Abstract
ABF/AREB bZIP transcription factors mediate plant abiotic stress responses by regulating the expression of stress-related genes. These proteins bind to the abscisic acid (ABA)-responsive element (ABRE), which is the major cis-acting regulatory sequence in ABA-dependent gene expression. In an effort to understand the molecular mechanisms of abiotic stress resistance in cultivated potato (Solanum tuberosum L.), we have cloned and characterized an ABF/AREB-like transcription factor from potato, named StABF1. The predicted protein shares 45–57% identity with A. thaliana ABFs proteins and 96% identity with the S. lycopersicum SlAREB1 and presents all of the distinctive features of ABF/AREB transcription factors. Furthermore, StABF1 is able to bind to the ABRE in vitro. StABF1 gene is induced in response to ABA, drought, salt stress and cold, suggesting that it might be a key regulator of ABA-dependent stress signaling pathways in cultivated potato. StABF1 is phosphorylated in response to ABA and salt stress in a calcium-dependent manner, and we have identified a potato CDPK isoform (StCDPK2) that phosphorylates StABF1 in vitro. Interestingly, StABF1 expression is increased during tuber development and by tuber-inducing conditions (high sucrose/nitrogen ratio) in leaves. We also found that StABF1 calcium-dependent phosphorylation is stimulated by tuber-inducing conditions and inhibited by gibberellic acid, which inhibits tuberization.
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Abbreviations
- ABA:
-
Abscisic acid
- GA:
-
Gibberellic acid
- PM:
-
Plasma membrane
References
Abelenda JA, Navarro C, Prat S (2011) From the model to the crop: genes controlling tuber formation in potato. Curr Opin Biotechnol 22:287–292
Banerjee AK, Lin T, Hannapel DJ (2009) Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–1843
Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Casaretto JA, Ho T-H (2005) Transcriptional regulation by abscisic acid in barley (Hordeum vulgare L.) seeds involves autoregulation of the transcription factor HvABI5. Plant Mol Biol 57:21–34
Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29
Chico JM, Raíces M, Téllez-Iñón MT, Ulloa RM (2002) A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol 128:256–270
Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730
Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761
Fan LM, Zhao ZX, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546
Fischer L, Lipavska H, Hausman JF, Opatrny Z (2008) Morphological and molecular characterization of a spontaneously tuberizing potato mutant: an insight into the regulatory mechanisms of tuber induction. BMC Plant Biol 8:117
Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinosaki K, Yamaguchi-Shinosaki 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, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K et al (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525
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 USA 103:1988–1993
Giammaria V, Grandellis C, Bachmann S, Gargantini PR, Feingold SE, Bryan G, Ulloa RM et al (2011) StCDPK2 expression and activity reveal a highly responsive potato calcium-dependent protein kinase involved in light signalling. Planta 233:593–609
Hannapel DJ (1990) Differential expression of potato tuber protein genes. Plant Physiol 94:919–925
Harmon AC (2003) Calcium-regulated protein kinases of plants. Gravit Space Biol Bull 16:83–90
Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouze P, Brunak S (1996) Splice site prediction in Arabidopsis thaliana DNA by combining local and global sequence information. Nucleic Acids Res 24:3439–3452
Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052
Hossain MA, Cho JI, Han M, Ahn CH, Jeon JS, An G, Park PB (2010a) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J Plant Physiol 167:1512–1520
Hossain MA, Lee Y, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB (2010b) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72:557–566
Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT et al (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473
Hu XY, Neill SJ, Cai WM, Tang ZC (2004) Induction of defence gene expression by oligogalacturonic acid requires increases in both cytosolic calcium and hydrogen peroxide in Arabidopsis thaliana. Cell Res 14:234–240
Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F, bZIP Research Group et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111
Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357
Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H (2006) Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748
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
