Abstract

Plant-mediated interactions between plant viruses and their vectors are important determinants of the population dynamics of both types of organisms in the field. The whitefly Bemisia tabaci can establish mutualism with begomoviruses via their shared host plants. This mutualism is achieved by the interaction between virulence factors and their host proteins. While the virulence factor βC1 encoded by tomato yellow leaf curl China betasatellite (TYLCCNB), a subviral agent associated to the begomovirus tomato yellow leaf curl China virus (TYLCCNV), may interact with plant protein MYC2, thereby establishing the indirect mutualism between TYLCCNV and whitefly, whether other mechanisms are involved remains unknown. Here, we found the in vitro and in vivo interactions between βC1 and tobacco protein S-phase kinase associated protein 1 (NtSKP1). Silencing the expression of NtSKP1 enhanced the survival rate and fecundity of whiteflies on tobacco plants. NtSKP1 could activate the transcription of genes in jasmonic acid (JA) pathways by impairing the stabilization of JAZ1 protein. Moreover, βC1-NtSKP1 interaction could interfere JAZ1 degradation and attenuate the plant JA defense responses. These results revealed a novel mechanism underlying the better performance of whiteflies on TYLCCNV/TYLCCNB-infected plants.

Highlights

  • Plants are constantly exposed to environmental biotic factors, including plant pathogens and herbivores, both of which are propelled into complex interaction networks in microecosystems (Rzanny and Voigt, 2012; Franco et al, 2017; Noman et al, 2020)

  • Betasatellites associated to begomoviruses have been shown to be determinants in virus disease symptom induction, virus movement, repression of plant defense, and other aspects of viral pathogenesis (Zhou, 2013). bC1 interacts with a number of host proteins to affect phytohormone, methylation, ubiquitin, and photosynthesis pathways in plants

  • We found that tomato yellow leaf curl China betasatellite (TYLCCNB) bC1 interacted with Nicotiana tabacum SKP1 protein (NtSKP1) to disrupt the integrality of SCF complex, thereby suppressing JAZ1 degradation and the subsequent activation of jasmonic acid (JA) signaling pathways (Figure 6)

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Summary

Introduction

Plants are constantly exposed to environmental biotic factors, including plant pathogens and herbivores, both of which are propelled into complex interaction networks in microecosystems (Rzanny and Voigt, 2012; Franco et al, 2017; Noman et al, 2020). Thereinto, virus-plant-vector tripartite interactions can impact the population dynamics of all the three members. In some cases, this tripartite interaction can become a determining factor in the outbreak of diseases and pests (Islam et al, 2020; Noman et al, 2020). Soybean mosaic virus infection of soybean plants may reduce plant palatability for its aphid vectors, but increase aphid feeding preference for infected plants, promoting its transmission (Peñaflor et al, 2016; Li et al, 2018). The biological significance of virus-plant-vector tripartite interactions has been appreciated, molecular mechanisms underlying these complex interactions remain largely unknown

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