Photosynthesis pp 175-190 | Cite as

Intracellular Signaling from Plastids to the Nucleus

Chapter
First Online:
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 34)

Summary

Signaling from chloroplasts or other plastids to the nucleus is part of the intracellular communication network of plants. Several signals originate in the plastids from processes like plastid gene expression, photosynthetic electron transport, or chlorophyll biosynthesis. In some cases, signaling compounds like reactive oxygen species or Mg-protoporphyrin are suggested to be involved in this process. Signaling leads to up- and down-regulation in the expression of certain nuclear genes. While the origins of signaling pathways in the plastids and the effect in the nucleus have been accessible to various experimental approaches, none of the signaling pathways has been completely elucidated. According to the present view, several signaling pathways are connected to a communication network in which light signals are also involved.

Keywords

Plastid Protein Light Induction Nuclear Gene Expression Plastid Gene Expression Plastid Signal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

ABA

– Abscisic acid;

APX

– Ascorbate peroxidase;

CAO

– Chlorophyllide a oxygenase;

2CPA

– 2-cystein peroxiredoxin A;

CRY

– Cryptochrome;

DBMIB

– 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone;

DCMU

– 3-(3,4-dichlorophenyl)-1,1-dimethyl urea;

ELIP2

– Early light-induced gene;

GUN

– Genomes uncoupled;

HEMA

– Gene encoding glutamyl-tRNA reductase;

HSP70

– 70 kDa heat shock protein;

LHC

– Light harvesting complex;

LHCB

– Light-harvesting chlorophyll a/b-binding protein;

MgProto

– Mg-protoporphyrin;

PETE

– Gene encoding plastocyanin;

PQ

– Plastoquinone;

PS I, PS II

– Photosystem I, photosystem II;

PSAD, PSAF

– Subunits of PS I;

RBCS

– Ribulose bisphosphate carboxylase small subunit;

ROS

– Reactive oxygen species

This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank all colleagues who made their results available to us. Special thanks are due to Drs. Christoph F. Beck, Dario Leister and Robert J. Porra for critical reading of the manuscript and helpful suggestions.

