WRKY Transcription Factors in Nicotiana tabacum Modulate Plant Immunity against Whitefly via Interacting with MAPK Cascade Pathways.

WRKY transcription factors are key regulators of many plant processes, most notably coping with biotic and abiotic stresses. Recently, the function of WRKY in plant defense against phloem-feeding insects such as whitefly (Bemisia tabaci) has been brought to attention. In this study, we found that the expression levels of Nicotiana tabacum WRKY4, WRKY6 and WRKY10 were significantly upregulated when tobacco plants were infested with whiteflies or treated with salicylic acid. Compared to controls, whiteflies lived longer and laid more eggs on NtWRKY-silenced tobacco plants but performed less well on NtWRKY-overexpressing plants. The three NtWRKYs interacted with five mitogen-activated protein kinases (NtMAPKs) in vivo and in vitro. These results suggest that the WRKYs in tobacco positively modulate plant defense against whiteflies through interaction with the mitogen-activated protein kinase cascade (MAPK cascade) pathways, and thus provide new insights into plant defense against phloem-feeding insects.

Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors.

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.

Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors.

Vectors often perform better on plants infected with pathogens, and this promotes the spread of pathogens. However, few studies have examined how plant defensive compounds mediate such mutualistic relationships. Although tobacco plants are relatively poor host plants for the whitefly Bemisia tabaci, tobacco's suitability to the whitefly was substantially increased when infected by the begomovirus Tomato yellow leaf curl China virus. The change in suitability was associated with induced terpenoid synthesis in whitefly-infested plants and repressed terpenoid synthesis in virus-infected plants. Elevation of terpenoid levels via exogenous stem applications reduced the performance of whiteflies. In contrast, suppression of terpenoid synthesis via gene silencing improved whitefly fitness. By integrating genomics, transcriptomics and metabolomics, this study demonstrated that virus infection depleted the terpenoid-mediated plant defence against whiteflies, thereby favouring vector-virus mutualism. These data suggest that plant terpenoids play a key role in shaping vector-pathogen relationships.