Abstract
The phytohormone abscisic acid (ABA) plays an important role in plant growth and development, for example in seed dormancy and germination, as well as in plant responses to environmental stresses, such as drought and high salinity. Previous studies have shown that ABA regulates the expression of genes with an ABA-responsive element (ABRE) and their corresponding physiological responses. Bioinformatics analysis identified a GRAM domain-containing gene family that has a multiple ABRE cis-element, which was termed the ABA-responsive protein (ABR) family. To analyze the function of the ABR family, we identified homozygous T-DNA insertion mutants and constructed abr1, 2, 3 double mutants and triple mutant. The abr1, abr2 and abr3 single mutants showed a normal phenotype; however, the germination of seeds of the double mutants and triple mutant were insensitive to ABA, NaCl, mannitol and glucose. ABR1-GFP was distributed as a punctate structure in the cytosol and may be localized in the endomembrane system. The ABR2-GFP and ABR3-GFP proteins localized in the cytoplasm. In addition, ABR1, ABR2 and ABR3 were expressed in various tissues, and could be induced by several abiotic stresses, especially by ABA. The expressions of these genes were significantly suppressed in aba2, abi1 and abi2 null mutants. These results suggested that the ABR family may act downstream of ABI1 and ABI2 in the ABA signal transduction process in plants.
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Cutler S R, Rodriguez P L, Finkelstein R R, et al. Abscisic acid: Emergence of a core signaling network. Annu Rev Plant Biol, 2010, 61:651–679
Gosti F, Beaudoin N, Serizet C, et al. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell, 1999, 11:1897–1910
Fujii H, Chinnusamy V, Rodrigues A, et al. In vitro reconstitution of an abscisic acid signalling pathway. Nature, 2009, 462:660–664
Ma Y, Szostkiewicz I, Korte A, et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 2009, 324:1064–1068
Park S Y, Hiroaki F, Yang Z, et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 2009, 324:1068–1071
He Y, Gan S. A novel zinc-finger protein with a proline-rich domain mediates ABA-regulated seed dormancy in Arabidopsis. Plant Mol Biol, 2004, 54:1–9
Giraudat J, Hauge B M, Valon C, et al. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell, 1992, 4:1251–1261
Van Z M, Carles A, Li Y, et al. Control and consequences of chromatin compaction during seed maturation in Arabidopsis thaliana. Plant Signal Behav, 2012, 7:338–341
Park J, Lee N, Kim W, et al. ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell, 2011, 23:1404–1415
Finkelstein R, Gampala S, Rock C. Abscisic acid signaling in seeds and seedlings. Plant Cell, 2002, 14(Suppl):S15–S45
Schmitz N, Abrams S R, Kermode A R. Changes in ABA turnover and sensitivity that accompany dormancy termination of yellow-cedar (Chamaeyparis nootkatensis) seeds. J Exp Bot, 2002, 53:89–91
Xiong L, Gong Z, Rock C D. Modulation of abscisic acid signal transduction and biosynthesis by a Sm-like protein in Arabidopsis. Dev Cell, 2001, 1:771–781
Liu J H, Luo M, Cheng K J, et al. Identification and characterization of a novel barley gene that is ABA-inducible and expressed specifically in embryo and aleurone. J Exp Bot, 1999, 50:727–728
Banno H, Chua N H. Characterization of the Arabidopsis formin-like protein AFH1 and its interacting protein. Plant Cell Physiol, 2000, 41:617–626
Doerks T, Strauss M, Brendel M, et al. GRAM, a novel domain in glucosyltransferases, myotubularins and other putative membrane-associated proteins. Trends Biochem Sci, 2000, 25:483–485
Berger P, Schaffitzel C, Berger I, et al. Membrane association of myotubularin-related protein 2 is mediated by a pleckstrin homology-GRAM domain and a coiled-coil dimerization module. Proc Natl Acad Sci USA, 2003, 100:12177–12182
Choudhury P, Srivastava S, Li Z, et al. Specificity of the myotubularin family of phosphatidylinositol-3-phosphatase is determined by the PH/GRAM Domain. J Biol Chem, 2006, 281:31762–31769
Tsujita K, Itoh T, Ijuin T, et al. Myotubularin regulates the function of the late endosome through the GRAM domain-phosphatidylinositol 3,5-bisphosphate interaction. J Biol Chem, 2004, 279: 13817–13824
