Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors

• Published in: PLoS pathogens 2019-02, Vol.15 (2), p.e1007607-e1007607
• Main Authors: Li, Ping, Liu, Chao, Deng, Wen-Hao, Yao, Dan-Mei, Pan, Li-Long, Li, Yun-Qin, Liu, Yin-Quan, Liang, Yan, Zhou, Xue-Ping, Wang, Xiao-Wei
• Format: Article
• Language: English
• Subjects: Agricultural ecosystems; Agricultural production; Agroecosystems; Agronomy; Analysis; Animals; Begomovirus - metabolism; Begomovirus - pathogenicity; Biology and Life Sciences; C2 protein; Cyclopentanes - metabolism; Defense industry; Deoxyribonucleic acid; DNA; DNA methylation; Ecosystems; Engineering and Technology; Epidemiology; Flowers & plants; Gene expression; Genes; Genetic engineering; Genetic vectors; Genomes; Health aspects; Hemiptera - metabolism; Hemiptera - virology; Infections; Insect Vectors - metabolism; Insects; Jasmonic acid; Leaf-curl; Medicine and Health Sciences; Molecular biology; Mutualism; Nicotiana - virology; Oxylipins - metabolism; Pest resistance; Plant diseases; Plant Diseases - virology; Plant resistance; Plant viruses; Plant Viruses - pathogenicity; Proteins; Research and Analysis Methods; Symbiosis; Terpene synthase; Tobacco; Tomatoes; Ubiquitin; Ubiquitination; Vectors; Viruses; Whiteflies; Yellow leaf
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1007607

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.