Stress Granule Protein TZF1 Enhances Salt Stress Tolerance by TargetingACA11mRNA for Degradation in Arabidopsis

Author:

He Siou-Luan,Li BinORCID,Zahurancik Walter J.,Arthur Henry C.,Sidharthan Vaishnavi,Gopalan Venkat,Wang LeiORCID,Jang Jyan-ChyunORCID

Abstract

ABSTRACTTandem CCCH zinc finger (TZF) proteins play diverse roles in plant growth and stress response. Although as many as 11 TZF proteins have been identified inArabidopsis, little is known about the mechanism by which TZF proteins select and regulate the target mRNAs. Here, we report thatArabidopsisTZF1 is a bona-fide stress granule protein. Ectopic expression ofTZF1(TZF1 OE), but not an mRNA binding-defective mutant (TZF1H186YOE), enhances salt stress tolerance inArabidopsis. RNA-seq analyses of NaCl-treated plants revealed that the down-regulated genes inTZF1 OEplants are enriched for functions in salt and oxidative stress responses. Because many of these down-regulated mRNAs contain AU- and/or U-rich elements (AREs and/or UREs) in their 3’-UTRs, we hypothesized that TZF1—ARE/URE interaction might contribute to the observed gene expression changes. Results from RNA immunoprecipitation-quantitative PCR analysis, gel-shift, and mRNA half-life assays indicate that TZF1 binds and triggers degradation of theautoinhibited Ca2+-ATPase 11(ACA11) mRNA, encoding a tonoplast-localized calcium pump that extrudes calcium and dampens the signal transduction pathways necessary for salt stress tolerance. Furthermore, this salt stress-tolerance phenotype was recapitulated inaca11null mutants. Remarkably, a set of positive regulators for salt stress tolerance was upregulated inTZF1 OEplants. These includeNa+/H+Exchanger(NHX) family members known to contribute to Na+homeostasis and salinity stress tolerance. Collectively, we present a model in which TZF1 targetsACA11andACA4directly, and repressors ofNHXsand other negative regulators indirectly for mRNA degradation to enhance plant salt stress tolerance.

Publisher

Cold Spring Harbor Laboratory

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