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’.
Although histone H3K9 methylation has been intensively studied in animals and a model
plant Arabidopsis thaliana, little is known about the evolution of the
histone methyltransferase and its roles in plant biotic stress response. Here we
identified a Nicotiana benthamiana homolog of H3K9 histone methyltransferase
KRYPTONITE (NbKYP) and demonstrated its fundamental roles on methylation of plant
and virus, beside of leading to the suppression of endogenous gene expression and
virus replication. NbKYP and another gene encoding DNA methyltransferase
CHROMOMETHYLTRANSFERASE 3 (NbCMT3-1) were further identified as
the key components of maintenance of transcriptional gene silencing, a DNA
methylation involved anti-virus machinery. All three types of DNA methylations
(asymmetric CHH and symmetric CHG/CG) were severely affected in
NbKYP-silenced plants, but only severe reduction of CHG methylation found in
NbCMT3-1-silenced plants. Attesting to the importance of plant histone
H3K9 methylation immunity to virus, the virulence of geminiviruses requires
virus-encoded trans-activator AC2 which inhibits the expression of KYP via
activation of an EAR-motif-containing transcription repressor RAV2
(RELATED TO ABI3 and VP1). The reduction of KYP was correlated
with virulence of various similar geminiviruses. These findings provide a novel
mechanism of how virus trans-activates a plant endogenous anti-silencing machinery
to gain high virulence.
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