Plastid-to-Nucleus Signaling

  • Åsa Strand
  • Tatjana Kleine
  • Joanne Chory
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

The function of the eukaryotic cell depends on the regulated and reciprocal interaction between its different compartments. This includes not only the exchange of energy equivalents but also information. Most information exchange flows from the nucleus to the organelles, because the large majority of genes encoding proteins with organellar function are encoded in the nucleus.

Keywords

Maize Photosynthesis Cytosol Porphyrin Chloro 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison LA, Simon LD and Maliga P (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J 15: 2802-2809PubMedGoogle Scholar
  2. Aluru MR, Bae H, Wu D and Rodermel SR (2001) The Ara-bidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiol 127: 67-77CrossRefPubMedGoogle Scholar
  3. Bae CH, Abe T, Matsuyama T, Fukunishi N, Nagata N, Nakano T, Kaneko Y, Miyoshi K, Matsushima H and Yoshida S (2001) Regulation of chloroplast gene expression is affected in ali, a novel tobacco albino mutant. Ann Bot 88: 545-553CrossRefGoogle Scholar
  4. Baumgartner BJ, Rapp JC and Mullet J (1989) Plastid transcrip-tion activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89: 1011-1018CrossRefPubMedGoogle Scholar
  5. Beale S (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60: 43-73CrossRefGoogle Scholar
  6. Bellaoui M, Keddie JS and Gruissem W (2003) DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development. Plant Mol Biol 53: 531-543CrossRefPubMedGoogle Scholar
  7. Bezhani S, Sherameti I, Pfannschmidt T and Oelmuller R (2001) A repressor with similarities to prokaryotic and eukaryotic DNA helicases controls the assembly of the CAAT box binding complex at a photosynthesis gene promoter. J Biol Chem 276: 23785-23789CrossRefPubMedGoogle Scholar
  8. Bolle C, Kusnetsov VV, Herrmann RG and Oelmuller R (1996) The spinach AtpC and AtpD genes contain elements for light-regulated, plastid-dependent and organ-specific expression in the vicinity of the transcription start sites. Plant J 9: 21-30CrossRefPubMedGoogle Scholar
  9. Bradbeer J, Atkinson Y, B örner T and Hagemann R (1979) Cy-toplasmic synthesis of plastid polypeptides may be controlled by plastid-synthesised RNA. Nature 279: 816-817CrossRefGoogle Scholar
  10. Bruce BD (2001) The paradox of plastid transit peptides: con-servation of function despite divergence in primary structure. Biochim Biophys Acta 1541: 2-21CrossRefPubMedGoogle Scholar
  11. Burgess D and Taylor W (1988) The chloroplast affects the tran-scription of a nuclear gene family. Mol Gen Genet 214: 89-96CrossRefGoogle Scholar
  12. Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G and Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11: 57-68CrossRefPubMedGoogle Scholar
  13. Chatterjee M, Sparvoli S, Edmunds C, Garosi P, Findlay K and Martin C (1996) DAG, a gene required for chloroplast dif-ferentiation and palisade development in Antirrhinum majus. EMBO J 15: 4194-4207PubMedGoogle Scholar
  14. Chatterjee M, Martin C, Sparvoli S, Edmunds C, Garosi P and Findlay K (1997) Tam3 produces a suppressible allele of the DAG locus of Antirrhinum majus similar to Mu-suppressible alleles of maize. Plant J 11: 759-771CrossRefPubMedGoogle Scholar
  15. Danon A and Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J 10: 3993-4001PubMedGoogle Scholar
  16. DeSantis-Maciossek G, Kofer W, Bock A, Schoch S, Maier RM, Wanner G, R üdiger W, Koop HU and Herrmann RG (1999) Targeted disruption of the plastid RNA polymerase gene rpoA, B and C1: molecular biology, biochemistry and ultrastructure. Plant J 18: 477-489CrossRefGoogle Scholar
  17. Dunford R and Walden RM (1991) Plastid genome structure and plastid-related transcript levels in albino barley plants derived from anther culture. Curr Genet 20: 339-347CrossRefPubMedGoogle Scholar
