Overexpression of the Trehalase Gene AtTRE1 Leads to Increased Drought Stress Tolerance in Arabidopsis and Is Involved in Abscisic Acid-Induced Stomatal Closure    

Abstract

Introduction of microbial trehalose biosynthesis enzymes has been reported to enhance abiotic stress resistance in plants but also resulted in undesirable traits. Here, we present an approach for engineering drought stress tolerance by modifying the endogenous trehalase activity in Arabidopsis (Arabidopsis thaliana). AtTRE1 encodes the Arabidopsis trehalase, the only enzyme known in this species to specifically hydrolyze trehalose into glucose. AtTRE1-overexpressing and Attre1 mutant lines were constructed and tested for their performance in drought stress assays. AtTRE1-overexpressing plants had decreased trehalose levels and recovered better after drought stress, whereas Attre1 mutants had elevated trehalose contents and exhibited a drought-susceptible phenotype. Leaf detachment assays showed that Attre1 mutants lose water faster than wild-type plants, whereas AtTRE1-overexpressing plants have a better water-retaining capacity. In vitro studies revealed that abscisic acidmediated closure of stomata is impaired in Attre1 lines, whereas the AtTRE1 overexpressors are more sensitive toward abscisic acid-dependent stomatal closure. This observation is further supported by the altered leaf temperatures seen in trehalase-modified plantlets during in vivo drought stress studies. Our results show that overexpression of plant trehalase improves drought stress tolerance in Arabidopsis and that trehalase plays a role in the regulation of stomatal closure in the plant drought stress response.

A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose

“…However, in most cases the enhanced stress tolerance did not appear to be linked to increased trehalose accumulation. Indeed, the opposite was true for Arabidopsis tre1 mutants that lacked trehalase activity and had moderately elevated trehalose levels but were more sensitive to drought than wild-type plants (Van Houtte et al, 2013). Thus, we need to search for alternative explanations for the beneficial effects of manipulating trehalose metabolism on stress tolerance and for understanding the role of trehalose metabolism in endogenous responses to abiotic stresses.…”

“…In Arabidopsis, the AtTPS1 gene is highly expressed is guard cells (Gómez et al, 2010), and these cells are one of the few examples where the AtTPS1 protein is abundant enough to have been detected in an untargeted proteomic analysis (Zhao et al, 2008). Expression of AtTPPG and AtTREHALASE1 (AtTRE1; encoding the only known trehalase in Arabidopsis) is also particularly prominent in guard cells, and both genes are induced by ABA, which plays a key role in regulation of stomatal conductance Van Houtte et al, 2013). The Arabidopsis tps1-12 mutant, which carries a weak allele of the AtTPS1 gene, has a smaller stomatal aperture than wild-type plants (Gómez et al, 2010).…”

“…If FT expression in fruits were also dependent on having a functional AtTPS1, as in leaves, then AtTPS1 (and presumably Tre6P) expressed in fruit tissues would have influence over seed dormancy. Impairment of trehalose metabolism in several Arabidopsis mutants (tps1, tppg, and tre1) abolishes the inhibition of seed germination by abscisic acid (ABA), although it is unclear if this is an inherited maternal effect (potentially mediated by FT) or an inherent trait of the mutant seeds (Gómez et al, 2010;Vandesteene et al, 2012;Van Houtte et al, 2013).…”

Trehalases: A neglected carbon metabolism regulator?

“…It seems that ABA directly participates in the upregulation of AtTRE and AtTRE1 is involved in the regulation of ABA signaling in plants. 30 In addition, during the pathogenic interaction between Plasmodiophora brassicae and Arabidopsis thaliana a marked AtTRE1 upregulation was also reported. 12 In contrast, downregulation of PvTRE1 in Phaseolus vulgaris root nodules had a direct role into carbon partitioning, increased nodule biomass and bacteroid viability.…”

Characterization of the promoter region of the glycerol-3-phosphate-O-acyltransferase gene in Lilium pensylvanicum

“…Previous studies have demonstrated that resistance could be improved by importing GPAT cDNA (Yokoi et al, 1998;Sui et al, 2007;Gupta et al, 2013;Mizoi and Yamaguchi-Shinozaki, 2013), but current studies are mostly focused on individual genes that can improve cold resistance in plants (Macková et al, 2013;Van Houtte and Vandesteene, 2013;Wang et al, 2014;Yadav et al, 2014), while associations between the promoters of these genes and resistance have not yet been reported. Plant promoters play an important role in the regulation of gene expression in plants (Kim et al, 2013;Reynolds et al, 2013).…”