References

  1. Ankele E, Kindgren P, Pesquet E and 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: 1964–1979PubMedCrossRefGoogle Scholar
  2. Apel K and Hirt H (2004) Reactive oxygen species: meta­bolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373–399PubMedCrossRefGoogle Scholar
  3. Baier M and 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: 1449–1462PubMedCrossRefGoogle Scholar
  4. Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222: 743–756PubMedCrossRefGoogle Scholar
  5. Biehl A, Richly E, Noutsos C, Salamini F and Leister D (2005) Analysis of 101 nuclear transcriptomas reveals 23 distinct regulons and their relationship to metabolism, chromosomal gene distribution and co-ordination of nuclear and plastid gene expression. Gene 344: 33–41PubMedCrossRefGoogle Scholar
  6. Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P and Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437: 1179–1182PubMedCrossRefGoogle Scholar
  7. Bradbeer JW, Atkinson YE, Börner T and Hagemann R (1979) Cytoplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesized RNA. Nature 279: 816–817CrossRefGoogle Scholar
  8. Bräutigam K, Dietzel L and Pfannschmidt T (2008) Plastid-nucleus communication: anterograde and retrograde signaling in the development and function of plastids. In: Bock R (ed) Topics in Current Genetics, Vol 19: Cell and Molecular Biology of Plastids, pp 409–456. Springer, Berlin/HeidelbergGoogle Scholar
  9. Chen YB, Durnford DG, Koblizek M and Falkowski PG (2004) Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol 136: 3737–3750PubMedCrossRefGoogle Scholar
  10. Durnford DG and Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53: 229–241CrossRefGoogle Scholar
  11. Emanuel C, Weihe A, Graner A, Hess WR and Börner T (2005) Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J 38: 460–472CrossRefGoogle Scholar
  12. Escoubas JM, Lomas M, La Roche J and Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92: 10237–10241PubMedCrossRefGoogle Scholar
  13. Feierabend J and 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: 133–145CrossRefGoogle Scholar
  14. Feierabend J and Wildner J (1978) Formation of the small in the absence of the large subunit of RuBP carboxylase in 70S ribosome-deficient rye leaves. Arch Biochem Biophys 186: 283–291PubMedCrossRefGoogle Scholar
  15. Fernandez AP and Strand Å (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opinion Plant Biol 11: 509–513CrossRefGoogle Scholar
  16. Fey V, Wagner R, Bräutigam K and Pfannschmidt T (2005) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56: 1491–1498PubMedCrossRefGoogle Scholar
  17. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM and Baker NR (2003) Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33: 691–705PubMedCrossRefGoogle Scholar
  18. Gadjieva R, Axelsson E, Olsson U and Hansson, M (2005) Analysis of gun phenotype in barley magnesium chelatase and Mg protoporphyrin IX monomethyl ester cyclase mutants. Plant Physiol Biochem 43: 901–908PubMedCrossRefGoogle Scholar
  19. Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M and Apel K (2004) Concurrent interactions of heme and FLU with Glut RNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J 40: 957–967PubMedCrossRefGoogle Scholar
  20. Gray JC (2005) Regulation of nuclear gene expression by plastid signals. Annu Plant Rev 13: 237–266Google Scholar
  21. Heiber I, Ströher E, Raatz B, Busse I, Kahmann U, Bevan M, Dietz K-J and Baier M (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol 143: 1774–1788PubMedCrossRefGoogle Scholar
  22. Hess WR, Schendel R, Börner T and Rüdiger W (1991) Reduction of mRNA level for two nuclear encoded light regulated genes in the barley mutant albostrians is not correlated with phytochrome content and activity. J Plant Physiol 138: 292–298CrossRefGoogle Scholar
  23. Hess WR, Müller A, Nagy F and Börner T (1994) Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol Gen Genet 242: 305–312PubMedCrossRefGoogle Scholar
  24. Hirashima M, Satoh S, Tanaka R and Tanaka A (2006) Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J Biol Chem 281: 15385–15393PubMedCrossRefGoogle Scholar
  25. Johanningmeier U (1988) Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem 177: 417–424PubMedCrossRefGoogle Scholar
  26. Johanningmeier U and Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. J Biol Chem 259: 13541–13549PubMedGoogle Scholar
  27. Karpinski S, Escobar C, Karpinska B, Creissen G and Mullineaux P (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9: 627–640PubMedGoogle Scholar
  28. Karpinski, S, Reynolds H, Karpinska B, Wingsle G, Creissen G and Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284: 654–657PubMedCrossRefGoogle Scholar
  29. Kimura M, Manabe K, Abe T, Yoshida S, Matsui M and Yamamoto YY (2003) Analysis of hydrogen peroxide-independent expression of the high-light-inducible ELIP2 gene with the aid of the ELIP2 promoter-luciferase fusion. Photochem Photobiol 77: 668–674PubMedCrossRefGoogle Scholar
  30. Kittsteiner U, Brunner H and Rüdiger W (1991a) The greening process in cress seedlings II. Complexing agents and 5-aminolevulinate inhibit accumulation of cab-mRNA coding for the light-harvesting chlorophyll a/b protein. Physiol Plant 81: 190–196CrossRefGoogle Scholar