  18. Durnford DG and Falkowski PG (1997) Chloroplast redox regu-lation of nuclear gene transcription during photoacclimation. Photosynth Res 53: 229-241CrossRefGoogle Scholar
  19. Escoubas JM, Lomas M, LaRoche 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: 10237-10241CrossRefPubMedGoogle Scholar
  20. Estevez JM, Cantero A, Romero C, Kawaide H, Jimenez LF, Kuzuyama T, Seto H, Kamiya Y and Leon P (2000) Anal-ysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol 124: 95-104CrossRefPubMedGoogle Scholar
  21. Fankhauser C and Chory J (1997) Light control of plant devel-opment. Annu Rev Cell Dev Biol 13: 203-229CrossRefPubMedGoogle Scholar
  22. Forsburg SL and Guarente L (1989) Communication between mi-tochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Annu Rev Cell Biol 5: 153-180CrossRefPubMedGoogle Scholar
  23. Hanaoka M, Kanamaru K, Takahashi H and Tanaka K (2003) Molecular genetic analysis of chloroplast gene promoters de-pendent on SIG2, a nucleus-encoded sigma factor for the plastid-encoded RNA polymerase, in Arabidopsis thaliana. Nucleic Acids Res 31: 7090-7098CrossRefPubMedGoogle Scholar
  24. Hauser CR, Gillham NW and Boynton JE (1996) Transla-tional regulation of chloroplast genes. Proteins binding to the 5’-untranslated regions of chloroplast mRNAs in Chlamy-domonas reinhardtii. J Biol Chem 271: 1486-1497CrossRefPubMedGoogle Scholar
  25. Hayes R, Kudla J, Schuster G, Gabay L, Maliga P and Gruis-sem W (1996) Chloroplast mRNA 3 -end processing by a high molecular weight protein complex is regulated by nuclear-encoded RNA binding proteins. EMBO J 15: 1132-1141PubMedGoogle Scholar
  26. Hedtke B, Borner T and Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Sci-ence 277: 809-811Google Scholar
  27. Hedtke B, Borner T and Weihe A (2000) One RNA polymerase serving two genomes. EMBO Rep 1: 435-440CrossRefPubMedGoogle Scholar
  28. Hess WR, Prombona A, Fieder B, Subramanian AR and Borner T (1993) Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12: 563-571PubMedGoogle Scholar
  29. Hess WR, Muller A, Nagy F and Borner T (1994) Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol Gen Genet 242: 305-312CrossRefPubMedGoogle Scholar
  30. Hirose T and Sugiura M (1996) Cis-acting elements and trans-acting factors for accurate translation of chloroplast psbA mR-NAs: development of an in vitro translation system from to-bacco chloroplasts. EMBO J 15: 1687-1695PubMedGoogle Scholar
  31. Huner NPA, O¨quist G and Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3: 224-230CrossRefGoogle Scholar
  32. Jacobs J and Jacobs N (1993) Porphyrin accumulation and export by isolated barley (Hordum vulgare) plastids. Plant Physiol 101: 1181-1187PubMedGoogle Scholar
  33. Jarvis P (2003) Intracellular signalling: the language of the chloroplast. Curr Biol 13: R314-R316CrossRefPubMedGoogle Scholar
  34. Jarvis P and Soll J (2002) Toc, tic, and chloroplast protein import. Biochim Biophys Acta 1590: 177-189CrossRefPubMedGoogle Scholar
  35. Jensen PE, Willows RD, Petersen BL, Vothknecht UC, Stum-mann BM, Kannangara CG, von Wettstein D and Henningsen KW (1996) Structural genes for Mg-chelatase subunits in bar-ley: xantha-f, -g and -h. Mol Gen Genet 250: 383-394PubMedGoogle Scholar
  36. Johanningmeier U and Howell SH (1984) Regulation of light-harvesting chlorophyll-binding protein mRNA accumula-tion in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors. J Biol Chem 259: 13541-13549PubMedGoogle Scholar
  37. Joyard J, Teyssier E, Mi ège C, Berny-Seigneurin D, Mar échal E, Block MA, Dorne AJ, Rolland N, Ajlani G and Douce R (1998) The biochemical machinery of plastid envelope membranes. Plant Physiol 118: 715-723CrossRefPubMedGoogle Scholar
