Date Published: February 21, 2019
Publisher: Public Library of Science
Author(s): Ping Li, Chao Liu, Wen-Hao Deng, Dan-Mei Yao, Li-Long Pan, Yun-Qin Li, Yin-Quan Liu, Yan Liang, Xue-Ping Zhou, Xiao-Wei Wang, Bryce W. Falk.
Most plant viruses are vectored by insects and the interactions of virus-plant-vector have important ecological and evolutionary implications. Insect vectors often perform better on virus-infected plants. This indirect mutualism between plant viruses and insect vectors promotes the spread of virus and has significant agronomical effects. However, few studies have investigated how plant viruses manipulate plant defenses and promote vector performance. Begomoviruses are a prominent group of plant viruses in tropical and sub-tropical agro-ecosystems and are transmitted by whiteflies. Working with the whitefly Bemisia tabaci, begomoviruses and tobacco, we revealed that C2 protein of begomoviruses lacking DNA satellites was responsible for the suppression of plant defenses against whitefly vectors. We found that infection of plants by tomato yellow leaf curl virus (TYLCV), one of the most devastating begomoviruses worldwide, promoted the survival and reproduction of whitefly vectors. TYLCV C2 protein suppressed plant defenses by interacting with plant ubiquitin. This interaction compromised the degradation of JAZ1 protein, thus inhibiting jasmonic acid defense and the expression of MYC2-regulated terpene synthase genes. We further demonstrated that function of C2 protein among begomoviruses not associated with satellites is well conserved and ubiquitination is an evolutionarily conserved target of begomoviruses for the suppression of plant resistance to whitefly vectors. Taken together, these results demonstrate that ubiquitination inhibition by begomovirus C2 protein might be a general mechanism in begomovirus, whitefly and plant interactions.
Vector-borne viruses and their insect vectors have coevolved complex relationships [1–4]. On the one hand, viruses and their vectors form a competitive relationship because they share the same host plants. On the other hand, due to the immobility of the host plant, insect vectors play significant roles in the epidemiology of plant viruses [5–10]. Attracting vectors to infected plants, facilitating their feeding and population growth and then dispersal of vectors carrying viruses to new plants would be highly beneficial to virus spread [11–13]. Several animal pathogens can directly affect their vectors to increase transmission rate . By contrast, plant pathogens have been shown mainly to modify behavior of vectors via their shared host plant to achieve an indirect mutualistic relationship between pathogen and vector . However, the innermost mechanisms of such mutualisms are largely unknown.
Whiteflies, host plants and geminiviruses have evolved complex relationship [51–53]. When exploring plant-mediated whitefly and geminivirus interaction, one must bear in mind that geminivirus infection may affect the defense of plant hosts, and in turn the behavior and ecology of the whitefly vector. Previously, most attention has been paid to the effects of begomoviruses associated with betasatellites on insect vectors [27,32,33], whereas the effects of begomoviruses in absence of betasatellites on insect vectors and the innermost mechanism have not been stated clearly. Moreover, association of monopartite begomoviruses with betasatellites and bipartite begomoviruses have originated from monopartite begomoviruses by capturing a pathogenic factor . Therefore, elucidation of mechanisms underlying the interactions between monopartite begomoviruses in the absence of betasatellites and their whitefly vectors will help us to explain how sophisticated mutualism has arisen in the geminivirus-insect vector system.