Abstract
During early seedling development of oil seed plants, the transition from lipid based heterotrophic to photoautotrophic carbohydrate metabolism is accompanied with a biphasic control of the chloroplast antioxidant system. In continuous light, organellar peroxiredoxins (Prx) and thylakoid-bound ascorbate peroxidase (tAPx) are activated early in seedling development, while stromal ascorbate peroxidase (sAPx), Cu/Zn-superoxide dismutase-2 (Csd2) and monodehydroascorbate reductase (MDHAR) and the cytosolic peroxiredoxins PrxIIB, PrxIIC and PrxIID are fully activated between 2.5 and 3 days after radicle emergence (DARE). Discontinuous light synchronized the expression of chloroplast antioxidant enzymes, but defined diurnally specific typeII-Prx-patterns in the cytosol and initiated chloroplast senescence around 2.5 DARE. Carbohydrate feeding uncoupled sAPx expression from the light pattern. In contrast, sucrose-feeding did not significantly impact on Prx transcript amounts. It is concluded that upon post-germination growth Prxs are activated endogenously to provide early antioxidant protection, which is supported by the Halliwell–Asada-Cycle, whose expressional activation depends on metabolic signals provided only later in development or in day-night-cycles.
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Abbreviations
- cDNA:
-
copy DNA
- Csd2:
-
CuZn-superoxide dismutase 2
- DARE:
-
Days after radicle emergence
- F M :
-
Maximum fluorescence
- F S :
-
Steady state fluorescence
- fw:
-
Fresh weight
- GUS:
-
Glucuronidase
- ICL:
-
Isocitrate lyase
- MDHAR:
-
Monodehydroascorbate reductase
- NBT:
-
Nitroblue tetrazolium
- NPQ:
-
Non-photochemical quenching
- Prx:
-
Peroxiredoxin
- ΦPSII :
-
Quantum yield of photosystem II
- qP:
-
Photochemical quenching
- ROS:
-
Reactive oxygen species
- RT-PCR:
-
Reverse transcription followed by polymerase chain reaction
- sAPx:
-
Stromal ascorbate peroxidase
- tAPx:
-
Thylakoid-bound ascorbate peroxidase
References
Abel S, Theologis A (1998) Transient gene expression in protoplasts of Arabidopsis thaliana. Methods Mol Biol 82:209–217
Appelquist L-Å, Boynton JE, Stumpf PK, von Wettstein D (1968) Lipid biosynthesis in relation to chloroplast development in barley. J Lipid Res 9:425–436
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Baier M, Bilger W, Wolf R, Dietz KJ (1996) Photosynthesis in the basal growing zone of barley leaves. Photosynth Res 49:169–181
Baier M, Dietz K-J (1997) The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J 12:179–190
Baier M, Dietz K-J (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119:1407–1414
Baier M, Dietz K-J (2005) Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology. J Exp Bot 56:1449–1462
Baier M, Noctor G, Foyer CH, Dietz KJ (2000) Antisense suppression of 2-Cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol 124:823–832
Brehélin C, Meyer EH, de Souris J-P, Bonnard G, Meyer Y (2003) Resemblance and dissemblance of Arabidopsis type II peroxiredoxins: similar sequences for divergent gene expression, protein localization, and activity. Plant Physiol 132:2045–2057
Conway LJ, Poethig RS (1997) Mutations of Arabidopsis thaliana that transform leaves into cotyledons. Proc Natl Acad Sci USA 94:10209–10214
Dekkers BJ, Schuurmans JA, Smeekens SCM (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588
Dekker JP, Boekema EJ (2005) Supramolecular ogranization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39
Dietz K-J, Jakob S, Oelze M-L, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I (2006) The function of peroxiredoxin in plant organelle redox metabolism. J Exp Bot 57:1697–1709
Eastmond PJ, Graham IA (2001) Re-examining the role of the glyoxylate cycle in oilseeds. Trends Plant Sci 6:72–77
Eastmond PJ, Germain V, Lange PR, Bryce JH, Smith SM, Graham IA (2000) Post-germinative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proc Nat Acad Sci USA 97:5669–5674
Engels A, Kahmann U, Ruppel HG, Pistorius EK (1997) Isolation, partial characterization and localization of a dihydrolipoamide dehydrogenase from the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1340:33–44
Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz K-J (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280:12168–12180
Foyer CH, Rowell J, Walker D (1983) Measurements of the ascorbate content of spinach leaf protoplasts and chloroplasts during illumination. Planta 157:239–244
Girotti AW (1985) Mechanism of lipid peroxidation. J Free Radicals Biol Med 1:87–95
Hideg E, Ogawa K, Kalai T, Hideg K (2001) Singlet oxygen imaging in Arabidopsis thaliana leaves under photoinhibition by excess photosynthetically active radiation. Physiol Plant 112:10–14
Holdsworth M, Kurup S, McKibbin R (1999) Molecular and genetic mechanisms regulating the transition from embryo development to germination. Trends Plant Sci 4:275–280
Horling F, König J, Dietz KJ (2002) Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. Plant Physiol Biochem 40:491–499