  38. Karpinski S, Escobar C, Karpinska B, Creissen G and Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9: 627-40CrossRefPubMedGoogle Scholar
  39. 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: 654-657CrossRefPubMedGoogle Scholar
  40. Keddie JS, Carol B, Jones JD and Gruissem W (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J 15: 4208-4217PubMedGoogle Scholar
  41. Keegstra K and Cline K (1999) Protein import and routing sys-tems of the chloroplasts. Plant Cell 11: 557-570CrossRefPubMedGoogle Scholar
  42. Kittsteiner U, Brunner H and Rudiger W (1991) The green-ing process in cress sedlings. II. Complexing agents and 5-aminolevulinate inhibit accumulation of cab messenger RNA coding for the light-harvesting chlorophyll a/b protein. Physiol Plant 81: 190-196CrossRefGoogle Scholar
  43. Kotani H and Tabata S (1998) Lessons from sequencing of the genome of a unicellular cyanobacterium, Synechocystis sp. PCC6803. Annu Rev Plant Physiol Plant Mol Biol 49: 151-171CrossRefPubMedGoogle Scholar
  44. Kropat J, Oster U, R üdiger W and Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Nat Acad Sci USA 94: 14168-14172CrossRefPubMedGoogle Scholar
  45. Kropat J, Oster U, R üdiger W and Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes re-quires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24: 523-531CrossRefPubMedGoogle Scholar
  46. Kusnetsov V, Bolle C, Lubberstedt T, Sopory S, Herrmann RG and Oelmuller R (1996) Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol Gen Genet 252: 631-639PubMedGoogle Scholar
  47. Kusumi K, Komori H, Satoh H and Iba K (2000) Characterization of a zebra mutant of rice with increased susceptibility to light stress. Plant Cell Physiol 41: 158-164PubMedGoogle Scholar
  48. La Rocca N, Rascio N, Oster U and R üdiger 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: 101-108CrossRefPubMedGoogle Scholar
  49. Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902-906CrossRefPubMedGoogle Scholar
  50. Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19: 47-56CrossRefPubMedGoogle Scholar
  51. Leon P, Arroyo A and Mackenzie S (1998) Nuclear control of plastid and mitochondrial development in higher plants. Annu Rev Plant Physiol Plant Mol Biol 49: 453-480CrossRefPubMedGoogle Scholar
  52. Li H, Culligan K, Dixon RA and Chory J (1995) CUE1: a mes-ophyll cell-specific positive regulator of light-controlled gene expression in Arabidopsis. Plant Cell 7: 1599-1610CrossRefPubMedGoogle Scholar
  53. Long D, Martin M, Sundberg E, Swinburne J, Puangsomlee P and Coupland G (1993) The maize transposable element system Ac/Ds as a mutagen in Arabidopsis: identification of an albino mutation induced by Ds insertion. Proc Natl Acad Sci USA 90: 10370-10374CrossRefPubMedGoogle Scholar
  54. Lopez-Juez E, Jarvis RP, Takeuchi A, Page AM and Chory J (1998) New Arabidopsis cue mutants suggest a close connec-tion between plastid- and phytochrome-regulation of nuclear gene expression. Plant Physiol 118: 803-815CrossRefPubMedGoogle Scholar
  55. Mandel MA, Feldmann KA, Herrera-Estrella L, Rocha-Sosa M and Leon P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9: 649-658CrossRefPubMedGoogle Scholar
  56. Martinez-Zapater JM, Gil P, Capel J and Somerville CR (1992) Mutations at the Arabidopsis CHM locus promote rearrange-ments of the mitochondrial genome. Plant Cell 4: 889-899CrossRefPubMedGoogle Scholar
  57. Matile P, Schellenberg M and Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloro-plasts. Planta 187: 230-235CrossRefGoogle Scholar
  58. Mayfield S and Taylor W (1984) Carotenoid-deficient maize seedlings fail to accumulate light harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur J Biochem 144: 79-84CrossRefPubMedGoogle Scholar
  59. Mayfield S, Yohn CB, Cohen A and Danon A (1995) Regulation of chloroplast gene expression. Annu Rev Plant Physiol Plant Mol Biol 46: 147-166CrossRefGoogle Scholar
