Colonization by Phloem-Feeding Herbivore Overrides Effects of Plant Virus on Amino Acid Composition in Phloem of Chili Plants

The 'adaptive host manipulation' hypothesis predicts that parasites can enhance their transmission rates via manipulation of their host's phenotype. For example, many plant pathogens alter the nutritional quality of their host for herbivores that serve as their vectors. However, herbivores, including non-vectors, might cause additional alterations in the plant phenotype. Here, we studied changes in the amino acid (AA) content in the phloem of chilli (Capsicum annuum) plants infected with Pepper golden mosaic virus (PepGMV) upon subsequent colonization with a non-vector, the phloem-feeding whitefly (Trialeurodes vaporariorum). Virus infection alone caused an almost 30-fold increase in overall phloem AAs, but colonization by T. vaporariorum completely reversed this effect. At the level of individual AAs, contents of proline, tyrosine, and valine increased, and histidine and alanine decreased in PepGMV-infected as compared to control plants, whereas colonization by T. vaporariorum caused decreased contents of proline, tyrosine, and valine, and increased contents of histidine and alanine. Overall, the colonization by the whitefly had much stronger effects on phloem AA composition than virus infection. We conclude that the phloem composition of a virus-infected host plant can rapidly change upon arrival of an herbivore and that these changes need to be monitored to predict the nutritional quality of the plant in the long run.