A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance

Abstract

Whiteflies, Bemisia tabaci (Hemiptera), are pests causing economic damage to many crops, capable of transmitting hundreds of plant vector-borne viruses. They are believed to secrete salivary protein effectors that can improve vector colonization and reproductive fitness in host plants. However, little is known about effector biology and the precise mechanism of action of whitefly effectors. Here, we report a functional screening of B. tabaci salivary effector proteins (Bsp) capable of modulating plant innate immunity triggered by plant endogenous pattern peptide Pep1. Four immunity suppressors and two elicitors were identified. Bsp9, the most effective immunity suppressor, was further identified to directly interact with an immunity regulator WRKY33. We provide evidence that Bsp9 may suppress plant immune signalling by interfering with the interaction between WRKY33 and a central regulator in the MAPK cascade. The interference by Bsp9 therefore reduces plant resistance to whitefly by inhibiting activation of WRKY33-regulated immunity-related genes. Further detailed analysis based on transgenic plants found that whitefly effector Bsp9 could promote whitefly preference and performance, increasing virus transmission. This study enriches our knowledge on insect effector biology.This article is part of the theme issue ‘Biotic signalling sheds light on smart pest management’.

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

“…Besides exploiting the indirect antagonistic relationship between SA and JA, the salivary effectors of herbivores can directly target JA signaling components to circumvent plant defenses during feeding. We identified that the whitefly salivary effector Bsp9 (also reported as Bt56) interacts with the JA-regulated WRKY33 transcription factor, which positively regulates plant resistance against whiteflies by inducing the expression of the PDF1.2 gene [69]. Another effector HARP1 from cotton bollworm oral secretions can interact with JAZ repressors to prevent COI1-mediated JAZ degradation, thus blocking the JA mediated host defense [70].…”

Herbivore-induced activation of viral phosphatase disarms plant antiviral immunities for pathogen transmission

“…One is that the host protein may be repressed e.g. via salivary effector Bsp9 of whitefly that shuts down host defense system reported previously (Wang et al, 2019). Since whitefly herbivory itself can activate plant defense instead of suppression, this explanation seems most unlikely.…”

“…The leucine-rich repeat protein kinase PEP RECEPTORs (PEPR1/PEPR2) are believed to sense the damage caused by herbivore feeding on plant cell (Huffaker et al, 2006). Besides, we observed that the expression of Arabidopsis PEPR1 was induced by whitefly feeding (Supplementary Figure 2A) or by the presence of Arabidopsis Pep1, a 23-amino acid endogenous peptide (Wang et al, 2019). The facts that Arabidopsis PEPR1/PEPR2 is highly expressed in plant vascular (Bartels et al, 2013), where whiteflies and begomoviruses infect (Yang et al, 2019), prompts us to hypothesize that PEPRs are one major perception machinery to sense whitefly infestation for plant cell.…”

“…We quantified virus infectivity and quantity of virus transmitted by whiteflies from Solanum lycopersicum (tomato) to Arabidopsis . To avoid a possible direct interference of whitefly feeding behavior by βC1 protein, we used whiteflies carrying the closely related begomovirus tomato yellow leaf curl virus (TYLCV) in a limited transmission period (72 h) as we demonstrated before (Wang et al, 2019). The quantity of virus in the βC1-plants and two mpk mutants was about 10-fold and 2-fold higher than in wild-type Col-0 plants (Figure 1E).…”

“…For instance, mosquito-borne bunyaviruses and flaviviruses as well as thrip-borne tospoviruses promote virus transmission by directly increasing vector biting rates and by interfering with the ingestion process (Stafford et al, 2011; Liu et al, 2017). Furthermore, arboviruses may indirectly promote transmission by 1) manipulating the immune responses of both the vector and the host, 2) suppressing host immunity by vector salivary factors, 3) manipulating vector behavior, and 4) encoding transmission facilitators (Vasilakis and Tesh 2015; Wang et al, 2019; Wu et al 2019; Wu and Ye, 2020). Since plants are sessile, around 80% plant viruses are transmitted by insect vectors, especially whiteflies and aphids that transmit more than 50% of all vector-borne viruses.…”