  60. McCormac AC, Fischer A, Kumar AM, Soll D and Terry MJ (2001) Regulation of HEMA1 expression by phytochrome and a plastid signal during de-etiolation in Arabidopsis thaliana. Plant J 25: 549-561CrossRefPubMedGoogle Scholar
  61. Meskauskiene R and Apel K (2002) Interaction of FLU, a nega-tive regulator of tetrapyrrole biosynthesis, with the glutamyl-tRNA reductase requires the tetratricopeptide repeat domain of FLU. FEBS Lett 532: 27-30CrossRefPubMedGoogle Scholar
  62. 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: 12826-12831CrossRefPubMedGoogle Scholar
  63. Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Nat Acad Sci USA 98: 2053-2058CrossRefPubMedGoogle Scholar
  64. Moore M, Harrison MS, Peterson EC, Henry R, Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G, Long D, Martin M, Swinburne J and Puangsomlee P (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275: 1529-1532CrossRefPubMedGoogle Scholar
  65. Mullet JE (1993) Dynamic regulation of chloroplast transcrip-tion. Plant Physiol 103: 309-313CrossRefPubMedGoogle Scholar
  66. Mullineaux P and Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5: 43-48CrossRefPubMedGoogle Scholar
  67. Oelm üller R and Mohr H (1986) Photo-oxidative destruction of chloroplasts and its consequences for expression of nuclear genes. Planta 167: 106-113CrossRefGoogle Scholar
  68. Oelm üller R, Levitan I, Bergfeld R, Rajasekhar V and Mohr H (1986) Expression of nuclear genes is affected by treatments acting on the plastids. Planta 168: 482-492CrossRefGoogle Scholar
  69. Osterlund MT, Wei N and Deng XW (2000) The roles of pho-toreceptor systems and the COP1-targeted destabilization of HY5 in light control of Arabidopsis seedling development. Plant Physiol 124: 1520-1524CrossRefPubMedGoogle Scholar
  70. Oswald O, Martin T, Dominy PJ and Graham IA (2001) Plastid re-dox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 13: 2047-2052CrossRefGoogle Scholar
  71. Pfannschmidt T (2003) Chloroplast redox signals: how photo-synthesis controls its own genes. Trends Plant Sci 8: 33-41CrossRefPubMedGoogle Scholar
  72. Pfannschmidt T, Nilsson A and Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625-628CrossRefGoogle Scholar
  73. Pfannschmidt T, Schutze K, Brost M and Oelmuller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photo-system stoichiometry adjustment. J Biol Chem 276: 36125-36130CrossRefPubMedGoogle Scholar
  74. Puente P, Wei N and Deng XW (1996) Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J 15: 3732-3743PubMedGoogle Scholar
  75. Rapp JC and Mullet JE (1991) Chloroplast transcription is re-quired to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently. Plant Mol Biol 17: 813-823CrossRefPubMedGoogle Scholar
  76. Reiter RS, Coomber SA, Bourett TM, Bartley GE and Scolnik PA (1994) Control of leaf and chloroplast development by the Arabidopsis gene pale cress. Plant Cell 6: 1253-1264CrossRefPubMedGoogle Scholar
  77. Rintamaki E, Martinsuo P, Pursiheimo S and Aro EM (2000) Cooperative regulation of light-harvesting complex II phos-phorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97: 11644-11649CrossRefPubMedGoogle Scholar
  78. Rodermel S and Park S (2003) Pathways of intracellular commu-nication: tetrapyrroles and plastid-to-nucleus signaling. Bioas-says 25: 631-636CrossRefGoogle Scholar
  79. Sakamoto W, Kondo H, Murata M and Motoyoshi F (1996) Al-tered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8: 1377-1390CrossRefPubMedGoogle Scholar
  80. Strand A, Hurry V, Gustafsson P and Gardestrom P (1997) De-velopment of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohy-drates. Plant J 12: 605-614CrossRefPubMedGoogle Scholar
