Advertisement

Plant Molecular Biology

, Volume 97, Issue 1–2, pp 165–176 | Cite as

The zinc-finger transcription factor ZAT6 is essential for hydrogen peroxide induction of anthocyanin synthesis in Arabidopsis

  • Haitao Shi
  • Guoyin Liu
  • Yunxie Wei
  • Zhulong Chan
Article
  • 467 Downloads

Abstract

The accumulation of flavonoids is activated by various abiotic stresses, and the induction of reactive oxygen species (ROS) especially hydrogen peroxide (H2O2) is a general response to abiotic stress in plants. However, the direct link between flavonoids and H2O2 and underlying mechanism remain elusive. In this study, we found that the concentrations of anthocyanin and flavonoids were significantly induced by H2O2 treatment. Furthermore, we found that the transcript level of ZINC FINGER of ARABIDOPSIS THALIANA 6 (ZAT6) was significantly activated after exogenous H2O2 treatment, and modulation of AtZAT6 expression positively affected the concentrations of both anthocyanin and total flavonoids. Notably, exogenous H2O2-induced anthocyanin synthesis was largely alleviated in AtZAT6 knockdown plants, but showed higher level in AtZAT6 overexpressing plants. AtZAT6 directly activated the expressions of TT5, TT7, TT3, TT18, MYB12, and MYB111 through binding to their promoters with TACAAT elements of these genes, and the activation of MYB12 and MYB111 up-regulated the expressions of TT4 and TT6. Taken together, this study indicates that AtZAT6 plays important role in H2O2-activated anthocyanin synthesis, via directly binding to the promoters of several genes that involved in anthocyanin synthesis.

Keywords

Anthocyanin synthesis Flavonoid Hydrogen peroxide (H2O2Transcription factor ZAT6 Arabidopsis 

Notes

Acknowledgements

This research was supported by National Natural Science Foundation of China (No. 31570249), the startup funding and the Scientific Research Foundation of Hainan University (No. kyqd1531) to Haitao Shi.

Author contributions

HS conceived and designed the experiments. HS, GL and YW performed the experiments and analyzed the manuscript. HS wrote and revised the manuscript. ZC provided suggestions and revised the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2018_730_MOESM1_ESM.doc (1.4 mb)
Supplementary material 1 (DOC 1434 KB)

