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Plastid-signalling-mediated anthocyanin accumulation in mature Arabidopsis rosettes

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Abstract

Genetic and physiological studies have revealed evidences for multiple signaling pathways by which the plastid exerts retrograde control over photosynthesis-associated-nuclear-genes (PhANGs). Recently, more and more studies showed that plastid signals affected more cellular processes other than PhANGs repression. Previous reports indicated that the herbicide norflurazon (NF)-derived signals, sugar signals and plastid gene expression (PGE)-derived signals all regulated anthocyanin accumulation and early anthocyanin biosynthesis gene expression in newly-germinated seedlings. In the research, we found that these signals also work as well for anthocyanin biosynthesis genes in mature Arabidopsis seedlings. Sugar/PGE signals doubled leaf total anthocyanins within 48 h (accumulated at the base of petiole), while NF signals induced a little anthocyanin accumulation (about 30 % and invisible to the naked eye). The plastid hexokinase (pHXK) participates in sugar/PGE signalling, while the plastid Genomes uncoupled protein 1 (GUN1) and the nuclear ABA-insensitive transcription factor 4 (ABI4) are involved in both sugar/PGE signalling and NF-derived signalling.

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References

  • Chattopadhyay S, Puente P, Deng XW, Wei N (1998) Combinatorial interaction of light-responsive elements plays a critical role in determining the response characteristics of light-regulated promoters in Arabidopsis. Plant J 15:69–77

    Article  PubMed  CAS  Google Scholar 

  • Cheng J, He CX, Zhang ZW, Xu F, Zhang DW, Wang X, Yuan S, Lin HH (2011) Plastid signals confer Arabidopsis tolerance to water stress. Z Naturforsch 66c:47–54

    Google Scholar 

  • Cominelli E, Gusmaroli G, Allegra D, Galbiati M, Wade HK, Jenkins GI, Tonelli C (2008) Expression analysis of anthocyanin regulatory genes in response to different light qualities in Arabidopsis thaliana. J Plant Physiol 165:886–894

    Article  PubMed  CAS  Google Scholar 

  • Cottage A, Mott EK, Kempster JA, Gray JC (2010) The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J Exp Bot 61:3773–3786

    Article  PubMed  CAS  Google Scholar 

  • Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17

    Article  PubMed  CAS  Google Scholar 

  • Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Mérillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140:499–511

    Article  PubMed  CAS  Google Scholar 

  • Dubos C, Le Gourrierec J, 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  PubMed  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  PubMed  CAS  Google Scholar 

  • Hoth S, Niedermeier M, Feuerstein A, Hornig J, Sauer N (2010) An ABA responsive element in the AtSUC1 promoter is involved in the regulation of AtSUC1 expression. Planta 232:911–923

    Article  PubMed  CAS  Google Scholar 

  • Jeong SW, Das PK, Jeoung SC, Song JY, Lee HK, Kim YK, Kim WJ, Park YI, Yoo SD, Choi SB, Choi G, Park YI (2010) Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 154:1514–1531

    Article  PubMed  CAS  Google Scholar 

  • Jung HS, Chory J (2010) Signaling between chloroplasts and the nucleus: can a systems biology approach bring clarity to a complex and highly regulated pathway? Plant Physiol 152:453–459

    Article  PubMed  CAS  Google Scholar 

  • Kim JS, Lee BH, Kim SH, Ok KH, Cho KY (2006) Response to environmental and chemical signals for anthocyanin biosynthesis in nonchlorophyllous corn (Zea mays L.) leaf. J Plant Biol 49:16–25

    Article  CAS  Google Scholar 

  • Kindgren P, Eriksson MJ, Benedict C, Mohapatra A, Gough SP, Hansson M, Kieselbach T, Strand A (2011) A novel proteomic approach reveals a role for Mg-protoporphyrin IX in response to oxidative stress. Physiol Plant 141:310–320

    Article  PubMed  CAS  Google Scholar 

  • Kleine T, Voigt C, Leister D (2009) Plastid signalling to the nucleus: messengers still lost in the mists? Trends Genet 25:185–192

    Article  PubMed  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mochler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    Article  PubMed  CAS  Google Scholar 

  • Kubasek WL, Shirley BW, McKillop A, Goodman HM, Briggs W, Ausubel FM (1992) Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings. Plant Cell 4:1229–1236

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55:1221–1230

    Article  PubMed  CAS  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 55:954–967

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci 98:2053–2058

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci 105:15178–15183

    Article  Google Scholar 

  • Moulin M, McCormac AC, Terry MJ, Smith AG (2008) The steady state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci 105:15184–15189

    Article  Google Scholar 

  • Neff MM, Chory J (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 118:27–35

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Oelmüller R, Mohr H (1986) Photooxidative destruction of chloroplast and its consequences for expression of nuclear genes. Planta 167:106–113

