Abstract
The phytohormone abscisic acid (ABA) plays crucial roles in adaptive responses of plants to abiotic stresses. ABA-responsive element binding proteins (AREBs) are basic leucine zipper transcription factors that regulate the expression of downstream genes containing ABA-responsive elements (ABREs) in promoter regions. A novel ABI-like (ABA-insensitive) transcription factor gene, named TaABL1, containing a conserved basic leucine zipper (bZIP) domain was cloned from wheat. Southern blotting showed that three copies were present in the wheat genome. Phylogenetic analyses indicated that TaABL1 belonged to the AREB subfamily of the bZIP transcription factor family and was most closely related to ZmABI5 in maize and OsAREB2 in rice. Expression of TaABL1 was highly induced in wheat roots, stems, and leaves by ABA, drought, high salt, and low temperature stresses. TaABL1 was localized inside the nuclei of transformed wheat mesophyll protoplast. Overexpression of TaABL1 enhanced responses of transgenic plants to ABA and hastened stomatal closure under stress, thereby improving tolerance to multiple abiotic stresses. Furthermore, overexpression of TaABL1 upregulated or downregulated the expression of some stress-related genes controlling stomatal closure in transgenic plants under ABA and drought stress conditions, suggesting that TaABL1 might be a valuable genetic resource for transgenic molecular breeding.
Similar content being viewed by others
References
Anderson SJ, Abraham KM, Nakayama T, Singer A, Perlmutter RM (1992) Inhibition of T-cell receptor beta-chain gene rearrangement by overexpression of the non-receptor protein tyrosine kinase p56lck. EMBO J 11(4877):4886
Brocard IM, Lynch TJ, Finkelstein RR (2002) Regulation and role of the Arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiol 129(1533):1543
Carles C, Bies-Etheve N, Aspart L, Leon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30(373):383
Casaretto J, Ho T-HD (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15(271):284
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci U S A 105(4495):4500
Chen YT, Liu H, Stone S, Callis J (2013) ABA and the ubiquitin E3 ligase keep on going affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J 75(6):965–976
Choi H, Hong J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 21(1723):1730
Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5(765):771
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12(599):609
Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signalling in seeds and seedlings. Plant Cell 14(S15):S45
Fujii H, Zhu J (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci U S A 106(8380):8385
Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39(863):876
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Keiichiro H, Masaru OT, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17(3470):3488
Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147(1):15–27
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci U S A 103:1988–1993
Gao Z, He X, Zhao B, Zhou C, Liang Y, Ge R, Shen Y, Huang Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51(5):767–775
Gao SQ, Chen M, Xu ZS, Zhao CP, Li LC, Xu HJ, Tang YM, Zhao X, Ma YZ (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75(537):553
Garcia AB, Engler JA, Claes B, Villarroel R, Van Montagu M, Gerats T, Caplan A (1998) The expression of the salt-responsive gene salt from rice is regulated by hormonal and developmental cues. Planta 207(172):180
Ha CV, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LS (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci 111(2):851–856
Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A (2002) Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol 43(136):140
Hobo T, Asada M, Kowyama Y, Hattori T (1999a) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19(679):689
Hobo T, Kowyama Y, Hattori T (1999b) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid induced transcription. Proc Natl Acad Sci U S A 96(15348):15353
Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231(1459):1473
Ito T, Shinozaki K (2002) The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43(1285):1292
Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(106):111
Johnson RR, Wagner RL, Verhey SD, Walker-Simmons MK (2002) The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiol 130(837):846
Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14(343):357
Kim SY, Ma J, Perret P, Li Z, Thomas TL (2002) Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol 130(688):697
Kim S, Kang JY, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40(75):87
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(939):949
Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134(74):86
Lan L, Li M, Lai Y, Xu W, Kong Z, Ying K, Han B, Xue Y (2005) Microarray analysis reveals similarities and variations in genetic programs controlling pollination/fertilization and stress responses in rice (Oryza sativa L.). Plant Mol Biol 59(151):164
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222
Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264(1448):1452
Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulators of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228(225):240