Horling F, Lamkemeyer P, König J, Finkemeier I, Baier M, Kandlbinder A, Dietz KJ (2003) Divergent light-, ascorbate- and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis thaliana. Plant Physiol 131:317–325
Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from oxidative stress. Proc Natl Acad Sci USA 100:4921–4926
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322
Ishiguro S, Nakamura K (1992) The nuclear factor SP8BF binds to the 5′-upstream regions of three different genes coding for major proteins of sweet potato tuberous roots. Plant Mol Biol 18:97–108
Jang J-C, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
König J, Baier M, Horling F, Kahmann U, Harris G, Schürmann P, Dietz K-J (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 99:5738–5743
Krapp A, Hofmann B, Schafer C, Stitt M (1993) Regulation of the expression of rbcS and other photosynthesis genes by carbohydrates: a mechanism for the “sink regulation” of photosynthesis. Plant J 3:817–828
Lamkemeyer P, Laxa M, Collin V, Li WX, Finkemeier I, Schöttler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, Kandlbinder A, Weis E, Miginac-Maslow M, Dietz KJ (2006) PrxQ of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968–981
Maly FE, Nakamura M, Gauchat JF, Urwyler A, Walker G, Dahinden CA, Cross AR, Jones OTG, Weck AL (1989) Superoxide-dependent nitroblue tetrazolium reduction and expression of cytochrome b 245 components by human tonsillar lymphocytes and B cell lines. J Immunol 142:1260–1267
Meskauskiene R, Apel K (2002) Interaction of FLU, a negative regulator of tetrapyrrole biosynthesis, with the glutamyl-tRNA reductase requires the tetratricopeptide repeat domain of FLU. FEBS Lett 532:27–30
Müller-Moulé P, Havaux M, Niyogi KK (2003) Zeaxanthin deficiency enhances the high light sensitivity of an ascorbate-deficient mutant of Arabidopsis. Plant Physiol 133:748–760
Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502
Noctor G, Dutilleul C, De Pape R, Foyer CH (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J Exp Bot 55:49–57
Penfield S, Rylott EL, Gilday AD, Graham S, Larson TR, Graham IA (2004) Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires phosphoenolpyruvate carboxykinase1. Plant Cell 16:2705–2718
Pinfield-Wells H, Rylott EL, Gilday AD, Graham S, Job K, Larson TR, Graham IA (2005) Sucrose rescues seedling establishment but not germination of Arabidopsis mutants disrupted in peroxisomal fatty acid catabolism. Plant J 43:861–872
Price J, Li T-C, Kang SG, Na KJ, Jang J-C (2003) Mechanisms of glucose signalling during germination of Arabidopsis. Plant Physiol 132:1424–1438
Puntarulo S, Sánchez RA, Boveris A (1988) Hydrogen peroxide metabolism in soybean embyonic axes at the onset of germination. Plant Physiol 86:626–630
Rodriguez AA, Grunberg KA, Talesisnik EL (2002) Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf expansion. Plant Physiol 129:1627–1632
Rook F, Bevan MW (2003) Genetic approaches to understanding sugar-response pathways. J Exp Bot 54:495–501
Rouhier N, Gelhaye E, Gualberto JM, Jordy MN, de Fay E, Hiasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot JP (2004) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant enzyme functional in pathogen defense. Plant Physiol 134:1027–1038
Rouhier N, Jacquot JP (2005) The plant multigenic family of thiol peroxidases. Free Radic Biol Med 38:1413–1421
Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489
Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. Progress Botany 54:151–173
To JPC, Reiter WD, Gibson SI (2002) Mobilization of seed storage lipid by Arabidopsis seedlings is retarded in the presence of exogenous sugars. BMC Plant Biol 2:4
To JPC, Reiter W-D, Gibson SI (2003) Chloroplast biogenesis by Arabidopsis seedlings is impaired in the presence of exogenous glucose. Physiol Plant 118:456–463
Trelease RN, Doman DC (1984) Mobilization of oil and wax reserves. In: Murray DR (ed) Seed physiology, vol 2. Germination and reserve mobilization. Academic Press, Orlando, FL, pp 201–245
Veljovic-Jovanovic SD, Pignocchi C, Noctor G, Foyer CH (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiol 127:426–435
Acknowledgements
We thank Martina Holt for excellent technical assistance, Dr. Steven Penfield (Univeristy of York, England) for providing us with the ICL:GUS reporter gene line and Dr. Andrea Kandlbinder for critical reading of the manuscript. The work was funded by the DAAD (grant given to A. P.-A.), the DFG (FOR387 TP3; Di 346/6-6 and Ba2011/2) and the University of Bielefeld.
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Pena-Ahumada, A., Kahmann, U., Dietz, KJ. et al. Regulation of peroxiredoxin expression versus expression of Halliwell-Asada-Cycle enzymes during early seedling development of Arabidopsis thaliana . Photosynth Res 89, 99–112 (2006). https://doi.org/10.1007/s11120-006-9087-3
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DOI: https://doi.org/10.1007/s11120-006-9087-3