmission: LMV is transmitted in a non-persistent manner by a high number of aphid species. Myzus persicae and Macrosiphum euphorbiae are particularly active in disseminating this virus in the fields. LMV is also seedborne in lettuce. The effectiveness of LMV transmission depends on the cultivar and the age of the seed carrier at the inoculation time.

Symptoms: The characteristic symptoms on susceptible lettuce cultivars are dwarfism, mosaic, distortion and yellowing of the leaves with sometimes a much reduced heart of lettuce (failure to form heads). The differences in virus strains, cultivars and the physiological stage of the host at the moment of the attack cause different symptom severity: from a very slight discoloration of the veins to severe necrosis leading to the death of the plant.

Figure 1

LMV particles and symptoms induced by LMV isolates on lettuce susceptible cultivar Trocadéro. (A) Electron micrograph of LMV virions (the bar represents 200 nm). (B–D) Severe symptoms induced by the LMV‐E isolate including dwarfing and necrosis (close‐up in C). (E) Mosaic symptoms induced by LMV‐AF199. (F) Leaf infected with LMV‐0 showing mosaic symptoms.

Figure 2

Dendrogram showing the relationships between LMV isolates. The dendrogram shows the levels of sequence divergence between LMV isolates using nucleotide sequences. It is derived from the Saitou & Nei distances calculated in an alignment of the variable nucleotide sequence of the NIB–CP junction (between nucleotide positions 8936 and 9151 of the LMV‐E genome). The bar represents 0.05 substitutions per site (sps). The upper line corresponds to the single isolate from Yemen. Remarkable clusters of isolates are represented by triangles. The cluster named Gr corresponds to the group of isolates from the Balkans. The cluster named RoW (Rest of the World) includes most of the LMV isolates, representing isolates from lettuce of various geographical origins (Europe, South America, North Africa, Middle East, China). Within this cluster, the Most and Common clusters have been named after Krause‐Sakate et al. (2002). The positions of the sequenced isolates LMV‐E, LMV‐0, LMV‐AF199 and LMV‐Yuhang are indicated by small spheres.

Figure 3

LMV‐GFP invasion in susceptible and resistant lettuce. (A–F) LMV‐GFP invasion in the susceptible lettuce cultivar Trocadéro. (A,B) Symptoms of vein clearing on the leaves located above the inoculated leaves at 10 dpi (days post inoculation). (C) Symptoms of mosaic on the upper non‐inoculated leaves at 20 dpi (photos taken under daylight). (D) GFP‐derived green fluorescence in the inoculated leaves showing infection foci at 7 dpi. (E) Vein clearing on the leaves located above the inoculated leaves at 10 dpi. (F) Mosaic on the upper non‐inoculated leaves at 20 dpi. (G) GFP‐derived green fluorescence in Salinas (susceptible cultivar) upper non‐inoculated leaves infected with LMV‐0‐GFP at 20 dpi. (H) Very sporadic GFP‐derived green fluorescence in Salinas 88 (resistant mo1 ²) upper non‐inoculated leaves infected with LMV‐0‐GFP at 20 dpi. Detection of LMV‐0‐GFP in the roots of both Salinas (I) and Salinas 88 (J) cultivars at 20 dpi.

Figure 4

LMV‐GUS invasion in susceptible and resistant lettuce. Infection foci at 4 dpi (A) and 8 dpi (B) are present in inoculated leaves of both quasi‐isogenic lettuce cultivars: Salinas (left) and Salinas 88 (S88, right). The cell‐to‐cell movement of LMV‐0 is delayed in Salinas 88 compared with Salinas but is not abolished. (C) At 20 dpi, the LMV‐0‐GUS systemic movement in the upper non‐inoculated systemic leaves is detected in the Salinas cultivar, but not in Salinas 88. (D) At the same point‐time (20 dpi), LMV‐0‐GUS can be detected in the roots of both cultivars, although at a reduced rate in Salinas 88.