Coinfection of Tomato Plants with Tomato yellow leaf curl virus and Tomato chlorosis virus Affects the Interaction with Host and Whiteflies

Susceptible plants infected by single or multiple viruses can differ in symptoms and other alterations influencing virus dissemination. Furthermore, behavior of viruliferous vectors may be altered in certain cases to favor acquisition and inoculation processes conductive to virus transmission. We explored single and mixed infections frequently occurring in tomato crops, caused by two viruses transmitted by the whitefly Bemisia tabaci: Tomato yellow leaf curl virus (TYLCV, Begomovirus, Geminiviridae) and Tomato chlorosis virus (ToCV, Crinivirus, Closteroviridae). Coinfection of both viruses in tomato plants showed more severe symptoms at late stages compared with single infections, although at earlier stages the interaction began with attenuation. This asymmetric synergism correlated with the dynamics of ToCV accumulation and expression of the salicylic acid responsive gene PR-P6. Visual and olfactory cues in whitefly preference were evaluated under controlled conditions in choice assays, testing viruliferous and nonviruliferous adult whiteflies. In experiments allowing both visual and olfactory cues, whiteflies preferred symptomatic leaflets from plants infected either with TYLCV alone or with TYLCV and ToCV, over those infected with ToCV alone or noninfected leaflets, suggesting that TYLCV drove host selection. Odor cues tested in Y-tube olfactometer assays showed neutral effects on whiteflies' preference, and bioassays comparing the attractiveness of colored sticky cards confirmed preference for sectors colored to mimic TYLCV symptomatic leaves compared with asymptomatic leaves. Our results show that the presence of coinfecting viruses affect the host and could alter the behavior of insect vectors.