Infection of tobacco plants by a begomovirus improves nutritional assimilation by a whitefly

The invasive Middle East-Asia Minor 1 (MEAM1) cryptic species (formerly referred to as the B biotype) of the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) complex has become a major crop pest worldwide due to its global invasion as well as epidemics of begomoviruses it transmits. Previous studies demonstrated that MEAM1 performed better on tobacco [Nicotiana tabacum L. (Solanaceae)] plants infected by Tomato yellow leaf curl China virus (TYLCCNV) than on uninfected plants. However, mechanisms underlying the interactions are not completely understood. In this study, we compared the composition of sugars and amino acids in the phloem sap of uninfected and TYLCCNV-infected tobacco plants with or without whiteflies feeding on the plants. No significant differences were detected in terms of amino acid profiles, percentage of essential amino acids, and sugars:amino acids ratio. However, whiteflies feeding on TYLCCNV-infected plants excreted comparatively a lower percentage of amino acids, especially essential amino acids, or proportionally a higher level of sugars than those feeding on uninfected plants, suggesting that whiteflies feeding on virus-infected plants are able to achieve a more balanced nutritional assimilation. We also compared the honeydew excreted by viruliferous and non-viruliferous whiteflies feeding on cotton [Gossypium hirsutum L. (Malvaceae)], a non-host plant for TYLCCNV, to test the direct effects of the virus on whiteflies. Although the amino acids profiles in honeydew were similar between viruliferous and non-viruliferous whiteflies, the sugars:amino acids ratio in honeydew excreted by viruliferous whiteflies was lower than that of non-viruliferous whiteflies, suggesting that the viruliferous whiteflies assimilated a more imbalanced nutrition with proportionally more sugar. Taken together, our data indicate that although a plant virus may exert negative direct effects on its vector, feeding by the vector on virus-infected plants may improve nutritional assimilation and consequently performance of the vector.