Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis

Abstract

Increasing numbers of investigations indicate that ethylene response factor (ERF) proteins play important roles in plant stress responses via interacting with GCC box and/dehydration-responsive element/C-repeat to modulate expression of downstream genes, but the detailed regulatory mechanism is not well elucidated. Revealing the modulation pathway of ERF proteins in response to stresses is vital. Previously, we showed that tomato ERF protein TERF2/LeERF2 is ethylene inducible, and ethylene production is suppressed in antisense TERF2/LeERF2 tomatoes, suggesting that TERF2/LeERF2 functions as a positive regulator in ethylene biosynthesis. In this paper, we report that regulation of TERF2/LeERF2 in ethylene biosynthesis is associated with enhanced freezing tolerance of tobacco and tomato. Analysis of gene expression showed that cold slowly induces expression of TERF2/LeERF2 in tomato, implying that TERF2/LeERF2 may be involved in cold response through ethylene modulation. To test the hypothesis, we first observed that overexpressing TERF2/LeERF2 tobaccos not only enhances freezing tolerance via activating expression of cold-related genes, but also significantly reduces electrolyte leakage. In addition, with treatment of ethylene biosynthesis inhibitor or ethylene receptor antagonist, we then showed that blockage of ethylene biosynthesis or the ethylene signaling pathway decreases freezing tolerance of overexpressing TERF2/LeERF2 tobaccos. Moreover, the results from tomatoes showed that overexpressing TERF2/LeERF2 tomatoes enhances while antisense TERF2/LeERF2 transgenic lines decreases freezing tolerance, and application of ethylene precursor 1-aminocyclopropane-1-carboxylic acid restored freezing tolerance of antisense lines. Therefore our results establish that TERF2/LeERF2 enhances freezing tolerance of plants through ethylene biosynthesis and the ethylene signaling pathway.

An AP2 Domain-Containing Gene, ESE1, Targeted by the Ethylene Signaling Component EIN3 Is Important for the Salt Response in Arabidopsis

“…However, overaccumulation of EIN3 in the ebf1 ebf2 mutant enhances tolerance to salt stress (Achard et al, 2006), indicating that EIN3 is an important regulator in the salt response. Interestingly, overexpression of a number of ERF genes can enhance stress tolerance, including to salt (Agarwal et al, 2006;Nakano et al, 2006;Wu et al, 2007Wu et al, , 2008Zhang and Huang, 2010;Zhu et al, 2010;Fukao et al, 2011), indicating that ERF proteins also play crucial roles in response to salt stress. In our research here, through mining the available microarray data and combined transcriptional confirmation, we identified three ERF genes (ESE1-ESE3) that were induced by both ethylene and high salt.…”

“…This regulation is also mediated by ethylene signaling (Yamaguchi-Shinozaki and Shinozaki, 2006;Zhang and Huang, 2010;Zhu et al, 2010). For instance, the modulation of ethylene in the salt response of Arabidopsis is controlled by ETR1, CTR1, EIN2, and EIN3 (Achard et al, 2006;Cao et al, 2006Cao et al, , 2007Wang et al, 2007;Yoo et al, 2008).…”

Ethylene Signaling Negatively Regulates Freezing Tolerance by Repressing Expression of CBF and Type-A ARR Genes in Arabidopsis

“…Although ethylene has been implicated in the cold stress response (Harber and Fuchigami, 1989;Ciardi et al, 1997;Yu et al, 2001;Zhang and Huang, 2010), the exact role that ethylene plays in the regulation of freezing stress remains unclear. Here, we undertook a molecular and genetic approach to investigate the role of ethylene biosynthesis and signaling in plant response to freezing stress.…”

Molecular characterization of two AP2/ERF transcription factor genes from Egyptian tomato cultivar (Edkawy)

“…AP2/EREBP (ERF) family members have been reported to function through both ABA-dependent and -independent pathways (Yamaguchishinozakiaib and Shinozaki, 1994; Kizis and Investigacio, 2002). Ethylene response factor (ERF) proteins have been shown to interact with DRE/CBF genes in enhancing plant stress responses, however, the regulatory mechanism is not well known (Zhang and Huang, 2010).…”