Cell Host & Microbe
Volume 29, Issue 9, 8 September 2021, Pages 1393-1406.e7
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Article
A calmodulin-binding transcription factor links calcium signaling to antiviral RNAi defense in plants

https://doi.org/10.1016/j.chom.2021.07.003Get rights and content
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Highlights

  • Plants recognize wounding-triggered Ca2+ flux to prime antiviral RNAi defense

  • CAMTA3 activates RDR6/BN2 expression to enhance antiviral RNAi

  • BN2 upregulates AGO1/2 and DCL1 RNA levels by degrading miRNAs

  • Geminivirus proteins disrupt CaM-CAMTA3 interaction to suppress antiviral RNAi

Summary

RNA interference (RNAi) is an across-kingdom gene regulatory and defense mechanism. However, little is known about how organisms sense initial cues to mobilize RNAi. Here, we show that wounding to Nicotiana benthamiana cells during virus intrusion activates RNAi-related gene expression through calcium signaling. A rapid wound-induced elevation in calcium fluxes triggers calmodulin-dependent activation of calmodulin-binding transcription activator-3 (CAMTA3), which activates RNA-dependent RNA polymerase-6 and Bifunctional nuclease-2 (BN2) transcription. BN2 stabilizes mRNAs encoding key components of RNAi machinery, notably AGONAUTE1/2 and DICER-LIKE1, by degrading their cognate microRNAs. Consequently, multiple RNAi genes are primed for combating virus invasion. Calmodulin-, CAMTA3-, or BN2-knockdown/knockout plants show increased susceptibility to geminivirus, cucumovirus, and potyvirus. Notably, Geminivirus V2 protein can disrupt the calmodulin-CAMTA3 interaction to counteract RNAi defense. These findings link Ca2+ signaling to RNAi and reveal versatility of host antiviral defense and viral counter-defense.

Keywords

Ca2+
RNAi
virus
CAMTA3
transcription factor
plant
geminivirus
V2

Data and code availability

All data and materials needed to replicate the work are available. Accession numbers: Sequence data from this article can be found in the GenBank/EMBL databases under the following accession numbers: CaM1 (MN746380); CaM3 (MN746379); CaM6 (MN746381); CAMTA3 (MN746383); BN2 (MN746382); CLCuMuV (GQ924756). WT and bn2 sRNA sequencing data have been deposited in National Center for Biotechnology Information (NCBI) under Bioproject PRJNA611704 and PRJNA611711. Original data have been deposited to Mendeley Data: https://data.mendeley.com/datasets/k5r6z5zkpk/draft?a=379ee2d9-9261-4541-8fd1-15ef39af9af5.

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These authors contributed equally

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