Begomovirus–whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor

Abstract

Plant-mediated interactions between herbivorous arthropods and pathogens transmitted by herbivores are important determinants of the population dynamics of both types of organisms in the field. The role of plant defence in mediating these types of tripartite interactions have been recognized but rarely examined especially at the physiological and molecular levels. Our previous work shows that a worldwide invasive whitefly can establish mutualism with the begomovirus Tomato yellow leaf curl China virus (TYLCCNV) via crop plants. Here, we show that TYLCCNV and betasatellite co-infection suppresses jasmonic acid defences in the plant. Impairing or enhancing defences mediated by jasmonic acid in the plant enhances or depresses the performance of the whitefly. We further demonstrate that the pathogenicity factor βC1 encoded in the betasatellite is responsible for the initiation of suppression on plant defences and contributes to the realization of the virus-vector mutualism. By integrating ecological, mechanistic and molecular approaches, our study reveals a major mechanism of the plant-mediated mutualism between a virus and its vector. As the test plant is an important economic crop, the results also have substantial implications for developing novel strategies for management of crop viruses and the insect vectors associated with them.

Disruption of Ethylene Responses by Turnip mosaic virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector

“…TYLCCNV-infected plants have reduced defense responses and impaired JA signaling, benefiting whitefly vectors and increasing attraction. TYLCCNV is transmitted with a b satellite pathogenicity factor, bC1, which mediates suppression of plant signaling and defense responses (Yang et al, 2008;Zhang et al, 2012). Recently, host proteins were identified that interact with bC1 and mediate suppression of plant signaling and defense responses.…”

Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance

“…Recent studies have shown that the TYLCCNB betasatellite encodes only one protein, bC1, which accounts for the attenuation of JA signaling in plants (Yang et al, 2008;Zhang et al, 2012). We examined whether the bC1 protein is responsible for the repression of plant terpene biosynthesis.…”

“…Irrespective of the genome composition, begomoviruses are transmitted exclusively by members of the whitefly B. tabaci species complex. Increasing evidence reveals that the plant jasmonic acid (JA) signaling pathway plays an important role in whitefly resistance (Zarate et al, 2007;Zhang et al, 2012). Begomovirus infection or stable transgene-expressed viral proteins in plants lead to reduced transcription of some JA-responsive genes (Ascencio-Ibáñez et al, 2008;Yang et al, 2008;LozanoDurán et al, 2011;Zhang et al, 2012), and the impairment of JA signaling enhances vector performance Luan et al, 2013).…”

New Synthesis: Investigating Mutualisms in Virus-Vector Interactions

“…For instance, the 2b silencing suppressor protein of cucumber mosaic virus compromises jasmonate-regulated insect defenses and improves performance of Myzus persicae (green peach aphid; Lewsey et al 2010). Similarly, pathogenicity factor βC1, which is encoded in the betasatellite of tomato yellow leaf curl China virus, suppresses jasmonate-mediated defenses and improves growth of Bemisia tabaci (silverleaf whitefly) on Nicotiana tabacum (Zhang et al 2012).…”

“…Our own unpublished observations show that, if Nicotiana benthamiana is infected with turnip mosaic virus, the survival of newly arriving Myzus persicae (green peach aphids) increases from 30 % to 90 %. Similarly, N. tabacum is a poor host for some B. tabaci biotypes, but whitefly performance is improved greatly through prior begomovirus infection (Zhang et al 2012).…”