Masahide O, Dirk W, Takeshi N, et al. Peroxisome degradation requires catalytically active sterol glucosyltransferase with a GRAM domain. EMBO J, 2003, 22:3231–3141
Shu Y J, Rengasamy R, Srinivasan R. Comparative transcriptional profiling and evolutionary analysis of the GRAM domain family in eukaryotes. Dev Biol, 2008, 314:418–432
Yoo S D, Cho Y H, Sheen J. Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc, 2007, 2:1565–1572
Nakashima K, Fujita Y, Katsura K, et al. Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol, 2006, 60:51–68
Kaplan B, Davydov O, Knight H, et al. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell, 2006, 18:2733–2748
Choi H, Hong J, Ha J, et al. ABFs, a family of ABA-responsive element binding factors. J Biol Chem, 2000, 275:1723–1730
Kang J Y, Choi H I, Im M Y, et al. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell, 2002, 14:343–357
Oh S J, Song S I, Kim Y S, et al. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol, 2005, 138:341–351
Choi H I, Park H J, Park J H, et al. Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol, 2005, 139:1750–1761
Yamaguchi S K, Shinozaki K. Identification of a cis-regulatory region of a gene in Arabidopsis thaliana whose induction by dehydration is mediated by abscisic acid and requires protein synthesis. Mol Gen Genet, 1995, 247:391–398
Luo M, Wang Y Y, Liu X, et al. HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. J Exp Bot, 2012, 63:3297–3306
Gao G, Zhang S, Wang C, et al. Arabidopsis CPR5 independently regulates seed germination and postgermination arrest of development through LOX pathway and ABA signaling. PLoS One, 2011, 6:e19406
Du S C, Byung K H. Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell, 2011, 23:823–842
Rowland O, Ludwig A A, Merrick C J, et al. Functional analysis of Avr9/Cf-9 Rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. Plant Cell, 2005, 17:295–310
Jiang S Y, Cai M, Ramachandran S. The Oryza sativa no pollen (Osnop) gene plays a role in male gametophyte development and most likely encodes a C2-GRAM domain-containing protein. Plant Mol Biol, 2005, 57:835–853
Severine L, Bai Q L, Marie C A, et al. VASCULAR ASSOCIATED DEATH1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell, 2004, 16:2217–2232
Somya D, Radomira V, Vaclav M, et al. Characterization of Arabidopsis thaliana mutant ror-1 (roscovitine-resistant) and its utilization in understanding of the role of cytokinin N-glucosylation pathway in plants. Plant Growth Regul, 2010, 61:231–242
Caro E, Castellano M M, Gutierrez C. A chromatin link that couples cell division to root epidermis patterning in Arabidopsis. Nature, 2007, 447:213–217
Elena C M, Mar C, Crisanto G. GEM, a novel factor in the coordination of cell division to cell fate decisions in the Arabidopsis epidermis. Plant Signal Behav, 2007, 2:494–495
Takemiya A, Yamauchi S, Yano T, et al. Identification of a regulatory subunit of protein phosphatase 1 which mediates blue light signaling for stomatal opening. Plant Cell Physiol, 2012, 54:24–35
Gonzalez G M, Apostolova N, Belles J M, et al. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell, 2002, 14:1833–1846
Lin P C, Hwang S G, Endo A, et al. Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiol, 2007, 143:745–758
Leung J, Merlot S, Giraudat J. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell, 1997, 9:759–771
Stefan H, Michele M, Juan P S, et al. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci, 2002, 115:4891–4900
Hai L S, Xiao J W, Wei H D, et al. Identification of an important site for function of the type 2C protein phosphatase ABI2 in abscisic acid signalling in Arabidopsis. J Exp Bot, 2011, 62:5713–5725
Wan H C, Akira E, Li Z, et al. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell, 2002, 14:2723–2743
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Liu, L., Li, N., Yao, C. et al. Functional analysis of the ABA-responsive protein family in ABA and stress signal transduction in Arabidopsis . Chin. Sci. Bull. 58, 3721–3730 (2013). https://doi.org/10.1007/s11434-013-5941-9
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DOI: https://doi.org/10.1007/s11434-013-5941-9