Tomato spotted wilt virus benefits a non-vector arthropod, Tetranychus urticae, by modulating different plant responses in tomato

PLoS One. 2013 Sep 18;8(9):e75909. doi: 10.1371/journal.pone.0075909. eCollection 2013.

Abstract

The interaction between plant viruses and non-vector arthropod herbivores is poorly understood. However, there is accumulating evidence that plant viruses can impact fitness of non-vector herbivores. In this study, we used oligonucleotide microarrays, phytohormone, and total free amino acid analyses to characterize the molecular mechanisms underlying the interaction between Tomato spotted wilt virus (TSWV) and a non-vector arthropod, twospotted spider mite (Tetranychusurticae), on tomato plants, Solanumlycopersicum. Twospotted spider mites showed increased preference for and fecundity on TSWV-infected plants compared to mock-inoculated plants. Transcriptome profiles of TSWV-infected plants indicated significant up-regulation of salicylic acid (SA)-related genes, but no apparent down-regulation of jasmonic acid (JA)-related genes which could potentially confer induced resistance against TSM. This suggests that there was no antagonistic crosstalk between the signaling pathways to influence the interaction between TSWV and spider mites. In fact, SA- and JA-related genes were up-regulated when plants were challenged with both TSWV and the herbivore. TSWV infection resulted in down-regulation of cell wall-related genes and photosynthesis-associated genes, which may contribute to host plant susceptibility. There was a three-fold increase in total free amino acid content in virus-infected plants compared to mock-inoculated plants. Total free amino acid content is critical for arthropod nutrition and may, in part, explain the apparent positive indirect effect of TSWV on spider mites. Taken together, these data suggest that the mechanism(s) of increased host suitability of TSWV-infected plants to non-vector herbivores is complex and likely involves several plant biochemical processes.

MeSH terms

  • Animals
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • Cyclopentanes / metabolism
  • Down-Regulation*
  • Gene Expression Regulation, Plant*
  • Oxylipins / metabolism
  • Plant Diseases*
  • Solanum lycopersicum / metabolism*
  • Solanum lycopersicum / virology
  • Tetranychidae*
  • Tospovirus / metabolism*
  • Transcriptome*

Substances

  • Cyclopentanes
  • Oxylipins
  • jasmonic acid

Grants and funding

This work was supported by a seed grant from The Ecological Genomics Institute at Kansas 565 State University. Publication of this article was funded in part by the Kansas State University Open Access Publishing Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.