Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms
ReviewNAC transcription factors in plant abiotic stress responses☆
Highlights
► Abiotic stresses adversely affect the growth and productivity of plants. ► NAC proteins are plant-specific transcription factors. ► Stress-inducible NAC genes have been shown to be involved in abiotic stress response. ► We review the progress on characterization of plant stress-inducible NAC proteins.
Introduction
Abiotic stresses such as drought and high salinity are among the major environmental factors which limit the productivity and growth potential of plants. As a consequence of their sessile growth habit, plants have adapted dynamic responses to these stresses at the physiological, biochemical, and molecular levels, thus enabling them to survive under variable environmental conditions. The phytohormone abscisic acid (ABA) is produced under abiotic stress conditions such as drought and high salinity. ABA is a key mediator in controlling plant response to abiotic stress by regulating stomatal closure and by triggering the activation of many stress-related genes, thereby increasing the tolerance of plants to the stresses. Many abiotic stress responsive genes have been identified in plants, including rice and Arabidopsis, by using molecular techniques such as microarray analysis [1], [2], [3], [4]. Stress induced genes not only function to protect cells from abiotic stress through the production of important enzymes and metabolic proteins (functional proteins) but they also regulate signal transduction and gene expression in the stress response (regulatory proteins). Functional proteins contain hydrophilic proteins including dehydrins and “late embryogenesis abundant” (LEA) proteins, and also enzymes that are required for the synthesis of osmoprotectants such as proline and sugars. Regulatory proteins that are activated in response to abiotic stresses, including transcription factors (TFs) such as DREBs (dehydration-responsive element-binding proteins), AREBs (ABA-responsive element-binding proteins) and NAC proteins, have been identified in Arabidopsis and rice [3], [4]. These proteins regulate the response of plants to abiotic stresses and are thought to be important for stress tolerance. In this article, we specifically review the progress on molecular characterization of stress-inducible NAC proteins of plants.
Section snippets
Various functions of plant-specific NAC transcription factors
NAC proteins are plant-specific TFs which have been shown to function in relation to plant development and also for abiotic and/or biotic stress responses. The cDNA encoding a NAC protein was first reported as the RESPONSIVE TO DEHYDRATION 26 (RD26) gene in Arabidopsis [5]. The NAC domain was identified based on consensus sequences from Petunia NAM and Arabidopsis ATAF1/2 and CUC2 proteins (the domain was named from their first letters of the genes) [6]. Many NAC proteins, including Arabidopsis
Structural feature of NAC proteins
The N-terminus of NAC proteins is a highly homologous region containing the DNA-binding NAC domain. The NAC domain is approximately 150 amino acids in length and contains five conserved regions (A to E). The structure of the DNA-binding NAC domain of Arabidopsis ANAC019 (Arabidopsis thaliana NAC019) has been determined by X-ray crystallography [15]. The NAC domain was reported to lack a classical helix–turn–helix motif; instead it was revealed to possess a new-type of TF fold consisting of a
NAC proteins related to abiotic stress response in Arabidopsis
Our group isolated abiotic stress-responsive NAC proteins as factors regulating the expression of the EARLY RESPONSIVE TO DEHYDRATION 1 (ERD1) gene in Arabidopsis [19], [20], [21], [22], [23]. Firstly, Kiyosue et al. [19] isolated the ERD1 cDNA encoding a Clp protease regulatory subunit (ClpD) from a cDNA library derived from one-hour-dehydrated Arabidopsis plants. Nakashima et al. [20] subsequently isolated the promoter region of the ERD1 gene and demonstrated that ERD1 is not only induced by
Expression of stress-responsive OsNAC genes in rice
Our group previously monitored the expression profiles of rice genes under various stresses using a 1700-cDNA microarray and RNA gel blot analysis [2]. We found that OsNAC6 expression was induced by cold, drought, high salinity, and ABA. OsNAC6 showed high sequence similarity to the Arabidopsis stress-responsive NAC proteins ANAC019, ANAC055, and ANAC072 (RD26) [13] (Fig. 1). Ohnishi et al. [33] also reported that OsNAC6 was induced by cold, high salinity, drought, ABA, and MeJA. Our group
Stress-responsive OsNACs regulate stress-inducible genes and stress tolerance in rice
Hu et al. [35] reported that the overexpression of the stress-responsive SNAC1 gene increased drought and salt tolerance in rice. SNAC1 enhanced drought resistance in transgenic rice plants at the reproductive stage during growth in fields under severe drought stress without affecting yields [35]. Our group showed that many abiotic and biotic stress-responsive genes were up-regulated in OsNAC6-overexpressing rice plants and that the transgenic lines were tolerant to dehydration and high
Stress-responsive NACs in other plants
Stress-responsive NAC genes have been reported in other plants as well. Nogueira et al. [44] reported that the SsNAC23 gene, which homologous to the rice OsNAC5, is associated with cold, herbivory and water stress in sugarcane. Tran et al. [45] identified 31 unigenes containing complete open reading frames encoding GmNAC proteins in soybean. Analysis of the C-terminal regulatory domain using a yeast one-hybrid system indicated that among the 31 GmNAC proteins, 28 have transcriptional activation
Stress-responsive NACs for biotic stress
As we mentioned, Arabidopsis stress-responsive NAC genes such as RD26 respond to JA [25]. JA is a well-known phytohormone that is functionally involved in regulating wounding and biotic stress responses [46]. Thus, it is reasonable to consider that the JA-responsive SNAC factors might function in both biotic as well as abiotic stress responses. Wu et al. [24] reported that ATAF1 overexpression plants, but not mutant lines, showed remarkably enhanced tolerance to drought. Additionally, ATAF1
Stress-responsive NACs and senescence
Our group reported that the Arabidopsis ERD1 gene is induced by senescence [20]. As we mentioned, the expression of ERD1 is controlled by the NAC TFs of the SNAC-A group with the ZFHD1 TF [22], [23]. However, the role of the stress-responsive NAC proteins for senescence is poorly understood. Recently, Sperotto et al. [49] reported that OsNAC5 expression is up-regulated by natural (aging) and induced senescence processes. They suggested that OsNAC5 is a novel senescence-associated ABA-dependent
Conclusion and perspective
Abiotic stress-responsive NAC-type transcription factors, especially the SNAC group genes, have important roles for the control of tolerance against environmental stresses such as drought. Stress-responsive Arabidopsis SNAC-A genes such as RD26 and ATAF1, and rice SNAC-A genes such as SNAC1, OsNAC6/SNAC2, and OsNAC5 can improve drought and/or high-salt stress tolerance by overexpression technology [34], [35], [39]. Recent studies showed that effects of these factors for growth are different
Acknowledgement
We would like to thank Dr Kyonoshin Maruyama for providing technical advice to construct a phylogenetic tree. This work was supported in part by a Grant-in-Aid for Scientific Research (C) of the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan, grants from the Ministry of Agriculture, Forestry and Fisheries (MAFF) of Japan and the Program for the Promotion of Basic Research Activities for Innovative Biosciences (BRAIN) of Japan.
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This article is part of a Special Issue entitled: Plant gene regulation in response to abiotic stress.