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The ethylene signaling pathway has a negative impact on sucrose-induced anthocyanin accumulation in Arabidopsis

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Abstract

In an attempt to understand the complex regulatory mechanisms underlying sucrose-induced flavonoid biosynthesis, we examined several Arabidopsis mutants with altered anthocyanin accumulation. We determined that disruption of ethylene signaling results in a dramatic increase in sucrose-induced anthocyanin accumulation. Furthermore, we investigated why the ein2-1 (ethylene insensitive) Arabidopsis mutant accumulates higher levels of anthocyanin in response to sucrose than wild-type Arabidopsis. An increased level of PAP1 transcript in the ein2-1 mutant appears to be the main factor responsible for the increased accumulation of anthocyanin in response to sucrose. Therefore, our results indicate that the ethylene signaling pathway plays a negative role in sucrose-induced anthocyanin accumulation. We believe that the explanation for this observation may be related to the initiation of the senescence program in plants.

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References

  • Baier M, Hemmann G, Holman R, Corke R, Card R, Smith C, Rook F, Bevan MW (2004) Characterization of mutants in Arabidopsis showing increased sugar-specific gene expression, growth, and developmental responses. Plant Physiol 134:81–91

    Article  CAS  PubMed  Google Scholar 

  • Bariola PA, MacIntosh GC, Green PJ (1999) Regulation of S-like ribonuclease levels in Arabidopsis. Antisense inhibition of RNS1 or RNS2 elevates anthocyanin accumulation. Plant Physiol 119:331–342

    Article  CAS  PubMed  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115

    Article  CAS  PubMed  Google Scholar 

  • Bharti AK, Khurana JP (1997) Mutants of Arabidopsis as tools to understand the regulation of phenylpropanoid pathway and UVB protection mechanisms. Photochem Photobiol 65:765–776

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393

    Article  CAS  PubMed  Google Scholar 

  • Broun P (2004) Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol 7:202–209

    Article  CAS  PubMed  Google Scholar 

  • Christie PJ, Alfenito MR, Walbot V (1994) Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 194:541–549

    Article  CAS  Google Scholar 

  • Cignarella A, Nastasi M, Cavalli E, Puglisi L (1996) Novel lipid-lowering properties of Vaccinium myrtillus L. leaves, a traditional antidiabetic treatment, in several models of rat dyslipidaemia: a comparaison with ciprofibrate. Thromb Res 84:311–322

    Article  CAS  PubMed  Google Scholar 

  • DeWald D, Sadka A, Mullet J (1994) Sucrose modulation of soybean Vsp gene expression is inhibited by auxin. Plant Physiol 104:439–444

    CAS  PubMed  Google Scholar 

  • Dijkwel PP, Huijser C, Weisbeek PJ, Chua NH, Smeekens SC (1997) Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9:583–595

    Article  CAS  PubMed  Google Scholar 

  • Elomaa P, Uimari A, Mehto M, Albert VA, Laitinen RAE, Teeri TH (2003) Activation of anthocyanin biosynthesis in Gerbera hybrida (Asteraceae) suggests conserved protein–protein and protein–promoter interactions between the anciently diverged monocots and eudicots. Plant Physiol 133:1831–1842

    Article  CAS  PubMed  Google Scholar 

  • Farrant JM (2000) A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecol 151:29–39

    Article  Google Scholar 

  • Ferreres F, Gil MI, Castaner M, Tomas FA (1997) Barberan phenolic metabolites in red pigmented lettuce (Lactuca sativa). Changes with minimal processing and cold storage. J Agric Food Chem 45:4249–4254

    Article  Google Scholar 

  • Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126

    Article  CAS  PubMed  Google Scholar 

  • Gollop R, Even S, Colova-Tsolova V, Peri A (2002) Expression of the grape dihydroflavonol reductase gene and analysis of its promoter region. J Exp Bot 53:1397–1409

    Article  CAS  PubMed  Google Scholar 

  • Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083

    Article  CAS  PubMed  Google Scholar 

  • Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 20:3901–3907

    Google Scholar 

  • Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bifunctional enolase. EMBO J 21:2692–2702

    Article  CAS  PubMed  Google Scholar 

  • Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179:1004–1016

    Article  CAS  PubMed  Google Scholar 

  • Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightner J (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanins biosynthesis, modification, and transport. Plant Cell 15:1689–1703

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Tanaka H, Ohme-Takagi M (2004) Suppression of the biosynthesis of proanthocyanidin in Arabidopsis by a chimeric PAP1 repressor. Plant Biotechnol J 2:487–493

    Article  CAS  PubMed  Google Scholar 

  • McKown R, Kuroki G, Warren G (1996) Cold responses of Arabidopsis mutants impaired in freezing tolerance. J Exp Bot 47:1919–1925

    Article  CAS  Google Scholar 

  • Nagira Y, Ozeki Y (2004) A system in which anthocyanin synthesis is induced in regenerated torenia shoots. J Plant Res 117:377–383

