Enhanced association of whitefly-begomovirus competence with plant-mediated mutualism

Vector-borne viruses often manipulate plant defenses against insect vectors, thereby impacting vector population dynamics and in turn virus spread. However, the factors regulating the outcome of insect vector-virus-plant tripartite interactions, such as the feature of virus-vector combinations, are understudied.

Using eight whitefly (Bemisia tabaci)-begomovirus combinations exhibiting different degrees of competence, namely virus transmission efficiency, we examined the association between whitefly-begomovirus competence and plant-mediated mutualism. We found that three begomoviruses, tomato yellow leaf curl virus (TYLCV), cotton leaf curl Multan virus (CLCuMuV) and Sri Lankan cassava mosaic virus (SLCMV), can effectively infect but cause distinct symptoms in tobacco (Nicotiana tabacum) plants. Although the efficient vectors Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) whiteflies performed significantly better on TYLCV-infected plants than on control plants, the less-efficient vector Asia II 1 performed similarly on TYLCV-infected and uninfected plants. CLCuMuV infection of plants significantly enhanced the performance of the efficient vector Asia II 1, whereas the performance of the inefficient vector MEAM1 was unaffected by the virus infection status of the plants. SLCMV infection of plants significantly increased the survival and fecundity of the efficient vector Asia II 1, but did not affect the performance of the poorer vectors MEAM1 and MED.

Combined analysis of our data and case studies from the literature indicates that plant-mediated mutualism between whiteflies and the begomoviruses they transmit is more likely to occur in competent combinations. Our findings shed novel light on the ecological principles governing the variations in insect vector-virus-plant tripartite interactions. © 2024 Society of Chemical Industry.