    Article  Google Scholar 

  • Papenbrock J, Mishra S, Mock HP, Kruse E, Schmidt EK, Petersmann A, Braun HP, Grimm B (2001) Impaired expression of the plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic phenotype of transformed tobacco plants. Plant J 28:41–50

    Article  PubMed  CAS  Google Scholar 

  • Pelletier MK, Burbulis IE, Shirley BW (1999) Disruption of specific flavonoid genes enhances the accumulation of flavonoid enzymes and end-products in Arabidopsis seedlings. Plant Mol Biol 40:45–54

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2010) Plastidial retrograde signalling – a true “plastid factor’’ or just metabolite signatures? Trends Plant Sci 15:427–435

    Article  PubMed  CAS  Google Scholar 

  • Quattrocchio F, Baudry A, Lepiniec L, Grotewold E (2006) The regulation of flavonoid biosynthesis. In: Grotewold E (ed) The science of flavonoids. Springer, Berlin, pp 97–122

    Chapter  Google Scholar 

  • Ren J, Sun L, Wang C, Zhao S, Leng P (2011) Expression analysis of the cDNA for magnesium chelatase H subunit (CHLH) during sweet cherry fruit ripening and under stress conditions. Plant Growth Regul 63:301–307

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cau Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    Article  PubMed  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Strand Å, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Wade HK, Bibikova TN, Valentine WJ, Jenkins GI (2001) Interactions within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J 25:675–685

    Article  PubMed  CAS  Google Scholar 

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  PubMed  CAS  Google Scholar 

  • Woodson JD, Perez-Ruiz JM, Chory J (2011) Heme Synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Curr Biol 21:897–903

    Article  PubMed  CAS  Google Scholar 

  • Yang YN, Qi M, Mei CS (2004) Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J 40:909–919

    Article  PubMed  CAS  Google Scholar 

  • Zhang NH, Wei ZQ, He JX, Du LF, Liang HG (2004) An efficient and economic method for preparation of high quality plant RNA. Prog Biochem Biophys 31:947–950

    CAS  Google Scholar 

  • Zhang ZW, Yuan S, Xu F, Yang H, Zhang NH, Cheng J, Lin HH (2010) The plastid hexokinase pHXK: a node of convergence for sugar and plastid signals in Arabidopsis. FEBS Lett 584:3573–3579

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZW, Yuan S, Feng H, Xu F, Cheng J, Shang J, Zhang DW, Lin HH (2011a) Transient accumulation of Mg-protoporphyrin IX regulates expression of PhANGs—new evidence for a signalling role of tetrapyrroles in mature Arabidopsis plants. J Plant Physiol 168:714–721

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZW, Yuan S, Xu F, Yang H, Chen YE, Yuan M, Xu MY, Xue LW, Xu XC, Lin HH (2011b) Mg-protoporphyrin, heme and sugar signals double cellular total RNAs against herbicide and high-light-derived oxidative stress. Plant, Cell Environ 34:1031–1042

    Article  CAS  Google Scholar 

  • Zhang ZW, Cheng J, Xu F, Yuan M, Du JB, Shang J, Wang Y, Du L, Li ZL, Yuan S (2011c) Mammal cells double their total RNAs against diabetes, ischemia reperfusion and malaria-induced oxidative stress. Mol Med 17:533–541

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Adriana Racolta (University of Arizona, Tucson, AZ, USA) for language polishing and Prof. Joanne Chory (The Salk Institute, La Jolla, USA) for gun1 seeds. This work was supported by the National Nature Science Foundation of China (31070210, 91017004, 30970214 and 30800071), the National Key Basic Research ‘973’ Program of China (2009CB118500), the Doctoral Foundation of the Ministry of Education (20110181110059), the Sichuan Nature Science Foundation (2010JQ0080) and the Chengdu Application Foundation Project (11DXYB097JH-027).

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Authors and Affiliations

  1. Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Science, Sichuan University, Chengdu, 610064, China

    Jian Cheng, Shu Yuan, Zhong-Wei Zhang, Feng Zhu, He Tang, Fei Xu, Huang-Fan Xie & Hong-Hui Lin

  2. College of Resources and Environmental Sciences, Sichuan Agriculture University, Chengdu, 611130, China

    Shu Yuan & Zhong-Wei Zhang

  3. Sichuan College of Education, Chengdu, 610041, China

    Hong Feng

  4. State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, 610065, China

    Wei-Lin Xu & Hong-Hui Lin

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  1. Jian Cheng
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Correspondence to Hong-Hui Lin.

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Jian Cheng and Shu Yuan have contributed equally to this work.

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Cheng, J., Yuan, S., Zhang, ZW. et al. Plastid-signalling-mediated anthocyanin accumulation in mature Arabidopsis rosettes. Plant Growth Regul 68, 223–230 (2012). https://doi.org/10.1007/s10725-012-9710-6

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  • DOI: https://doi.org/10.1007/s10725-012-9710-6

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