The C2H2 zinc‐finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B

Abstract

SummaryAbiotic stresses are a major cause of crop loss. Ascorbic acid (AsA) promotes stress tolerance by scavenging reactive oxygen species (ROS), which accumulate when plants experience abiotic stress. Although the biosynthesis and metabolism of AsA are well established, the genes that regulate these pathways remain largely unexplored. Here, we report on a novel regulatory gene from tomato (Solanum lycopersicum) named SlZF3 that encodes a Cys2/His2‐type zinc‐finger protein with an EAR repression domain. The expression of SlZF3 was rapidly induced by NaCl treatments. The overexpression of SlZF3 significantly increased the levels of AsA in tomato and Arabidopsis. Consequently, the AsA‐mediated ROS‐scavenging capacity of the SlZF3‐overexpressing plants was increased, which enhanced the salt tolerance of these plants. Protein–protein interaction assays demonstrated that SlZF3 directly binds CSN5B, a key component of the COP9 signalosome. This interaction inhibited the binding of CSN5B to VTC1, a GDP‐mannose pyrophosphorylase that contributes to AsA biosynthesis. We found that the EAR domain promoted the stability of SlZF3 but was not required for the interaction between SlZF3 and CSN5B. Our findings indicate that SlZF3 simultaneously promotes the accumulation of AsA and enhances plant salt‐stress tolerance.

C2H2 Zinc Finger Proteins: Master Regulators of Abiotic Stress Responses in Plants

“…C2H2-type zinc finger proteins with EAR motifs play important roles in regulating abiotic-stress-related gene expression under conditions such as salt, drought, and low temperature (Han and Fu, 2019). The DLNL sequence (DLNbox) at the C-terminus of STZ, with trans-activation activity, functions in the transcriptional activation of DREB1A under salt stress (Sakamoto et al, 2004;Kazan, 2006;Zhang et al, 2016c;Li et al, 2018), while the DLN-box is not the only domain that determines the transcriptional inhibitory activity of C2H2 zinc finger proteins (Huang et al, 2009a).…”

“…C2H2 zinc finger proteins directly target key genes involved in the biosynthesis of osmotic adjustment substances to improve osmotic stress resistance in plants (Xu et al, 2008;Sun et al, 2010;Huang et al, 2012;Yu et al, 2014;Wang et al, 2016;Han et al, 2019b). C2H2 zinc finger proteins also directly target antioxidant genes associated with reactive oxygen species (ROS) scavenging under abiotic stress conditions (Rizhsky et al, 2004;Davletova et al, 2005a;Huang et al, 2009a;Sun et al, 2010;Chu et al, 2016;Liu et al, 2017;Li et al, 2018). C2H2 zinc finger proteins directly target C-repeat/DRE-binding factor genes (CBFs) to improve cold resistance in plants (Vogel et al, 2005).…”

“…Transgenic tomato and Arabidopsis plants overexpressing SlZF3 show significantly increased levels of ascorbic acid. Bimolecular fluorescence complementation (BiFC) and Co-Immunoprecipitation (Co-IP) experiments show that SlZF3 directly binds CSN5B, a key component of the COP9 signalosome; CSN5B can promote the degradation of AsA in Arabidopsis by binding to VTC1, so the interaction of SlZF3 and CSN5B inhibited the binding of CSN5B to VTC1, which contributes to AsA biosynthesis (Li et al, 2018).…”

Manipulation of Ascorbate Biosynthetic, Recycling, and Regulatory Pathways for Improved Abiotic Stress Tolerance in Plants

“…The tomato C2H2-type zinc finger 3 (ZF3) gene was first identified based on being induced in salt-stressed tomato plants [128]. The ZF3 protein in tomato has now recently been identified to interact with CSN5B and inhibit the interaction between CSN5B and GMP [129]. By doing so, ZF3 prevents the ubiquitination and degradation of GMP through the 26S proteasome pathway, promoting the accumulation of GMP [129].…”

“…The ZF3 protein in tomato has now recently been identified to interact with CSN5B and inhibit the interaction between CSN5B and GMP [129]. By doing so, ZF3 prevents the ubiquitination and degradation of GMP through the 26S proteasome pathway, promoting the accumulation of GMP [129]. Knock-down of the ZF3 gene with RNAi in tomato reduced ascorbate to 80% of wild-type levels [129].…”