Planta

, Volume 235, Issue 4, pp 761–778 | Cite as

Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro

  • María Noelia Muñiz García
  • Verónica Giammaria
  • Carolina Grandellis
  • María Teresa Téllez-Iñón
  • Rita María Ulloa
  • Daniela Andrea Capiati
Original Article

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.

Keywords

StABF1 Solanum tuberosum L. Abscisic acid Abiotic stress StCDPK2 Tuberization 

Abbreviations

ABA

Abscisic acid

GA

Gibberellic acid

PM

Plasma membrane

Notes

Acknowledgments

This work was supported by grants from the National Research Council of Science and Technology (CONICET) and the University of Buenos Aires.

Supplementary material

425_2011_1540_MOESM1_ESM.doc (645 kb)
Supplementary material 1 (DOC 645 kb)

References

  1. Abelenda JA, Navarro C, Prat S (2011) From the model to the crop: genes controlling tuber formation in potato. Curr Opin Biotechnol 22:287–292PubMedCrossRefGoogle Scholar
  2. Banerjee AK, Lin T, Hannapel DJ (2009) Untranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–1843PubMedCrossRefGoogle Scholar
  3. Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424PubMedCrossRefGoogle Scholar
  4. 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 72:248–254PubMedCrossRefGoogle Scholar
  5. 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 57:21–34PubMedCrossRefGoogle Scholar
  6. Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29PubMedCrossRefGoogle Scholar
  7. 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 128:256–270PubMedCrossRefGoogle Scholar
  8. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730PubMedCrossRefGoogle Scholar
  9. 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 139:1750–1761PubMedCrossRefGoogle Scholar
  10. Fan LM, Zhao ZX, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546PubMedCrossRefGoogle Scholar
  11. 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 8:117PubMedCrossRefGoogle Scholar
  12. 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 106:8380–8385PubMedCrossRefGoogle Scholar
  13. 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 17:3470–3488PubMedCrossRefGoogle Scholar
  14. 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 124:509–525PubMedCrossRefGoogle Scholar
  15. 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 103:1988–1993PubMedCrossRefGoogle Scholar
  16. 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 233:593–609PubMedCrossRefGoogle Scholar
  17. Hannapel DJ (1990) Differential expression of potato tuber protein genes. Plant Physiol 94:919–925PubMedCrossRefGoogle Scholar
  18. Harmon AC (2003) Calcium-regulated protein kinases of plants. Gravit Space Biol Bull 16:83–90PubMedGoogle Scholar
  19. 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 24:3439–3452PubMedCrossRefGoogle Scholar
  20. Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479PubMedCrossRefGoogle Scholar
  21. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052PubMedCrossRefGoogle Scholar
  22. 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 167:1512–1520PubMedCrossRefGoogle Scholar
  23. 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 72:557–566CrossRefGoogle Scholar
  24. 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 231:1459–1473PubMedCrossRefGoogle Scholar
  25. 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 14:234–240PubMedCrossRefGoogle Scholar
  26. 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 7:106–111PubMedCrossRefGoogle Scholar
  27. Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357PubMedCrossRefGoogle Scholar
  28. 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 18:2733–2748PubMedCrossRefGoogle Scholar
  29. 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 40:75–87PubMedCrossRefGoogle Scholar
  30. 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 89:175–183PubMedCrossRefGoogle Scholar
  31. 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 19:1065–1080PubMedCrossRefGoogle Scholar
  32. Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134:74–86PubMedCrossRefGoogle Scholar
  33. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269PubMedCrossRefGoogle Scholar
  34. 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 267:737–745PubMedCrossRefGoogle Scholar
  35. Lorenzen JH, Ewing EE (1992) Starch accumulation in leaves of potato (Solanum tuberosum L.) during the 1st 18 days of photoperiod treatment. Ann Bot 69:481–485Google Scholar
  36. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294PubMedCrossRefGoogle Scholar
  37. Menzel BM (1980) Tuberization in potato (Solanum tuberosum) cultivar Sebago at high temperatures: responses to gibberellins and growth inhibitors. Ann Bot 46:259–266Google Scholar
  38. 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:e327PubMedCrossRefGoogle Scholar
  39. 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 233:661–674PubMedCrossRefGoogle Scholar
  40. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedCrossRefGoogle Scholar
  41. 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 33:2191–2208PubMedCrossRefGoogle Scholar
  42. 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 230:13–25PubMedCrossRefGoogle Scholar
  43. País SM, Muñíz García MN, Téllez-Iñón MT, Capiati DA (2010) Protein phosphatases type 2A mediate tuberization signaling in Solanum tuberosum L. leaves. Planta 232:37–49PubMedCrossRefGoogle Scholar
  44. Poovaiah BW, Reddy ASN (1987) Calcium messenger system in plants. CRC Crit Rev Plant Sci 6:47–103PubMedCrossRefGoogle Scholar
  45. Raices M, Gargantini PR, Chinchilla D, Crespi M, Tellez-Inon MT, Ulloa RM (2003) Regulation of CDPK isoforms during tuber development. Plant Mol Biol 52:1011–1024PubMedCrossRefGoogle Scholar
  46. Reddy VS, Reddy AS (2004) Proteomics of calcium-signaling components in plants. Phytochemistry 65:1745–1776PubMedCrossRefGoogle Scholar
  47. Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032PubMedCrossRefGoogle Scholar
  48. Sarkar D (2008) The signal transduction pathways controlling in planta tuberization in potato: an emerging synthesis. Plant Cell Rep 27:1–8PubMedCrossRefGoogle Scholar
  49. Schütze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13:247–255PubMedCrossRefGoogle Scholar
  50. Sheen J (1996) Ca2+-dependent protein kinases and stress signal transduction in plants. Science 274:1900–1902PubMedCrossRefGoogle Scholar
  51. The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195Google Scholar
  52. 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 97:11632–11637PubMedCrossRefGoogle Scholar
  53. 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 33:375–379PubMedCrossRefGoogle Scholar
  54. Vreugdenhil D, Struik PC (1989) An integrated view of the hormonal regulation of tuber formation in potato (Solanum tuberosum). Physiol Plant 75:525–531CrossRefGoogle Scholar
  55. 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 84:675–680CrossRefGoogle Scholar
  56. 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 1:198–217PubMedCrossRefGoogle Scholar
  57. 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 12:41–50CrossRefGoogle Scholar
  58. 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 117:575–584PubMedCrossRefGoogle Scholar
  59. 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 21:539–541PubMedCrossRefGoogle Scholar
  60. 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 28:1497–1507PubMedCrossRefGoogle Scholar
  61. 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: 991–1001Google Scholar
  62. 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 140:558–579PubMedCrossRefGoogle Scholar
  63. 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 192:61–73PubMedCrossRefGoogle Scholar
  64. 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 19:3019–3036PubMedCrossRefGoogle Scholar
  65. 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 154:1232–1243PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • María Noelia Muñiz García
    • 1
  • Verónica Giammaria
    • 1
  • Carolina Grandellis
    • 1
  • María Teresa Téllez-Iñón
    • 1
  • Rita María Ulloa
    • 1
  • Daniela Andrea Capiati
    • 1
  1. 1.Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Consejo Nacional de Investigaciones Científicas y Técnicas and Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos AiresBuenos AiresArgentina

Personalised recommendations