  31. Kittsteiner U, Mostowska A and Rüdiger W (1991b) The greening process in cress seedlings I. Pigment accumulation and ultrastructure after application of 5-aminolevulinate and complexing agents. Physiol Plant 81: 139–147CrossRefGoogle Scholar
  32. Kleine T, Kindgren P, Benedict C, Hendrickson L and Strand A (2007) Genome-wide gene expression analysis reveals a critical role for crytochrome 1 in the response of Arabidopsis to high irradiance. Plant Physiol 144: 1391–1406PubMedCrossRefGoogle Scholar
  33. Kropat J, Oster U, Rüdiger W and Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-hock genes. Proc Natl Acad Sci USA 94:14168–14172PubMedCrossRefGoogle Scholar
  34. Kropat J, Pöpperl G, Rüdiger W and Beck CF (1999) Identification of Mg-protoporphyrin IX as a chloroplast signal that mediates the expression of nuclear genes. In: Wagner E, Normann J, Greppin H, Hackstein JHP, Hermann RG, Kowallik KV, Schenk HEA, Seckbach J (eds) From symbiosis to eukaryotism. Endocytobiol VII, pp 341–348. University of Geneva, GenevaGoogle Scholar
  35. Kropat J, Oster U, Rüdiger W and Beck CF (2000) Chloroplast signaling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24: 523–531PubMedCrossRefGoogle Scholar
  36. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R and Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316: 715–719PubMedCrossRefGoogle Scholar
  37. La Rocca N, Rascio N, Oster U and Rüdiger 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: 101–108PubMedCrossRefGoogle Scholar
  38. La Rocca N, Rascio N, Oster U and Rüdiger W (2007) Inhibition of lycopene cyclase results in accumulation of chlorophyll precursors. Planta 225: 1019–1029PubMedCrossRefGoogle Scholar
  39. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I and Apel K (2007) Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci USA 104: 672–677PubMedCrossRefGoogle Scholar
  40. Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902–906PubMedCrossRefGoogle Scholar
  41. Lee KP, Kim C, Landgraf F and Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA104: 10270–10275PubMedCrossRefGoogle Scholar
  42. Leister D (2005) Genomics-based dissection of the cross-talk of chloroplasts with the nucleus and mitochondria in Arabidopsis. Gene 354: 110–116PubMedCrossRefGoogle Scholar
  43. Maxwell DP, Laudenbach DE and Huner NPA (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109: 787–795PubMedGoogle Scholar
  44. Meskauskiene R and 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: 27–30PubMedCrossRefGoogle Scholar
  45. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R and Apel K (2001) FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826–12831PubMedCrossRefGoogle Scholar
  46. Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN 5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053–2058PubMedCrossRefGoogle Scholar
  47. Mochizuki N, Tanaka R, Tanaka A, Masuda T and 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: 15184–15189PubMedCrossRefGoogle Scholar
  48. Moulin M, McCormac MC, Terry MJ and 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: 15178–15183PubMedCrossRefGoogle Scholar
  49. Nott A, Jung H-S, Koussevitzky S and Chory J (2006) Plastid-to-nucleus retrograde signaling- Annu Rev Plant Biol 57: 739–759PubMedCrossRefGoogle Scholar
  50. Oelmüller R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene expression and extraplastidic enzyme levels. Photochem Photobiol 49:229–239CrossRefGoogle Scholar
  51. Oelmüller R, Dietrich G, Link G and Mohr H (1986) Regulatory factors involved in gene expression (subunits of ribulose-1,5-bisphosphate carboxylase) in mustard (Sinapis alba L.) cotyledons. Planta 169: 260–266CrossRefGoogle Scholar
  52. Oelze ML, Kandlbinder A and Dietz K-J (2008) Redox regulation and overreduction control in the photosynthesizing cell: complexity in redox regulatory networks. Biochim Biophys Acta 1780: 1261–1272PubMedCrossRefGoogle Scholar
  53. Oster U, Brunner H and Rüdiger W (1996) The greening process in cress seedlings. V. Possible interference of chlorophyll precursors, accumulated after thujaplicin treatment, with light-regulated expression of Lhc genes. J Photochem Photobiol B 36: 255–261CrossRefGoogle Scholar
  54. Oswald O, Martin T, Dominy PJ and Graham IA (2001) Plastid redox state and sugars: Interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98: 2047–2052PubMedCrossRefGoogle Scholar
  55. Pesaresi P, Masiero S, Eubel H, Braun HP, Bhushan S, Glaser E, Salamini F and Leister D (2006) Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell 18: 970–991PubMedCrossRefGoogle Scholar
  56. Pesaresi P, Schneider A, Kleine T and Leister D (2007) Interorganellar communication. Curr Opinion Plant Biol 10: 1–7CrossRefGoogle Scholar
  57. Petracek ME, Dickey LF and Thompson WF (1997) Light-regulated changes in abundance and polyribosome association of ferredoxin are dependent on photosynthesis. Plant Cell 9: 2291–2300PubMedGoogle Scholar
  58. Petracek ME, Dickey LF, Nguyen TT, Gatz G, Sowinski DA, Allen GC and Thompson WF (1998) Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc Natl Acad Sci USA 95: 9009–9013PubMedCrossRefGoogle Scholar
  59. Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8: 33–41PubMedCrossRefGoogle Scholar
  60. Pfannschmidt T, Schütze K, Brost M and Oelmüller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276: 36125–36130PubMedCrossRefGoogle Scholar
