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Light and dark modulation of chlorophyll biosynthetic genes in response to temperature

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Abstract

Temperature and light significantly influence chloroplast development and chlorophyll biosynthesis. To understand the mechanism of the modulation of chlorophyll biosynthesis, the levels of transcripts and proteins of many enzymatic steps of tetrapyrrole biosynthesis in wheat and cucumber were simultaneously examined. The effect of low (chill-stress) as well as high (heat-stress) temperatures on dark- and light-grown seedlings was monitored. The protochlorophyllide oxidoreductase (POR) content was greatly reduced in response to light in control and heat-stressed seedlings. However, the POR level was not reduced in light-exposed chill-stressed seedlings. The genes for glutamate semialdehyde aminotransferase (gsa; cucumber), glutamyl-tRNA reductase (GluTR; cucumber), 5-aminolevulinic acid dehydratase (Ala D; cucumber and wheat) and for a subunit of Mg-chelatase (Chl I; wheat) showed a reduced expression in cold stress compared to controls and heat-stress conditions. Although expression of the ferrochelatase gene (Fch) and geranylgeranyl reductase gene (Chl P) was upregulated in light, they were downregulated by both chill- and heat-stress. Interestingly, gsa and uroporphyrinogen decarboxylase gene (UroD) and gene product abundance was stimulated by light and heat-stress implying the presence of both light and heat-inducible elements in their promoters. This observation corroborates with the previous report of increased enzymatic activity of UroD in heat-stressed cucumber seedlings. The gsa and Uro D may play an important role in tolerance of the greening process of plants to heat-stress.

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Abbreviations

ALA:

5-Aminolevulinicacid

ALAD:

5-Aminolevulinate dehydratase

Chlide:

Chlorophyllide

CPO:

Coproporphyrinogen oxidase

GluTR:

Glutamyl-tRNA reductase

GSAT:

Glutamate-1-semialdehyde aminotransferase

PBG:

Porphobilinogen

proto:

Protoporphyrin IX

Pchlide:

Protochlorophyllide

POR:

Protochlorophyllide oxidoreductase

UroD:

Uroporphyrinogen decarboxylase

References

  • Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH: protochlorophyllide oxidoreductase A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108:1505–1517

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guannidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Eckhardt U, Grimm B, Hortensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14

    Article  PubMed  CAS  Google Scholar 

  • Feierabend J (1977) Capacity for chlorophyll synthesis in heat-bleached 70S ribosome-deficient rye leaves. Planta 135:83–88

    Article  CAS  Google Scholar 

  • Feierabend J, Mikus M (1976) Occurrence of a high temperature sensitivity of chloroplast ribosome formation in several higher plants. Plant Physiol 59:863–867

    Article  Google Scholar 

  • Feierabend J, Schrader-Reichhardt U (1976) Biochemical differentiation of plastids and other organelles in rye leaves with a high-temperature-induced deficiency of plastid ribosomes. Planta 129:133–145

    Article  CAS  Google Scholar 

  • Gibson LC, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M, Hunter CN (1996) A putative Mg chelatase subunit from Arabidopsis thaliana cv. C24. sequence and transcript analysis of the gene, import of the protein into chloroplasts, and in situ localization of the transcript and protein. Plant Physiol 111:61–71

    Article  PubMed  CAS  Google Scholar 

  • Griffiths WT (1978) Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem J 174:681–692

    PubMed  CAS  Google Scholar 

  • Grimm B (1998) Novel insights in the control of tetrapyrrole metabolism of higher plants. Curr Opin Plant Biol 1:245–250

    Article  PubMed  CAS  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    CAS  Google Scholar 

  • Hodgins R, van Huystee RB (1986a) 5-aminolevulinic acid metabolism in chill-stressed maize (Zea mays L.). J Plant Physiol 126:257–268

    CAS  Google Scholar 

  • Hodgins R, van Huystee RB (1986b) Porphyrin metabolism in chill-stressed maize (Zea mays L.). J Plant Physiol 125:325–336

    CAS  Google Scholar 

  • Holtorf H, Apel K (1996) Transcripts of the two NADPH-protochlorophyllide oxidoreductase genes PorA and PorB are differentially degraded in etiolated barley seedlings. Plant Mol Biol 31:387–392

