Hong-Xing Xu, Li-Xin Qian, Xing-Wei Wang, Ruo-Xuan Shao, Yue Hong, Shu-Sheng Liu, and Xiao-Wei Wang

PNAS January 8, 2019 116 (2) 490-495

Significance

Phytohormone pathways provide plants with a powerful regulatory potential to prioritize their defense strategies to different attackers. However, some pathogens and herbivores can manipulate plant defenses for their own benefits by leveraging these pathways. Identification of effectors that modulate host defenses could provide new insights into pathogens/herbivores-plant interaction. Here we report that a newly discovered insect salivary effector, injected into plant tissues during feeding, facilitates insect performance by activation of plant salicylic acid-signaling pathway. The insect salivary effector achieves this function via interacting with a plant KNOTTED 1-like homeobox transcription factor. These findings extend the existing pathogen effector paradigm to herbivores and give valuable clues for developing novel strategies for pest management.

Abstract

Phloem-feeding insects feed on plant phloem using their stylets. While ingesting phloem sap, these insects secrete saliva to circumvent plant defenses. Previous studies have shown that, to facilitate their feeding, many phloem-feeding insects can elicit the salicylic acid- (SA-) signaling pathway and thus suppress effective jasmonic acid defenses. However, the molecular basis for the regulation of the plant's defense by phloem-feeding insects remains largely unknown. Here, we show that Bt56, a whitefly-secreted low molecular weight salivary protein, is highly expressed in the whitefly primary salivary gland and is delivered into host plants during feeding. Overexpression of the Bt56 gene in plantapromotes susceptibility of tobacco to the whitefly and elicits the SA-signaling pathway. In contrast, silencing the whitefly Bt56 gene significantly decreases whitefly performance on host plants and interrupts whitefly phloem feeding with whiteflies losing the ability to activate the SA pathway. Protein-protein interaction assays show that the Bt56 protein directly interacts with a tobacco KNOTTED 1-like homeobox transcription factor that decreases whitefly performance and suppresses whitefly-induced SA accumulation. The Bt56 orthologous genes are highly conserved but differentially expressed in different species of whiteflies. In conclusion, Bt56 is a key salivary effector that promotes whitefly performance by eliciting salicylic acid-signaling pathway.

See: https://www.pnas.org/content/116/2/490

Figure 3: Bt56 induces a tobacco SA-signaling pathway. (A and B) The effect of overexpressing Bt56 on the tobacco SA pathway. The level of SA (A) and the expression levels of SA-marker genes (B) were measured 48 h after agroinfiltration. (C and D) The effect of infestation by Bt56-silenced whiteflies on the tobacco SA pathway. Three days after infestation by dsGFP- and dsBt56-fed whiteflies, the level of SA (C), and the expression levels of SA-marker genes (D) were measured. The data shown are mean ± SE, n = 6 for the phytohormone measurement, n = 12 for the gene expression on Bt56-overexpressed tobacco, and n = 8 for dsRNA-fed whitefly-infested tobacco. One-way ANOVA, the least significant difference (LSD) test, **P < 0.01, ***P < 0.001.