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

Kiran R Gadhave,Rajagopalbabu Srinivasan,Bhabesh Dutta,Timothy Coolong

doi:10.1038/s41598-019-39256-5

Kiran R Gadhave, Rajagopalbabu Srinivasan + Show 2 more

Open Access

https://doi.org/10.1038/s41598-019-39256-5

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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.

Highlights

A majority of plant viruses rely on insect vectors for plant-to-plant dispersal
We examined the effects of Papaya ringspot virus (PRSV) infection in squash on the preference and biology of its vector; A. gossypii and a ubiquitous non-vector; B. tabaci
Our study demonstrated that PRSV selectively favors A. gossypii, but not B. tabaci fitness through host plant quality manipulation

Summary

Introduction

A majority of plant viruses rely on insect vectors for plant-to-plant dispersal. Plant viruses transmitted in a persistent manner are known to be strongly associated with insect vectors. The speculation is that the long-term settling and subsequent development of alatae would foster the establishment of large number of inoculum foci over greater distances than the rapid and fewer inoculum foci due to quick vector dispersal[6] Most of these virus driven plant and vector manipulations are likely mediated through biochemical determinants such as free amino acids, soluble carbohydrates, and defense signaling compounds[5,6,7]. Apart from examining PRSV transmission efficiency of A. gossypii, Aphis craccivora (Koch), and Myzus persicae (Sulzer)[32], vector-virus interactions in a cucurbit-PRSV- aphid pathosystem remain unexplored It is not clear whether the virus-mediated effects on vectors are specific or if they would impact non-vectors that belong to the same feeding guild as the vector and are simultaneously exposed to virus-mediated changes in the host plant. To explore such indirect effects, we examined the effects of PRSV-infection on silverleaf whitefly, Bemisia tabaci (Gennadius), a ubiquitous non-vector species sharing the same phloem feeding guild along with the vector in the current study system

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