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A new gun mutant of oilseed rape with a reduced porphyrin flux through Mg-chelatase

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Abstract

Plastid-to-nucleus retrograde signaling coordinates the expression of nuclear photosynthetic genes with the developmental and functional state of the plastid. These signals are essential not only for coordinating the expression of photosynthetic genes both in the plastome and nuclear genome, but also for plants to respond optimally to environmental stress. In the present study, we found that the expression of the nuclear genes that encode plastid and non-plastid photosynthesis-related proteins was still maintained or slightly higher in cr3529, a chlorophyll deficient mutant of oilseed rape that possesses an arrested development of chloroplasts, suggesting that the expression of photosynthesis-related nuclear genes was uncoupled from the normal dependence on the developmental state of the chloroplast in cr3529. When the development of the plastid in cr3529 and the wild type was completely inhibited by lincomycin, much higher expression of photosynthesis-related nuclear genes was observed in cr3529, suggesting that the genomes uncoupled (gun) phenotype of cr3529 is even more apparent than under normal growth conditions. Lincomycin treatment also derepressed the expression of plastid genes in cr3529. The determination of porphyrin flux through Mg-chelatase showed that the content of protoporphyrin IX and Mg-protoporphyrin decreased in cr3529. The obvious gun phenotype of cr3529 under normal growth conditions and the pattern of tetrapyrrole metabolism in cr3529 suggest that it is a new gun mutant that could be used to study the regulation of the expression of nuclear and plastid genes by plastid-to-nucleus retrograde signaling under more physiological conditions and the mechanism of plant stress responses mediated by plastid signals.

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Abbreviations

Chl:

Chlorophyll

cr3529 :

A chlorophyll-reduced seedling obtained from the Brassica napus inbred line 3529

gun mutant:

Genomes uncoupled mutant

Lin:

Lincomycin

MgProto:

Mg-protoporphyrin

Pchlide:

Prochlorophyllide

Proto IX:

Protoporphyrin IX

References

  • Ankele E, Kindgren P, Pesquet E, Strand Å (2007) In vivo visualization of Mg-Protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 19:1964–1979

    Article  PubMed  CAS  Google Scholar 

  • Bräutigam K, Dietzel L, Pfannschmidt T (2007) Plastid-nucleus communication: anterograde and retrograde signalling in the development and function of plastids. In: Bock R (ed) Cell and molecular biology of plastids, vol 19. Springer, Berlin, pp 409–455

    Chapter  Google Scholar 

  • Fernández AP, Strand Å (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513

    Article  PubMed  Google Scholar 

  • Gray JC, Sullivan JA, Wang J-H, Jerome CA, MacLean D (2003) Coordination of plastid and nuclear gene expression. Philos Trans Roy Soc B 358:135–145

    Article  CAS  Google Scholar 

  • Hedtke B, Wagner I, Börner T, Hess WR (1999) Inter-organellar crosstalk in higher plants: impaired chloroplast development affects mitochondrial gene and transcript levels. Plant J 19:635–643

    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 A, Nott A, Mockler TC, Hong FX, 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 

  • Lee HJ, Ball MD, Parham R, Rebeiz CA (1992) Chloroplast biogenesis 65: enzymic conversion of protoporphyrin IX to Mg-protoporphyrin IX in a subplastidic membrane fraction of cucumber etiochloroplasts. Plant Physiol 99:1134–1140

    Article  PubMed  CAS  Google Scholar 

  • Leister D (2003) Chloroplast research in the genomic age. Trends Plant Sci 19:47–56

    CAS  Google Scholar 

  • Mochizuki N, Susek R, Chory J (1996) An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol 112:1465–1469

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A (2008) The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabidopsis. Proc Natl Acad Sci USA 105:15184–15189

    Article  PubMed  CAS  Google Scholar 

  • Moulin M, McCormac AC, Terry MJ, Smith AG (2008) Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protoporphyrin IX accumulation. Proc Natl Acad Sci USA 105:15178–15183