    Article  PubMed  CAS  Google Scholar 

  • Jensen PE, Willows RD, Petersen BL, Vothknecht UC, Stummann BM, Kannangara CG, von Wettstein D, Henningsen KW (1996) Structural genes for Mg-chelatase subunits in barley: Xantha-f, -g, and -h. Mol Gen Genet 250:383–394

    PubMed  CAS  Google Scholar 

  • Jilani A, Kar S, Bose S, Tripathy BC (1996) Regulation of the carotenoid content and chloroplast development by levulinic acid. Physiol Plant 96:139–145

    Article  CAS  Google Scholar 

  • Kannangara CG, Vothknecht UC, Hansson M, von Wettstein D (1997) Magnesium chelatase: association with ribosome and mutant complementation studies identify barley subunit Xantha-G as a functional counterpart of Rhodobacter subunit BchD. Mol Gen Genet 254:85–92

    Article  PubMed  CAS  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Mohapatra A, Tripathy BC (2002) Detection of proto in envelope membranes of pea chloroplasts. Biochem Biophys Res Commun 299:751–754

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu S, Kojima K, Igasaki T, Azumi Y, Shinihara K (2001) Inhibition of light-independent synthesis of chlorophyll in pine cotyledons at low temperature. Plant Cell Physiol 42:868–872

    Article  PubMed  CAS  Google Scholar 

  • Papenbrock J, Pfundel E, Mock HP, Grimm B (2000) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J 22:155–64

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ (1997) Recent progress in porphyrin and chlorophyll biosynthesis. Photochem Photobiol 65:492–516

    Article  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 

  • Rebeiz CA, Parham R, Fasoula DA, Ioannides IM (1994) Chlorophyll a biosynthetic heterogeneity. In: Chadwick DJ, Ackrill K (eds) Biosynthesis of tetrapyrrole pigments. Ciba Symposium 180, Wiley, New York, pp 177–193

  • Reinbothe C, Apel K, Reinbothe S (1995) A light-induced protease from barley plastids degrades NADPH: protochlorophyllide oxidoreductase complexed with chlorophyllide. Mol Cell Biol 15:6206–6212

    PubMed  CAS  Google Scholar 

  • Reinsberg D, Ottman K, Booth PJ, Paulsen H (2001) Effects of chlorophyll a, chlorophyll b and xanthophylls on the in vitro assembly kinetics of major light-harvesting chlorophyll a/b complex LHC IIb. J Mol Biol 308:59–67

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sundqvist C, Dahlin C (1997) With chlorophyll from prolamellar bodies to light-harvesting complexes. Physiol Plant 100:748–759

    Article  CAS  Google Scholar 

  • Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  PubMed  CAS  Google Scholar 

  • Tewari AK, Tripathy BC (1999) Acclimation of chlorophyll biosynthetic reactions to temperature stress in cucumber (Cucumis sativus L.). Planta 208:431–437

    Article  CAS  Google Scholar 

  • Van Hasselt PR, Strikwerda JT (1976) Pigment degradation discs of the thermophilic Cucumis sativus as affected by light, temperature, sugar application and inhibitors. Plant Physiol 37:253–257

    Article  Google Scholar 

  • Van Huystee RB, Hodgins RR (1989) Chlorophyll synthesis from protochlorophyllide in chill stressed maize (Zea mays L.). J Exp Bot 40:431–435

    Article  Google Scholar 

  • Von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057

    Article  PubMed  Google Scholar 

  • Welburn AR, Lichtenthaler H (1984) Formula and program to determine total carotenoids and Chla and b of leaf extracts in different solvents. In: Sybesma C (ed) Advances in photosynthesis research, vol II. Martinus Nijoff/Dr. W. Junk Publishers. The Hague, pp 9–12

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Acknowledgements

This research work was supported by a grant (BTPR1778/BRB/15/176/1999) from the Department of Biotechnology, Government of India, New Delhi to BCT. We thank C.G. Kannangara (Washington State University, USA) and W.T. Griffiths (University of Bristol, UK) for the gift of barley antibodies for glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase and wheat antibody for POR, used for Western-blot analysis.

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Correspondence to Baishnab C. Tripathy.

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Mohanty, S., Grimm, B. & Tripathy, B.C. Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224, 692–699 (2006). https://doi.org/10.1007/s00425-006-0248-6

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