Kirchler T, Briesemeister S, Singer M, Schütze K, Keinath M, Kohlbacher O, Vicente-Carbajosa J, Teige M, Harter K, Chaban C (2010) The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors. Eur J Cell Biol 89:175–183
Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080
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
Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269
Li Z, Komatsu S (2000) Molecular cloning and characterization of calreticulin, a calcium-binding protein involved in the regeneration of rice cultured suspension cells. Eur J Biochem 267:737–745
Lorenzen JH, Ewing EE (1992) Starch accumulation in leaves of potato (Solanum tuberosum L.) during the 1st 18 days of photoperiod treatment. Ann Bot 69:481–485
McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294
Menzel BM (1980) Tuberization in potato (Solanum tuberosum) cultivar Sebago at high temperatures: responses to gibberellins and growth inhibitors. Ann Bot 46:259–266
Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327
Muñiz García MN, País SM, Téllez-Iñón MT, Capiati DA (2011) Characterization of StPPI1, a proton pump interactor from Solanum tuberosum L. that is up-regulated during tuber development and by abiotic stress. Planta 233:661–674
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Orellana S, Yañez M, Espinoza A, Verdugo I, González E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208
País SM, González MA, Téllez-Iñón MT, Capiati DA (2009) Characterization of potato (Solanum tuberosum) and tomato (Solanum lycopersicum) protein phosphatases type 2A catalytic subunits and their involvement in stress responses. Planta 230:13–25
País SM, Muñíz García MN, Téllez-Iñón MT, Capiati DA (2010) Protein phosphatases type 2A mediate tuberization signaling in Solanum tuberosum L. leaves. Planta 232:37–49
Poovaiah BW, Reddy ASN (1987) Calcium messenger system in plants. CRC Crit Rev Plant Sci 6:47–103
Raices M, Gargantini PR, Chinchilla D, Crespi M, Tellez-Inon MT, Ulloa RM (2003) Regulation of CDPK isoforms during tuber development. Plant Mol Biol 52:1011–1024
Reddy VS, Reddy AS (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65:1745–1776
Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032
Sarkar D (2008) The signal transduction pathways controlling in planta tuberization in potato: an emerging synthesis. Plant Cell Rep 27:1–8
Schütze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13:247–255
Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900–1902
The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637
Verslues PE, Zhu JK (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans 33:375–379
Vreugdenhil D, Struik PC (1989) An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75:525–531
Vreugdenhil D, Xu X, Jung CS, van Lammeren AAM, Ewing EE (1999) Initial anatomical changes associated with tuber formation on single-node potato (Solanum tuberosum L.) cuttings: a re-evaluation. Ann Bot 84:675–680
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frei dit Frey N, Leung J (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217
Wenzler HC, Mignery GA, Fisher LM, Park WD (1989) Analysis of a chimeric class-I Patatin-GUS gene in transgenic potato plants: high-level expression in tubers and sucrose-inducible expression in cultured leaf and stem explants. Plant Mol Biol 12:41–50
Xu X, van Lammeren AAM, Vermeer E, Vreugdenhil D (1998) The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol 117:575–584
Yamagishi K, Mitsumori C, Takahashi K, Fujino K, Koda Y, Kikuta Y (1993) Jasmonic acid-inducible gene expression of a Kunitz-type proteinase inhibitor in potato tuber disks. Plant Mol Biol 21:539–541
Yáñez M, Cáceres S, Orellana S, Bastías A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep 28:1497–1507
Yoon GM, Cho HS, Ha HJ, Liu JR, Lee HS (1999) Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol Biol 39: 991–1001
Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XL, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579
Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192:61–73
Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036
Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243
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This work was supported by grants from the National Research Council of Science and Technology (CONICET) and the University of Buenos Aires.
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Muñiz García, M.N., Giammaria, V., Grandellis, C. et al. Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235, 761–778 (2012). https://doi.org/10.1007/s00425-011-1540-7
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DOI: https://doi.org/10.1007/s00425-011-1540-7