Dynamics of responses in compatible potato-Potato virus Y interaction are modulated by salicylic acid

Abstract

To investigate the dynamics of the potato-Potato virus Y (PVY) compatible interaction in relation to salicylic acid-controlled pathways we performed experiments using non-transgenic potato cv. Désirée, transgenic NahG-Désirée, cv. Igor and PVY(NTN), the most aggressive strain of PVY. The importance of salicylic acid in viral multiplication and symptom development was confirmed by pronounced symptom development in NahG-Désirée, depleted in salicylic acid, and reversion of the effect after spraying with 2,6-dichloroisonicotinic acid (a salicylic acid-analogue). We have employed quantitative PCR for monitoring virus multiplication, as well as plant responses through expression of selected marker genes of photosynthetic activity, carbohydrate metabolism and the defence response. Viral multiplication was the slowest in inoculated potato of cv. Désirée, the only asymptomatic genotype in the study. The intensity of defence-related gene expression was much stronger in both sensitive genotypes (NahG-Désirée and cv. Igor) at the site of inoculation than in asymptomatic plants (cv. Désirée). Photosynthesis and carbohydrate metabolism gene expression differed between the symptomatic and asymptomatic phenotypes. The differential gene expression pattern of the two sensitive genotypes indicates that the outcome of the interaction does not rely simply on one regulatory component, but similar phenotypical features can result from distinct responses at the molecular level.

Figure 1. Symptom development following PVY inoculation in three potato genotypes.

Local symptoms on inoculated (I) at 7 dpi and systemic symptoms on upper non-inoculated leaves (U) at 10 and 11 dpi of cv. Désirée, NahG-Désirée and cv. Igor.

Figure 2. Accumulation of PVY RNA in leaves of potato plants.

(A) Relative PVY RNA concentration (average of 3 individual plants) in inoculated leaves 3–9 days post inoculation (dpi). Results of statistical evaluation of data are shown in Table 1 . (B) PVY RNA concentration (relative to the lowest detected viral amount) in non-inoculated leaves (3 plants per genotype, 2 leaves per plant: e.g. 1.2 denotes second leaf of plant 1) 7–11 dpi. (C) PVY RNA concentration in non-inoculated leaves of ten NahG-Désirée and eight cv. Igor plants at 16 dpi. PVY RNA concentrations are presented relative to the lowest detected viral amount in all plants. (D) Relative PVY RNA concentration (±SE, n = 4, normalised to COX gene expression) in the inoculated leaves 6 dpi (light grey) and in non-inoculated leaves 14 dpi (dark grey) of the NahG-Désirée plants following treatment with water (control), 0.3 mM or 1 mM INA.

Figure 3. Dynamics of selected host gene expression in inoculated potato leaves.

Expression of defence-related (A, C, E), photosynthesis and carbohydrate (CH) metabolism marker genes (B, D, F) in inoculated leaves of different potato genotypes (cv. Désirée, NahG-Désirée and cv. Igor) at 3, 4, 5, 7 and 9 days post infection (dpi). Relative viral RNA concentration (Pvy I) is plotted on each chart. PR-1b: pathogenesis-related protein 1b; Glu I, II, III: β-1,3-glucanase classes I, II, III; RA: RuBisCO activase; GBSSI: granule bound starch synthase I; CAB4: chlorophyll a–b binding protein 4. Data points represent the mean of three measurements. Statistical evaluation of data is shown separately in Table 1 .

Figure 4. Dynamics of selected host gene expression in upper non-inoculated potato leaves.

Expression of defence-related (A, C, E), photosynthesis and carbohydrate (CH) metabolism marker genes (B, D, F) in upper non-inoculated leaves of different potato genotypes (cv. Désirée, NahG-Désirée and cv. Igor) at 3, 4, 5, 7, 9, 10 and 11 days post infection (dpi). Relative viral RNA concentration (Pvy I) in the inoculated leaves is plotted on each chart. PR-1b: pathogenesis-related protein 1b; Glu I, II, III: β-1,3-glucanase classes I, II, III; RA: RuBisCO activase; GBSSI: granule bound starch synthase I; CAB4: chlorophyll a–b binding protein 4. Data points represent the mean of three measurements. Statistical evaluation of the data obtained is shown separately in Table 1 .