Transcriptional Regulatory Networks in Response to Abiotic Stresses in Arabidopsis and Grasses

Abstract

Various abiotic stresses such as drought, high salinity, high temperature, and low temperature negatively impact plant growth and productivity of crops. Plants have adapted to respond to these stresses at the molecular, cellular, physiological, and biochemical level, enabling them to survive. Various adverse environmental stresses induce the expression of a variety of genes in many plant species (Xiong et al., 2002; Shinozaki et al., 2003; Bartels and Sunkar, 2005). Numerous stress-induced genes have been identified using microarray experiments (Kreps et al., 2002; Seki et al., 2002). The products of these genes are thought to promote stress tolerance and to regulate gene expression through signal transduction pathways (Xiong et al., 2002; Shinozaki et al., 2003). Abscisic acid (ABA) is produced under water deficit conditions and plays an important role in the stress response and tolerance of plants to drought and high salinity. Exogenous application of ABA induces a number of genes that respond to dehydration and cold stress (Zhu, 2002; Shinozaki et al., 2003). Several reports have characterized genes that are induced by dehydration and cold stress, but do not respond to exogenous application of ABA in Arabidopsis (Arabidopsis thaliana; Zhu, 2002; Yamaguchi-Shinozaki and Shinozaki, 2006). This suggests the existence of ABA-independent and ABA-dependent signal transduction pathways that convert the initial stress signal into cellular responses. To better understand the molecular mechanisms regulating gene expression in response to abiotic stresses, including dehydration and cold stress, studies have initially focused on the analysis of Arabidopsis cis- and trans-acting elements and their role in mediating stress responses (Yamaguchi-Shinozaki and Shinozaki, 2006). Recently, abiotic stress-inducible genes and their cis- and trans-acting elements were also studied in rice (Oryza sativa), a preferred crop plant to study stress responses because of its commercial value, relatively small genome size (approximately 430 Mb), diploid origin (2x = 24), and close relationship to other important cereal crops. Major transcriptional regulatory networks of cis-acting elements and TFs involved in abiotic stress-responsive gene expression in Arabidopsis and grasses such as rice. TFs controlling stress-inducible gene expression are shown in ellipses. cis-Acting elements involved in stress-responsive transcription are shown in white boxes. Protein kinases involved in phosphorylation of TFs are shown in light purple boxes. Small filled circles illustrate modifications of TFs, for example, through phosphorylation, in response to stress signals. The dehydration-responsive element (DRE) containing the core sequence A/GCCGAC was identified as an ABA-independent cis-acting element important for the regulation of gene expression in response to drought, high salinity, and cold stresses in Arabidopsis (Yamaguchi-Shinozaki and Shinozaki, 1994). Similar cis-acting elements, named C-repeat (CRT) and low-temperature-responsive element, both containing the DRE core motif, are present in cold-inducible genes (Baker et al., 1994; Jiang et al., 1996). DRE/CRTs were identified in many promoters of stress-inducible genes from various plants, including Arabidopsis and grasses. The Arabidopsis cDNAs encoding DREB1/CBF and DREB2 were isolated using yeast one-hybrid screening (Stockinger et al., 1997; Liu et al., 1998). These proteins contain APETALA2 (AP2)/ethylene-responsive element binding factor (ERF) motifs and specifically bind to the DRE/CRT sequence, thereby activating transcription of genes driven by the DRE/CRT sequence in Arabidopsis. The AP2/ERF motif is specific to plants and functions as a DNA-binding domain. The Arabidopsis genome contains six DREB1/CBF genes and eight DREB2 genes (Sakuma et al., 2002), including DREB1A, DREB1B, and DREB1C, which are rapidly and transiently induced by cold, but not by dehydration and high-salinity stress (Liu et al., 1998; Fig. 1). By contrast, DREB2A and DREB2B genes are induced upon dehydration and high salinity, but not by cold stress (Liu et al., 1998; Nakashima et al., 2000; Fig. 1). Transcript levels of three other DREB1- and six other DREB2-related genes were low under these stress conditions (Sakuma et al., 2002). DREB1A, DREB1B, and DREB1C proteins are major TFs required for cold-inducible gene expression, whereas the Arabidopsis DREB2A and DREB2B are major TFs required for high salinity- and drought-inducible gene expression, respectively. However, CBF4/DREB1D, DREB1E/DDF2, and DREB1F/DDF1 are weakly induced by osmotic stress, suggesting the existence of cross talk between the DREB1/CBF and the DREB2 pathways under osmotic stresses (Haake et al., 2002; Sakuma et al., 2002; Magome et al., 2004). Transgenic Arabidopsis plants overexpressing DREB1B/CBF1 or DREB1A/CBF3 under control of the cauliflower mosaic virus (CaMV) 35S promoter showed strong tolerance to drought, high salinity, and freez