    Article  PubMed  CAS  Google Scholar 

  • Mulo P, Pursiheimo S, Hou CX, Tyystjärvi T, Aro E-M (2003) Multiple effects of antibiotics on chloroplast and nuclear gene expression. Funct Plant Biol 30:1097–1103

    Article  CAS  Google Scholar 

  • Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8:87–99

    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 

  • Papenbrock J, Mock HP, Kruse E, Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208:264–273

    Article  CAS  Google Scholar 

  • Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signaling to the nucleus and beyond. Trends Plant Sci 13:602–609

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Qin T, Fu J, Zhang N, Du L (2006) Comparative studies of senescence-related enzymes in the cotyledon of chlorophyll b-deficient mutant and its wild type oilseed rape during senescence. Plant Sci 171:293–299

    Article  PubMed  CAS  Google Scholar 

  • Rebeiz CA, Mattheis JR, Smith BB, Rebeiz CC, Dayton DF (1975) Chloroplast biogenesis. Biosynthesis and accumulation of protochlorophyll by isolated etioplasts and developing chloroplasts. Arch Biochem Biophys 171:549–567

    Article  PubMed  CAS  Google Scholar 

  • Rodermal S (2001) Pathways of plastid-to nucleus signaling. Trends Plant Sci 6:471–478

    Article  Google Scholar 

  • Rodermal S, Park S (2003) Pathways of intracellular communication: tetrapyrrole and plastid-to nucleus signaling. BioEssays 25:631–636

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sun J-Y, Zhang N-H, Du L-F (2007) Chlorophyll biosynthesis in a chlorophyll b-deficient oilseed rape mutant cr3529. Acta Bot Boreal-Occident Sin 27:1962–1966

    CAS  Google Scholar 

  • Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799

    Article  PubMed  CAS  Google Scholar 

  • Wang T, Zhang N, Du L (2005) Isolation of functional total RNA with high quality and yield from Ginkgo biloba leaves. Biotechnol Lett 27:629–633

    Article  PubMed  Google Scholar 

  • Whelan J, Smith MK, Meijer M, Yu JW, Badger MR, Price CD, Day DA (1995) Cloning of an additional cDNA for the alternative oxidase in tobacco. Plant Physiol 107:1469–1470

    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 

  • 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 

  • Zhao Y, Wang ML, Zhang YZ, Du LF, Pan T (2000) A chlorophyll-reduced seedlings mutant in oilseed rape, Brassica napus, for utilization in F1 hybrid production. Plant Breed 119:131–135

    Article  Google Scholar 

  • Zhu YS, Kung SD, Bogorad L (1985) Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol 79:372–376

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Jim Whelan and Dr. Yusheng Zhu for generously providing us Aox1 and Lhcb1, respectively, Dr. Naiyan Zeng and Dr. Xiaoping Gou for correction to the language. This work was supported by the China National Nature Science Foundation 30170500 and 30270124, and the National Basic Research 973 Program 2009CB118502.

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Authors and Affiliations

  1. Key Laboratory of Bio-resource and Bio-environment of the Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, 610064, China

    Nian-Hui Zhang, Yun Zhao, Hou-Guo Liang, Jie-Yin Sun & Lin-Fang Du

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  1. Nian-Hui Zhang
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  2. Yun Zhao
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  3. Hou-Guo Liang
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  4. Jie-Yin Sun
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  5. Lin-Fang Du
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Correspondence to Lin-Fang Du.

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Communicated by J. W. Sadowski.

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Zhang, NH., Zhao, Y., Liang, HG. et al. A new gun mutant of oilseed rape with a reduced porphyrin flux through Mg-chelatase. Acta Physiol Plant 35, 75–84 (2013). https://doi.org/10.1007/s11738-012-1049-0

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  • DOI: https://doi.org/10.1007/s11738-012-1049-0

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