References

  1. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380CrossRefPubMedGoogle Scholar
  2. Bao JS, Cai Y, Sun M, Wang GY, Corke H (2005) Anthocyanins, flavonols, and free radical scavenging activity of Chinese bayberry (Myrica rubra) extracts and their color properties and stability. J Agric Food Chem 53:2327–2332CrossRefPubMedGoogle Scholar
  3. Chen D, Xu G, Tang W, Jing Y, Ji Q, Fei Z, Lin R (2013) Antagonism basic helix-loop-helix/bZIP transcription factors from transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25:1657–1673CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen J, Yang L, Yan X, Liu Y, Wang R, Fan T, Ren Y, Tang X, Xiao F, Liu Y, Cao S (2016) Zinc-finger transcription factor ZAT6 positively regulates cadmium tolerance through the glutathione-dependent pathway in Arabidopsis. Plant Physiol 165:707–719CrossRefGoogle Scholar
  5. Devaiah BN, Nagarajan VK, Raghothama KG (2007) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145:147–159CrossRefPubMedPubMedCentralGoogle Scholar
  6. Field B, Jordan F, Osbourn A (2006) First encounters-deployment of defence-related natural products by plants. New Phytol 172:193–207CrossRefPubMedGoogle Scholar
  7. Gallego-Bartolomé J, Alabadí D, Blázquez MA (2011) DELLA-induced early transcriptional changes during etiolated development in Arabidopsis thaliana. PLoS ONE 6:e23918CrossRefPubMedPubMedCentralGoogle Scholar
  8. Grunewald W, De Smet I, Lewis DR, Löfke C, Jansen L, Goeminne G, Vanden Bossche R, Karimi M, De Rybel B, Vanholme B, Teichmann T, Boerjan W, Van Montagu MC, Gheysen G, Muday GK, Friml J, Beeckman T (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci USA 109:1554–1559CrossRefPubMedPubMedCentralGoogle Scholar
  9. Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504CrossRefPubMedGoogle Scholar
  10. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57:155–171CrossRefPubMedGoogle Scholar
  11. Heppel SC, Jaffé FW, Takos AM, Schellmann S, Rausch T, Walker AR, Bogs J (2013) Identification of key amino acids for the evolution of promoter target specificity of anthocyanin and proanthocyanidin regulating MYB factors. Plant Mol Biol 82:457–471CrossRefPubMedGoogle Scholar
  12. Kim SM, Chung MJ, Ha TJ, Choi HN, Jang SJ, Kim SO, Chun MH, Do SI, Choo YK, Park YI (2012) Neuroprotective effects of black soybean anthocyanins via inactivation of ASK1-JNK/p38 pathways and mobilization of cellular sialic acids. Life Sci 90:874–882CrossRefPubMedGoogle Scholar
  13. Kusano M, Tohge T, Fukushima A, Kobayashi M, Hayashi N, Otsuki H, Kondou Y, Goto H, Kawashima M, Matsuda F, Niida R, Matsui M, Saito K, Fernie AR (2011) Metabolomics reveals comprehensive reprogramming involving two independent metabolic responses of Arabidopsis to UV-B light. Plant J 67:354–369CrossRefPubMedGoogle Scholar
  14. Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, Quail PH (2012) Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24:1398–1419CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430CrossRefPubMedGoogle Scholar
  16. Li Y, den Ende WV, Rolland F (2014) Sucrose induction of anthocyanin biosynthesis is mediated by DELLA. Mol Plant 7:570–572CrossRefPubMedGoogle Scholar
  17. Liu XM, Nguyen XC, Kim KE, Han HJ, Lee K, Yun DJ, Chung WS (2012) Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochem Biophys Res Commun 430:1054–1059CrossRefPubMedGoogle Scholar
  18. Liu Z, Shi MZ, Xie DY (2014) Regulation of anthocyanin biosynthesis in Arabidopsis thaliana red pap1-D cells metabolically programmed by auxins. Planta 239:765–781CrossRefPubMedGoogle Scholar
  19. Luo J, Nishiyama Y, Fuell C, Taguchi G, Elliott K, Hill L, Tanaka Y, Kitayama M, Yamazaki M, Bailey P, Parr A, Michael AJ, Saito K, Martin C (2007) Convergent evolution in the BAHD family of acyl transferases: identification and characterization of anthocyanin acyl transferases from Arabidopsis thaliana. Plant J 50:678–695CrossRefPubMedGoogle Scholar
  20. Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326CrossRefPubMedGoogle Scholar
  21. Maier A, Schrader A, Kokkelink L, Falke C, Welter B, Iniesto E, Rubio V, Uhrig JF, Hülskamp M, Hoecker U (2013) Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74:638–651CrossRefPubMedGoogle Scholar
  22. Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138:1083–1096CrossRefPubMedPubMedCentralGoogle Scholar
  23. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489CrossRefPubMedGoogle Scholar
