Advertisement

High anthocyanin accumulation in an Arabidopsis mutant defective in chloroplast biogenesis

  • Meijia Wu
  • Xiaolin Lv
  • Yingjie Zhou
  • Yongjun Zeng
  • Dong LiuEmail author
Original paper
  • 16 Downloads

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.

Keywords

Arabidopsis AtDPG1 Anthocyanin ABA Oxidative stress 

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2019_481_MOESM1_ESM.doc (4.3 mb)
Supplementary material 1 (DOC 4452 KB)

References

  1. 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 78:307–323CrossRefGoogle Scholar
  2. 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 277:2006–2011CrossRefGoogle Scholar
  3. Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393CrossRefGoogle Scholar
  4. 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 138:27–34CrossRefGoogle Scholar
  5. Burgess D, Taylor W (1987) Chloroplast photooxidation affects accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170:520–527CrossRefGoogle Scholar
  6. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9CrossRefGoogle Scholar
  7. 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 85:425–435CrossRefGoogle Scholar
  8. 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 68:223–230CrossRefGoogle Scholar
  9. 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 58:991–999CrossRefGoogle Scholar
  10. 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 61:3773–3786CrossRefGoogle Scholar
  11. 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 55:940–953CrossRefGoogle Scholar
  12. 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 113:10708–10713CrossRefGoogle Scholar
  13. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415CrossRefGoogle Scholar
  14. 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 9:12–29CrossRefGoogle Scholar
  15. 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 56:916–927CrossRefGoogle Scholar
  16. Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391CrossRefGoogle Scholar
  17. 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 153:488–496CrossRefGoogle Scholar
  18. 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 53:814–827CrossRefGoogle Scholar
  19. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780CrossRefGoogle Scholar
  20. 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 117:217–224CrossRefGoogle Scholar
  21. 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 22:87–95CrossRefGoogle Scholar
  22. Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense response. Plant Cell 8:1773–1791CrossRefGoogle Scholar
  23. Hernandez JA, Olmos E, Corpas FJ, Sevilla F, del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167CrossRefGoogle Scholar
  24. 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 79:275–285CrossRefGoogle Scholar
  25. Holton T, Cornish E (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083CrossRefGoogle Scholar
  26. 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 173:27–38CrossRefGoogle Scholar
  27. Huang X, Zhang X, Yang S (2009) A novel chloroplast-localized protein EMB1303 is required for chloroplast development in Arabidopsis. Cell Res 19:1205–1216CrossRefGoogle Scholar
  28. Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28CrossRefGoogle Scholar
  29. 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 42:1265–1273CrossRefGoogle Scholar
  30. Jiang M, Zhang J (2002) Role of abscisic acid in water stress induced antioxidant defense in leaves of maize seedlings. Free Rad Res 36:1001–10l0l5CrossRefGoogle Scholar
  31. 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–S225CrossRefGoogle Scholar
  32. 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 21:1781–1797CrossRefGoogle Scholar
  33. 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 144:1391–1406CrossRefGoogle Scholar
  34. 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 213:101–108CrossRefGoogle Scholar
  35. Larkindale J, Knight MR (2002) Protection against heat stress induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695CrossRefGoogle Scholar
  36. 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 19:731–749CrossRefGoogle Scholar
  37. Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354:110–116CrossRefGoogle Scholar
  38. Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592CrossRefGoogle Scholar
  39. 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:srep25742CrossRefGoogle Scholar
  40. 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 219–220:61–68CrossRefGoogle Scholar
  41. 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 55:945–967CrossRefGoogle Scholar
  42. Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138:1083–1096CrossRefGoogle Scholar
  43. 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 61:2433–2445CrossRefGoogle Scholar
  44. 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 20:3148–3162CrossRefGoogle Scholar
  45. Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759CrossRefGoogle Scholar
  46. 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 35:388–404CrossRefGoogle Scholar
  47. 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 113:1437–1445CrossRefGoogle Scholar
  48. 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 182:102–115CrossRefGoogle Scholar
  49. 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 56:705–716CrossRefGoogle Scholar
  50. 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 5:11–24CrossRefGoogle Scholar
  51. 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 49:981–994CrossRefGoogle Scholar
  52. Steyn WJ, Wand SJE, Holcroft DM, Jacobs G (2002) Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytol 155:349–361CrossRefGoogle Scholar
  53. 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 50:660–667CrossRefGoogle Scholar
  54. 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 139:1840–1852CrossRefGoogle Scholar
  55. 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 9:1395–1405CrossRefGoogle Scholar
  56. Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210CrossRefGoogle Scholar
  57. Winkel-Shirley B (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493CrossRefGoogle Scholar
  58. 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 9:711–721CrossRefGoogle Scholar
  59. 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 127:315–323CrossRefGoogle Scholar
  60. 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 61:436–445CrossRefGoogle Scholar
  61. 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 81:31–50CrossRefGoogle Scholar
  62. 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:e1002669CrossRefGoogle Scholar
  63. Zeevaart JAD, Creelman RA (1988) Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39:439–473CrossRefGoogle Scholar
  64. Zhu D, Scandalios JG (1994) Differential accumulationof manganese-superoxide dismutase transcripts in maize in response to abscisic acid and high osmoticum. Plant Physiol 106:173–178CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.College of Agronomy/Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of EducationJiangxi Agricultural UniversityNanchangChina

Personalised recommendations