Liu Y, Zhao TJ, Yan YB, Zhou HM (2005) Increase of soluble expression in Escherichia coli cytoplasm by a protein disulfide isomerase gene fusion system. Protein Expr Purif 44(155):161
Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci U S A 98(4782):4787
Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH (2003) AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17(410):418
Lu GJ, Gao CX, Zheng XN, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229(605):615
Lv S, Zhang K, Gao Q, Lian L, Song Y, Zhang J (2008) Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49(1150):1164
Lynch T, Erickson BJ, Finkelstein RR (2012) Direct interactions of ABA-insensitive (ABI)-clade protein phosphatase (PP)2Cs with calcium-dependent protein kinases and ABA response element-binding bZIPs may contribute to turning off ABA response. Plant Mol Biol 80(6):647–658
Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci 96(8271):8276
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(490):498
Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32(7):959–970
Ooms J, Veen R, Karssen CM (1994) Abscisic acid and osmotic stress or slow drying independently induce desiccation tolerance in mutant seeds of Arabidopsis thaliana. Physiol Plant 92(506):510
Oracz K, El-Maarouf Bouteau H, Farrant JM, Cooper K, Belghazi M, Job C, Job D, Corbineau F, Bailly C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. Plant J 50:452–465
Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyl transferase in ABA regulation of guard cell anion channels and plant water loss. Science 282(287):290
Pilot G, Lacombe B, Gaymard F, Cherel I, Boucherez J, Thibaud JB, Sentenac H (2001) Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2. J Biol Chem 276(3215):3221
Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20(2729):2745
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(1755):1767
Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49(865):879
Schroeder JI, Kwak JM, Allen GJ (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410(327):330
Tezuka K, Taji T, Hayashi T, Sakata Y (2013) A novel abi5 allele reveals the importance of the conserved Ala in the C3 domain for regulation of downstream genes and salt tolerance during germination in Arabidopsis. Plant Signal Behav 8(3):e23455
Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178(703):718
Wang Y, Li L, Ye T, Lu Y, Chen X, Wu Y (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64(2):675–684
Xiang Y, Tang N, Du H, Ye HY, Xiong LZH (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952
Xu F, Park MR, Kitazumi A, Herath V, Mohanty B, Yun SJ, Reyes BG (2012) Cis-regulatory signatures of orthologous stress-associated bZIP transcription factors from rice, sorghum and Arabidopsis based on phylogenetic footprints. BMC Genomics 13(497):507
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salinity stress. Plant Cell 6(251):264
Yang X, Yang YN, Xue LJ, Zou MJ, Liu JY, Chen F, Xue HW (2011) Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol 156(1397):1409
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572
Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43(1473):1483
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61(672):685
Zou M, Guan Y, Ren H, Zhang F, Chen F (2007) Characterization of alternative splicing products of bZIP transcription factors OsABI5. Biochem Biophys Res Commun 360(307):313
Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66(675):683
Acknowledgments
We are grateful to Dr. Robert McIntosh (University of Sydney) and Dr. Xingguo Ye (Institute of Crop Science, Chinese Academy of Agricultural Sciences) for modifying this manuscript. The work was funded in part by the National 863 High-tech Project (2012AA10A309), the National Natural Science Foundation of China (31201200), and the International Cooperation Project of Beijing Academy of Agricultural and Forestry Science.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Dong-Bei Xu and Shi-Qing Gao contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Fig. 1
The sequence analysis of TaABL1 protein. A. The conserved domain analysis of TaABL1 protein with other homology proteins. B. Phylogenetic tree of TaABL1 and related proteins using MEGA 4.0 software. TaABL1 belongs to the A subfamily and exhibits high similarities to ZmABI5 (NP_001150949), EeABF6 (AED99724), HvABI5 (ADQ48070), WABI5 (BAD97366), Ntphi-2 (BAB61098), GmABL2 (XP_003526362), BdbZIP (XP_003574628), and SbbZIP (XP_002454604). (GIF 497 kb)
Supplementary Fig. 2
The EMSA analysis of TaABL1 protein. EB staining result of TaABL1 protein binding ABRE element on 12 % PAGE gel. Normal ABRE probe; Mutant ABRE probe; GST: glutathione S-transferase; TaABL1-GST: TaABL1 and GST fusion protein. The experiments were repeated three times. (JPEG 19 kb)
Rights and permissions
About this article
Cite this article
Xu, DB., Gao, SQ., Ma, YZ. et al. ABI-like transcription factor gene TaABL1 from wheat improves multiple abiotic stress tolerances in transgenic plants. Funct Integr Genomics 14, 717–730 (2014). https://doi.org/10.1007/s10142-014-0394-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-014-0394-z