A non-persistent aphid-transmitted Potyvirus differentially alters the vector and non-vector biology through host plant quality manipulation

Abstract

The association of plant viruses with their vectors has significant implications for virus transmission and spread. Only a few studies, with even fewer pathosystems, have explored non-persistent (NP) virus-vector interactions that are presumed to be transient. We studied how a NP virus, Papaya ringspot virus (PRSV) influenced the behavior and biology of its vector, the melon aphid (Aphis gossypii Glover) and the non-vector, silverleaf whitefly (Bemisia tabaci Gennadius). We also assessed whether the fitness effects on aphids are modulated through changes in the host plant, squash (Cucurbita pepo L.) nutrient profile. The overall performance of A. gossypii was substantially higher on PRSV-infected plants, along with increased arrestment on PRSV-infected than non-infected plants. No such PRSV-modulated fitness effects were observed with B. tabaci. PRSV-infected plants had increased concentrations of free essential amino acids: threonine, arginine and lysine; non-essential amino acids: glycine and homocysteine; and soluble carbohydrates: galactose, raffinose and cellobiose. In general, PRSV encouraged long-term feeding and enhanced fitness of A. gossypii through host plant nutrient enrichment. These findings provide evidence for a NP virus mediated positive fitness effects on its vector, with no spillover fitness benefits to the non-vector within the same feeding guild.

Figure 1

Number of emigrating and immigrating aphids on PRSV-infected and non-infected plants at 10 min time intervals (Mean ± SEM, n = 10).

Figure 2

Life history traits of A. gossypii on PRSV-infected and non-infected plants. NP = Nymphal period, RP = reproductive period, PRP = Pre-reproductive period, AP = adult period. The time period values are represented in median (n = 20). Asterisks indicate significant effects (*P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, by Mann-Whitney U Test/ANOVA).

Figure 3

Soluble carbohydrate analysis of PRSV-infected and non-infected plants (Mean ± SEM, n = 5). Asterisks indicate significant effects (*P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, by Mann-Whitney U Test).

Figure 4

Free amino acid analysis of PRSV-infected and non-infected plants (Mean ± SEM, n = 5). Asterisks indicate significant effects (*P ≤ 0.05, **P ≤ 0.01, ***P ≤ 0.001, by Mann-Whitney U Test).

Figure 5

Overall nutrient status of PRSV-infected and non-infected plants (Mean ± SEM).