Skip to main content
Log in

High anthocyanin accumulation in an Arabidopsis mutant defective in chloroplast biogenesis

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Anthocyanin has an important antioxidant protective effect on plant resistance to oxidative stress. In this study, an Arabidopsis mutant dpg1 (delayed pale-greening) with a chloroplast development defect was studied. It was found that the anthocyanin accumulation of this mutant had increased during the seedling stage, and the expressions of the anthocyanin biosynthetic and regulatory genes were up-regulated. Further studies showed that exogenous ABA (abscisic acid) treatments significantly promoted the chloroplast development of the dpg1 mutant, and the anthocyanin content was significantly decreased to the level of the wild-type. When using NF (norflurazon) to simulate the oxidative stress treatments of wild-type Arabidopsis, the anthocyanin content had significantly increased compared with the control. However, the exogenous ABA treatments could significantly reduce the anthocyanin accumulation level induced by the oxidative stress. Furthermore, the components ABI1 (abscisic acid insensitive 1) and ABI3 (abscisic acid insensitive 3) of the ABA signaling pathway were found to play important roles during this process. These results indicate that the increases in the anthocyanin accumulation in the dpg1 mutant seedlings could be mediated by oxidative stress. Meanwhile, the ABI1 and ABI3 were involved in the process of the ABA inhibiting anthocyanin accumulation which had been induced by the oxidative stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Azeem S, Li Z, Zheng H, Lin W, Arafat Y, Zhang Z, Lin X, Lin W (2016) Quantitative proteomics study on Lsi1 in regulation of rice (Oryza sativa L.) cold resistance. Plant Growth Regul 78:307–323

    Article  CAS  Google Scholar 

  • Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NM (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277:2006–2011

    Article  CAS  PubMed  Google Scholar 

  • Borevitz JO, Xia Y, 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  PubMed Central  Google Scholar 

  • Bueno P, Piqueras A, Kurepa J, Savoure A, Verbruggen A, Montagu MV, Inze D (1998) Expression of antioxidant enzymes in response to abscisic acid and high osmoticum in tobacco BY-2 cell cultures. Plant Sci 138:27–34

    Article  CAS  Google Scholar 

  • Burgess D, Taylor W (1987) Chloroplast photooxidation affects accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170:520–527

    Article  CAS  PubMed  Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9

    Article  CAS  Google Scholar 

  • Chen P, Hu H, Zhang Y, Wang Z, Dong G, Cui Y, Qian Q, Ren D, Guo L (2018) Genetic analysis and fine-mapping of a new rice mutant, white and lesion mimic leaf1. Plant Growth Regul 85:425–435

    Article  CAS  Google Scholar 

  • Cheng J, Yuan S, Zhang ZW, Zhu F, Tang H, Xu F, Feng H, Xie HF, Xu WL, Lin HH (2012) Plastid-signalling-mediated anthocyanin accumulation in mature Arabidopsis rosettes. Plant Growth Regul 68:223–230

    Article  CAS  Google Scholar 

  • Chory J, Peto C, Feinbaum R, Pratt L, Ausubel F (1989) Arabidopsis thaliana mutant that develops as a light-grown plant in the absence of light. Cell 58:991–999

    Article  CAS  PubMed  Google Scholar 

  • Cottage A, Mott EK, Kempster JA, Gray JC (2010) The Arabidopsis plastid-signalling mutant gun (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J Exp Bot 61:3773–3786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubos C, Le JG, Baudry A, Huep G, Lanet E, Debeaujon I, Routaboul JM, Alboresi A, Weisshaar B, Lepiniec L (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J 55:940–953

    Article  CAS  PubMed  Google Scholar 

  • Feng P, Guo H, Chi W, Chai X, Sun X, Xu X, Ma J, Rochaix JD, Leister D, Wang H, Lu C, Zhang L (2016) Chloroplast retrograde signal regulates flowering. Proc Natl Acad Sci 113:10708–10713

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Frenkel M, Kulheim C, Jankanpaa HJ, Skogstrom O, Dall’Osto L, Agren J, Bassi R, Moritz T, Moen J, Jansson S (2009) Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming. BMC Plant Biol 9:12–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan Y, Li H, Xie Y, Wu W, Li M, Wang X, Huang J (2014) THF1 mutations lead to increased basal and wound-induced levels of oxylipins that stimulate anthocyanin biosynthesis via COI1 signaling in Arabidopsis. J Integr Plant Biol 56:916–927

    Article  CAS  PubMed  Google Scholar 

  • Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391

    Article  CAS  PubMed  Google Scholar 

  • Gong M, Li YJ, Chen SZ (1998) Abscisic acid-induced thermotoleranee in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol 153:488–496

    Article  CAS  Google Scholar 

  • Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827

    Article  CAS  PubMed  Google Scholar 

  • Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780

    Article  CAS  PubMed  Google Scholar 

  • Guan L, Scandalios JG (1998) Two structurally similar maize cytosolic superoxide dismutase genes, Sod4 and Soc4A, respond differentially to abscisic acid and high osmoticum. Plant Physiol 117:217–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan L, Zhao J, Scandalios JG (2000) Cis-elements and transfactors that regulate expression of the maize Catl antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense response. Plant Cell 8:1773–1791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez JA, Olmos E, Corpas FJ, Sevilla F, del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167

    Article  CAS  Google Scholar 

  • Hoffmann AM, Noga G, Hunsche M (2016) Alternating high and low intensity of blue light affects PSII photochemistry and raises the contents of carotenoids and anthocyanins in pepper leaves. Plant Growth Regul 79:275–285

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Jiang M, Zhang A (2006) Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New phytol 173:27–38