    Article  CAS  PubMed  Google Scholar 

  • Nagira Y, Ikegami K, Koshiba T, Ozeki Y (2006) Effect of ABA upon anthocyanin synthesis in regenerated torenia shoots. J Plant Res 119:137–144

    Article  CAS  PubMed  Google Scholar 

  • Nemeth K, Salchert K, Putnoky P (1998) Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev 12:3059–3073

    Article  CAS  PubMed  Google Scholar 

  • Ohto MA, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–261

    Article  CAS  PubMed  Google Scholar 

  • Pasqua G, Monacellia B, Mulinacci N, Rinaldi S, Giaccherini C, Innocenti M, Vinceri F (2005) The effect of growth regulators and sucrose on anthocyanin production in Camptotheca acuminata cell cultures. Plant Physiol Biochem 43:293–298

    Article  CAS  PubMed  Google Scholar 

  • Perata P, Matsukura C, Vernieri P, Yamaguchi J (1997) Sugar repression of a gibberellin-dependent signaling pathway in barley embryos. Plant Cell 9:2197–2208

    Article  CAS  PubMed  Google Scholar 

  • Pfündel EE, Agati G, Cerovic ZG (2006) Optical properties of plant surfaces. In: Riederer M, Müller C (eds) Annual plant reviews 23: Biology of the plant cuticle. Blackwell, Oxford, pp 216–249

    Chapter  Google Scholar 

  • Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R (1999) Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11:1433–1444

    Article  CAS  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Sarkar FH, Li Y (2004) Cell signalling pathways altered by chemoprotective agents. Mutat Res 555:53–64

    CAS  PubMed  Google Scholar 

  • Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646

    Article  CAS  PubMed  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Tahara A (2007) A journey of twenty-five years through the ecological biochemistry of Flavonoids. Biosci Biotechnol Biochem 71:1387–1404

    Article  CAS  PubMed  Google Scholar 

  • Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139:1840–1852

    Article  CAS  PubMed  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Tsukaya H, Ohshima T, Naito S, Chino M, Komeda Y (1991) Sugar dependent expression of the CHS-A gene for chalcone synthase from petunia in transgenic Arabidopsis. Plant Physiol 97:1414–1421

    Article  CAS  PubMed  Google Scholar 

  • Tzvetkova-Chevolleau T, Hutin C, Noël LD (2007) Canonical signal recognition particle components can be bypassed for posttranslational protein targeting in chloroplasts. Plant Cell 19:1635–1648

    Article  CAS  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 18:1–11

    Google Scholar 

  • Vitrac X, Larronde F, Krisa S, Decendit A, Deffieux G, Merillon JM (2000) Sugar sensing and Ca2+ ± calmodulin requirement in Vitis vinifera cells producing anthocyanins. Phytochemistry 53:659–665

    Article  CAS  PubMed  Google Scholar 

  • Vom Endt D, Kijne JW, Memelink J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators? Phytochemistry 61:107–114

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Nair MG, Strasburg GM, Chang YC, Booren AM, Gray JI, De Witt DL (1999) Antioxidant and antiinflammatory activities of anthocyanins and their aglycon, cyanidin, from tart cherries. J Nat Prod 62:294–296

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Liu C, Li K, Sun F, Hu H, Li X, Zhao Y, Han C, Zhang W, Duan Y, Liu M, Li X (2007) Arabidopsis EIN2 modulates stress response through abscisic acid response pathway. Plant Mol Biol 64:633–644

    Article  CAS  PubMed  Google Scholar 

  • Williams RJ, Spencer JPE, Rice-Evans C (2004) Flavonoids: antioxidants or signaling molecules? Free Radic. Biol Med 36:838–849

    CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Ito D, Shinkai Y, Kondo T (2008) Change of color and components in sepals of chameleon hydrangea during maturation and senescence. Phytochemistry 69:3159–3165

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95:10294–10299

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a grant from the National Research Foundation (to Hojoung Lee, 2009; Grant #2009-0078046 & #2009-0065693) and in part by Technology Development Program for Agriculture and Forestry, Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea (to Hojoung Lee; Grant #108066-3).

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Correspondence to Hojoung Lee.

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Y. Kwon and J. E. Oh contributed equally.

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10265_2010_354_MOESM1_ESM.jpg

Figure S1. The ein2-1 mutant has a high level of anthocyanin. Wild-type (black rectangle) and ein2-1 (white rectangle) mutant plants were germinated on MS medium with 50 mM sucrose. Four-day-old seedlings germinated in normal MS-agar medium (50 mM sucrose) were transferred to the designated medium supplemented with 0 or 200 mM mannitol, allowed to grow for 3 days, and then collected for anthocyanin measurement. Data represent the mean values of three independent experiments (n = 50). (JPG 189 kb)

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Kwon, Y., Oh, J.E., Noh, H. et al. The ethylene signaling pathway has a negative impact on sucrose-induced anthocyanin accumulation in Arabidopsis. J Plant Res 124, 193–200 (2011). https://doi.org/10.1007/s10265-010-0354-1

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