  81. Strand A, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumu-lation of Mg-protoporphyrinIX. Nature 421: 79-83CrossRefPubMedGoogle Scholar
  82. Streatfield SJ, Weber A, Kinsman EA, Hausler RE, Li J, Post-Beittenmiller D, Kaiser WM, Pyke KA, Flugge UI and Chory J (1999) The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression. Plant Cell 11: 1609-1622CrossRefPubMedGoogle Scholar
  83. Sullivan JA and Gray JC (1999) Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant. Plant Cell 11: 901-910CrossRefPubMedGoogle Scholar
  84. Sullivan JA and Gray JC (2000) The pea light-independent pho-tomorphogenesis1 mutant results from partial duplication of COP1 generating an internal promoter and producing two dis-tinct transcripts. Plant Cell 12: 1927-1938CrossRefPubMedGoogle Scholar
  85. Sullivan JA and Gray JC (2002) Multiple plastid signals regu-late the expression of the pea plastocyanin gene in pea and transgenic tobacco plants. Plant J 32: 763-774CrossRefPubMedGoogle Scholar
  86. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C and Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717-730CrossRefPubMedGoogle Scholar
  87. Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74: 787-799CrossRefPubMedGoogle Scholar
  88. Terry MJ and Kendrick RE (1999) Feedback inhibition of chloro-phyll synthesis in the phytochrome chromophore-deficient au-rea and yellow-green-2 mutants of tomato. Plant Physiol 119: 143-152CrossRefPubMedGoogle Scholar
  89. Terry MJ, Maines MD and Lagarias JC (1993) Inactivation of phytochrome- and phycobiliprotein-chromophore precursors by rat liver biliverdin reductase. J Biol Chem 268: 26099-26106PubMedGoogle Scholar
  90. Terzagi WB and Cashmore AR (1995) Light regulated transcrip-tion. Annu Rev Plant Physiol Plant Mol Biol 40: 211-233Google Scholar
  91. Thomas J and Weinstein J (1990) Measurement of heme efflux and heme content in isolated developing chloroplasts. Plant Physiol 94: 1414-1423CrossRefPubMedGoogle Scholar
  92. Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S and Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100: 16119-16124CrossRefPubMedGoogle Scholar
  93. Wakasugi T, Tsudzuki T and Sugiura M (2001) The genomics of land plant chloroplasts: gene content and alterations of ge-nomic information by RNA editing. Photosynth Res 70: 107-118CrossRefPubMedGoogle Scholar
  94. Wetzel CM, Jiang CZ, Meehan LJ, Voytas DF and Roder-mel SR (1994) Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J 6: 161-175CrossRefPubMedGoogle Scholar
  95. Wilson KE, Krol M and Huner NP (2003) Temperature-induced greening of Chlorella vulgaris. The role of the cellular en-ergy balance and zeaxanthin-dependent nonphotochemical quenching. Planta 217: 616-627CrossRefPubMedGoogle Scholar
  96. Wu D, Wright DA, Wetzel C, Voytas DF and Rodermel S (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11: 43-55CrossRefPubMedGoogle Scholar
  97. Zhang H, Scheirer DC, Fowle WH and Goodman HM (1992) Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Ara-bidopsis. Plant Cell 4: 1575-1588CrossRefPubMedGoogle Scholar
  98. Zhang H, Wang W-Y and Goodman HM (1994) Expression of the Arabidopsis gene Akr coincides with chloroplast development. Plant Physiol 106: 1261-1267PubMedGoogle Scholar
  99. Zhang L and Hach A (1999) Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator. Cell Mol Life Sci 56: 415-426CrossRefPubMedGoogle Scholar
  100. Zubko MK and Day A (1998) Stable albinism induced without mutagenesis: a model for ribosome-free plastid inheritance. Plant J 15: 265-271CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Åsa Strand
    • 1
  • Tatjana Kleine
    • 1
  • Joanne Chory
    • 2
  1. 1.Department of Plant BiologyUmeå UniversitySweden
  2. 2.Plant Biology Laboratory and Howard Hughes Medical InstituteThe Salk InstituteLa JollaUSA

Personalised recommendations