    Article  CAS  Google Scholar 

  • Huang X, Zhang X, Yang S (2009) A novel chloroplast-localized protein EMB1303 is required for chloroplast development in Arabidopsis. Cell Res 19:1205–1216

    Article  CAS  PubMed  Google Scholar 

  • Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Role of abscisic acid in water stress induced antioxidant defense in leaves of maize seedlings. Free Rad Res 36:1001–10l0l5

    Article  CAS  Google Scholar 

  • Kaminaka H, Morita S, Tokumoto M, Masumura T, Tanaka K (1999) Differential gene expression of rice superoxide dismutase isoforms to oxidative and environmental stresses. Free Rad Res 31:S219–S225

    Article  CAS  Google Scholar 

  • Kikuchi S, Oishi M, Hirabayashi Y, Lee DW, Hwang I, Nakai M (2009) A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 21:1781–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand A (2007) Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol 144:1391–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La Rocca N, Rascio N, Oster U, Rudiger W (2001) Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 213:101–108

    Article  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354:110–116

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Liu D, Li W, Cheng J (2016) The novel protein DELAYED PALE-GREENING1 is required for early chloroplast biogenesis in Arabidopsis thaliana. Sci Rep 6:srep25742

    Article  CAS  Google Scholar 

  • Maruta T, Noshi M, Nakamura M, Matsuda S, Tamoi M, Ishikawa T, Shigeoka S (2014) Ferulic acid 5-hydroxylase 1 is essential for expression of anthocyanin biosynthesis-associated genes and anthocyanin accumulation underphotooxidative stress in Arabidopsis. Plant Sci 219–220:61–68

    Article  CAS  PubMed  Google Scholar 

  • Matsui K, Umemura Y, Ohme-Takagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55:945–967

    Article  CAS  Google Scholar 

  • Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138:1083–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura E, Kato Y, Sakamoto W (2010) Comparative transcriptome analysis of green/white variegated sectors in Arabidopsis yellow variegated2: responses to oxidative and other stresses in white sectors. J Exp Bot 61:2433–2445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20:3148–3162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759

    Article  CAS  PubMed  Google Scholar 

  • Page M, Sultana N, Paszkiewicz K, Florance H, Smirnoff N (2012) The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. Plant Cell Environ 35:388–404

    Article  CAS  PubMed  Google Scholar 

  • Pelletier MK, Murrell JR, Shirley BW (1997) Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis. Further evidence for differential regulation of “early” and “late” genes. Plant Physiol 113:1437–1445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowan DD, Cao M, Lin WK, Cooney JM, Jensen DJ, Austin PT, Hunt MB, Norling C, Hellens RP, Schaffer RJ, Allan AC (2009) Environmental regulation of leaf colour in red 35S:PAP1 Arabidopsis thaliana. New Phytol 182:102–115

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W, Miura E, Kaji Y, Okuno T, Nishizono M, Ogura T (2004) Allelic characterization of the leaf-variegated mutation var2 identifies the conserved amino acid residues of FtsH that are important for ATP hydrolysis and proteolysis. Plant Mol Biol 56:705–716

    Article  CAS  PubMed  Google Scholar 

  • Sarafraz-Ardakani MR, Khavari-Nejad RA, Moradi F, Najafi F (2014) Abscisic acid and cytokinin-induced carbohydrate and antioxidant levels regulation in drought-resistant and -susceptible wheat cultivar during grain filling under field conditions. Int J Biosci 5:11–24

    Article  CAS  Google Scholar 

  • Shin J, Park E, Choi G (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 49:981–994

    Article  CAS  PubMed  Google Scholar 

  • Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361

    Article  CAS  Google Scholar 

  • 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 50:660–667

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • Wang Y, Wang Y, Song Z, Zhang H (2016) Repression of MYBL2 by both microRNA858a and HY5 leads to the activation of anthocyanin biosynthetic pathway in Arabidopsis. Mol Plant 9:1395–1405

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  CAS  PubMed  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  PubMed Central  Google Scholar 

  • Xie Y, Tan H, Ma Z, Huang J (2016) DELLA proteins promote anthocyanin biosynthesis via sequestering MYBL2 and JAZ suppressors of the MYB/bHLH/WD40 complex in Arabidopsis thaliana. Mol Plant 9:711–721

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youssef A, Laizet Y, Block MA, Marecha E, Alcaraz JP, Larson TR, Pontier D, Gaffe J, Kuntz M (2010) Plant lipid-associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J 61:436–445

    Article  CAS  PubMed  Google Scholar 

  • Yousuf PY, Ahmad A, Ganie AH, Sareer O, Krishnapriya V, Aref IM, Iqbal M (2017) Antioxidant response and proteomic modulations in Indian mustard grown under salt stress. Plant Growth Regul 81:31–50

    Article  CAS  Google Scholar 

  • Yu HD, Yang XF, Chen ST, Wang YT, Li JK, Shen Q, Liu XL, Guo FQ (2012) Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis. PLoS Genet 8:e1002669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeevaart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39:439–473

    Article  CAS  Google Scholar 

  • Zhu D, Scandalios JG (1994) Differential accumulationof manganese-superoxide dismutase transcripts in maize in response to abscisic acid and high osmoticum. Plant Physiol 106:173–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to give our great thanks to Mrs. Li-Xia Ma for technical assistance, and the Arabidopsis Biological Resource Center at The Ohio State University for providing the T-DNA insertion line. This work was supported by the National Natural Science Foundation of China (Grant Number 31560077) and the National Key Research and Development Program of China (Grant Number 2017YFD0301605).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 4452 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, M., Lv, X., Zhou, Y. et al. High anthocyanin accumulation in an Arabidopsis mutant defective in chloroplast biogenesis. Plant Growth Regul 87, 433–444 (2019). https://doi.org/10.1007/s10725-019-00481-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-019-00481-7

Keywords

Navigation