  61. Piipo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N and Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25: 142–152CrossRefGoogle Scholar
  62. Pontier D, Albrieux C, Joyard J, Lagrange T and Block M (2007) Knock-out of the magnesium protophorphyrin IX methyltransferase gene in Arabidopsis. Effects on chloroplast development and on chloroplast-to-nucleus signa­ling. J Biol Chem 282: 2297–2304PubMedCrossRefGoogle Scholar
  63. Pöpperl G, Oster U and Rüdiger W (1998) Light-dependent increase in chlorophyll precursors during the day-night cycle in tobacco and barley seedlings. J Plant Physiol 153: 40–45CrossRefGoogle Scholar
  64. Pursiheimo S, Mulo P, Rintamäki E and Aro EM (2001) Coregulation of light-harvesting complex II phosphorylation and Lhcb accumulation in winter rye. Plant J 26: 317–327PubMedCrossRefGoogle Scholar
  65. Reinbothe C, Bartsch S, Eggink LL, Hoober K, Bruslan J, Andrade-Paz R, Monnet J and Reinbothe S (2006) A role foe chlorophyllide a oxygenase in the regulated import and stabilization of light-harvesting chlorophyll a/b proteins. Proc Natl Acad Sci USA 103: 4777–4782PubMedCrossRefGoogle Scholar
  66. Richly E, Dietzmann A, Biehl A, Kurth J, Laloi C, Apel K, Salamini F and Leister D (2003) Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep 4: 491–498PubMedCrossRefGoogle Scholar
  67. Ruckle ME, DeMarco SM and Larkin RM (2007) Plastid signals remodel light signaling networks and are essential for efficient chloroplast biogenesis in Arabidopsis. Plant Cell 19: 3944–3960PubMedCrossRefGoogle Scholar
  68. Rzeznicka K, Walker CJ, Westergren T, Kannangara CG, von Wettstein D, Merchant S, Gough SP and Hansson, M. (2005) Xantha-l encodes a membrane subunit of the aerobic Mg-protoporphyrin IX monomethyl ester cyclase involved in chlorophyll biosynthesis. Proc Natl Acad Sci USA 102: 5886–5891PubMedCrossRefGoogle Scholar
  69. Shao N, Vallon O, Dent R, Niyogi KK and Beck CF (2006) Defects in the cytochrome b 6    f complex prevent light-induced expression of nuclear genes involved in chlorophyll biosynthesis. Plant Physiol 141: 1128–1137PubMedCrossRefGoogle Scholar
  70. Shao N, Krieger-Liszkay A, Schroda M and Beck CF (2007) A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J 50: 475–487PubMedCrossRefGoogle Scholar
  71. Sherameti I, Sopory SK, Trebicka A, Pfannschmidt T and Oelmüller R (2002) Photosynthetic electron transport determines nitrate reductase gene expression and activity in higher plants. J Biol Chem 277: 46594–46600PubMedCrossRefGoogle Scholar
  72. Strand Å (2004) Plastid-to-nucleus signaling. Curr Opinion Plant Biol 7: 621–625CrossRefGoogle Scholar
  73. Strand Å, Asami T, Alonso J Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421: 79–83PubMedCrossRefGoogle Scholar
  74. Sullivan JA and Gray JC (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in the roots of the pea lip1 mutant. Plant Cell 11: 901–910PubMedGoogle Scholar
  75. Sullivan JA and Gray JC (2002) Multiple plastid signals regulate the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J 32: 763–774PubMedCrossRefGoogle Scholar
  76. Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants in Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787–799PubMedCrossRefGoogle Scholar
  77. Tanaka R and Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321–346PubMedCrossRefGoogle Scholar
  78. Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Annu Rev Plant Physiol Plant Mol Biol 40: 211–233CrossRefGoogle Scholar
  79. Taylor WC, Burgess DG and Mayfield SP (1986) The use of carotenoid deficiencies to study nuclear-chloroplast regulatory interactions. In: Randall D (ed) Current Topics in Plant Biochemistry and Physiology, Vol 5, pp 117–127. The Interdisciplinary Plant Biochemistry and Physiology Program, University of Missouri, ColumbiaGoogle Scholar
  80. Vasileuskaya Z, Oster U and Beck C (2004) Involvement of tetrapyrroles in inter-organellar signaling in plants and algae. Photosynth Res 82: 289–299PubMedCrossRefGoogle Scholar
  81. Vasileuskaya Z, Oster U and Beck C (2005) Mg-Protopor­phyrin IX and heme control HEMA, the gene enco­ding the first specific step of tetrapyrrole biosynthesis, in Chlamydomonas reinhardtii. Eukaryotic Cell 4: 1620–1628PubMedCrossRefGoogle Scholar
  82. von Gromoff ED, Schroda M, Oster U and Beck CF (2006) Identification of a plastid response element that acts as an enhancer within the Chlamydomonas HSP70A. Nucleic Acids Res 34: 4767–4779CrossRefGoogle Scholar
  83. von Gromoff ED, Alawady A, Meinecke L, Grimm B and Beck CF (2008) Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell 20: 552–567CrossRefGoogle Scholar
  84. Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E and Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306: 1183–1185PubMedCrossRefGoogle Scholar
  85. Wilde A, Mikolajczyk S, Alawady A, Lokstein H and Grimm B (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571: 119–123PubMedCrossRefGoogle Scholar
  86. Yabuta Y, Maruta T, Yoshimura K, Ishikawa T and Shigeoka S (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol 45: 1586–1594PubMedCrossRefGoogle Scholar
  87. Yang DH, Andersson B, Aro EM and Ohad I (2001) The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHII) during photoacclimation. Photosynth Res 68: 163–174PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Department Biologie IBotanik der Ludwig-Maximilians-UniversitätMunichGermany

Personalised recommendations