  24. Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268CrossRefPubMedPubMedCentralGoogle Scholar
  25. Misyura M, Colasanti J, Rothstein SJ (2013) Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. J Exp Bot 64:229–240CrossRefPubMedGoogle Scholar
  26. Mito T, Seki M, Shinozaki K, Ohme-Takagi M, Matsui K (2011) Generation of chimeric repressors that confer salt tolerance in Arabidopsis and rice. Plant Biotechnol J 9:736–746CrossRefPubMedGoogle Scholar
  27. Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K, Michael AJ, Tohge T, Yamazaki M, Saito K (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379CrossRefPubMedGoogle Scholar
  28. Nemie-Feyissa D, Olafsdottir SM, Heidari B, Lillo C (2014) Nitrogen depletion and small R3-MYB transcription factors affecting anthocyanin accumulation in Arabidopsis leaves. Phytochemistry 98:34–40CrossRefPubMedGoogle Scholar
  29. Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181:219–229CrossRefPubMedGoogle Scholar
  30. Rabino I, Mancinelli AL (1986) Light, temperature, and anthocyanin production. Plant Physiol 81:922–924CrossRefPubMedPubMedCentralGoogle Scholar
  31. Saito K, Matsuda F (2010) Metabolomics for functional genomics, systems biology, and biotechnology. Annu Rev Plant Biol 61:463–489CrossRefPubMedGoogle Scholar
  32. Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34CrossRefPubMedGoogle Scholar
  33. Shi H, Chan Z (2014) The Cysteine2/Histidine2-type transcription factor ZINC FINGER of ARABIDOPSIS THALIANA 6-activated C-REPEAT-BINDING FACTOR pathway is essential for melatonin-mediated freezing stress resistance in Arabidopsis. J Pineal Res 57:185–191CrossRefPubMedGoogle Scholar
  34. Shi H, Wang X, Ye T, Chen F, Deng J, Yang P, Zhang Y, Chan Z (2014) The Cysteine2/Histidine2-type transcription factor zinc finger of Arabidopsis thaliana 6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-REPEAT-BINDING FACTOR genes in Arabidopsis. Plant Physiol 165:1367–1379CrossRefPubMedPubMedCentralGoogle Scholar
  35. Shin DH, Choi M, Kim K, Bang G, Cho M, Choi SB, Choi G, Park YI (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett 587:1543–1547CrossRefPubMedGoogle Scholar
  36. Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660–677CrossRefPubMedPubMedCentralGoogle Scholar
  37. Stracke R, Favory JJ, Gruber H, Bartelniewoehner L, Bartels S, Binkert M, Funk M, Weisshaar B, Ulm R (2010a) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ 33:88–103PubMedGoogle Scholar
  38. Stracke R, Jahns O, Keck M, Tohge T, Niehaus K, Fernie AR, Weisshaar B (2010b) Analysis of production of flavonol glycosides-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation. New Phytol 188:985–1000CrossRefPubMedGoogle Scholar
  39. Tohge T, Watanabe M, Hoefgen R, Fernie AR (2013) The evolution of phenylpropanoid metabolism in the green lineage. Crit Rev Biochem Mol Biol 48:123–152CrossRefPubMedGoogle Scholar
  40. Van Oosten MJ, Sharkhuu A, Batelli G, Bressan RA, Maggio A (2013) The Arabidopsis thaliana mutant air1 implicates SOS3 in the regulation of anthocyanins under salt stress. Plant Mol Biol 83:405–415CrossRefPubMedGoogle Scholar
  41. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821CrossRefPubMedPubMedCentralGoogle Scholar
  42. Varshney RK, Ribaut JM, Buckler ES, Tuberosa R, Rafalski JA, Langridge P (2012) Can genomics boost productivity of orphan crops? Nat Biotechnol 30:1172–1176CrossRefPubMedGoogle Scholar
  43. Xu W, Grain D, Le Gourrierec J, Harscoët E, Berger A, Jauvion V, Scagnelli A, Berger N, Bidzinski P, Kelemen Z, Salsac F, Baudry A, Routaboul JM, Lepiniec L, Dubos C (2013) Regulation of flavonoid biosynthesis involves an unexpected complex transcriptional regulation of TT8 expression, in Arabidopsis. New Phytol 198:59–70CrossRefPubMedGoogle Scholar
  44. Zhang Y, Butelli E, De Stefano R, Schoonbeek HJ, Magusin A, Pagliarani C, Wellner N, Hill L, Orzaez D, Granell A, Jones JD, Martin C (2013) Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Curr Biol 23:1094–1100CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhu JJ, Li YR, Liao JX (2013) Involvement of anthocyanins in the resistance to chilling-induced oxidative stress in Saccharum officinarum L. leaves. Plant Physiol Biochem 73:427–433CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, Institute of Tropical Agriculture and ForestryHainan UniversityHaikouChina
  2. 2.Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhanChina

Personalised recommendations