1932

Abstract

Abstract

Plant cells store genetic information in the genomes of three organelles: the nucleus, plastid, and mitochondrion. The nucleus controls most aspects of organelle gene expression, development, and function. In return, organelles send signals to the nucleus to control nuclear gene expression, a process called retrograde signaling. This review summarizes our current understanding of plastid-to-nucleus retrograde signaling, which involves multiple, partially redundant signaling pathways. The best studied is a pathway that is triggered by buildup of Mg-ProtoporphyrinIX, the first intermediate in the chlorophyll branch of the tetrapyrrole biosynthetic pathway. In addition, there is evidence for a plastid gene expression-dependent pathway, as well as a third pathway that is dependent on the redox state of photosynthetic electron transport components. Although genetic studies have identified several players involved in signal generation, very little is known of the signaling components or transcription factors that regulate the expression of hundreds of nuclear genes.

Loading

Article metrics loading...

/content/journals/10.1146/annurev.arplant.57.032905.105310
2006-06-02
2025-02-09
Loading full text...

Full text loading...

/deliver/fulltext/pp/57/1/annurev.arplant.57.032905.105310.html?itemId=/content/journals/10.1146/annurev.arplant.57.032905.105310&mimeType=html&fmt=ahah

Literature Cited

  1. Abdallah F, Salamini F, Leister D. 2000. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci. 5:141–42 [Google Scholar]
  2. Acevedo-Hernandez GJ, Leon P, Herrera-Estrella LR. 2005. Sugar and ABA responsiveness of a minimal RBCS light-responsive unit is mediated by direct binding of ABI4. Plant J. 43:506–19 [Google Scholar]
  3. Adamska I. 1995. Regulation of early light-inducible protein gene expression by blue and red light in etiolated seedlings involves nuclear and plastid factors. Plant Physiol. 107:1167–75 [Google Scholar]
  4. Anderson JM. 1986. Photoregulation of the composition, function, and structure of thylakoid membranes. Annu. Rev. Plant Physiol. 37:93–136 [Google Scholar]
  5. Anderson SL, Teakle GR, Martino-Catt SJ, Kay SA. 1994. Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter. Plant J. 6:457–70 [Google Scholar]
  6. Apel K, Hirt H. 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373–99 [Google Scholar]
  7. Bolle C, Kusnetsov VV, Herrmann RG, Oelmüller 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. 9:21–30 [Google Scholar]
  8. Bradbeer JW, Atkinson YA, Börner T, Hagemann R. 1979. Cytoplasmic synthesis of plastid polypeptide may be controlled by plastid-synthesized RNA. Nature 279:816–17 [Google Scholar]
  9. Brown NJ, Sullivan JA, Gray JC. 2005. Light and plastid signals regulate the expression of the pea plastocyanin gene through a common region at the 5′ end of the coding region. Plant J. 43:541–52 [Google Scholar]
  10. Chandok MR, Sopory SK, Oelmüller R. 2001. Cytoplasmic kinase and phosphatase activities can induce PsaF gene expression in the absence of functional plastids: evidence that phosphorylation/dephosphorylation events are involved in interorganellar crosstalk. Mol. Gen. Genomics 264:819–26 [Google Scholar]
  11. Chekounova E, Voronetskaya V, Papenbrock J, Grimm B, Beck CF. 2001. Characterization of Chlamydomonas mutants defective in the H subunit of Mg-chelatase. Mol. Genet. Genomics 266:363–73 [Google Scholar]
  12. Chen YB, Durnford DG, Koblizek M, Falkowski PG. 2004. Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol. 136:3737–50 [Google Scholar]
  13. Crawford MS, Wang W. 1983. Metabolism of magnesium protoporphyrin monomethyl ester in Chlamydomonas reinhardtii. Plant Physiol. 71:303–6 [Google Scholar]
  14. Duggan J, Gassman M. 1974. Induction of porphyrin synthesis in etiolated bean leaves by chelators of iron. Plant Physiol. 68:206–15 [Google Scholar]
  15. Eguchi S, Takano H, Ono K, Takio S. 2002. Photosynthetic electron transport regulates the stability of the transcript for the protochlorophyllide oxidoreductase gene in the liverwort, Marchantia paleacea var. diptera. Plant Cell Physiol. 43:573–77 [Google Scholar]
  16. Emanuel C, Weihe A, Graner A, Hess WR, Börner T. 2004. Chloroplast development affects expression of phage-type RNA polymerases in barley leaves. Plant J. 38:460–72 [Google Scholar]
  17. Escoubas J, Lomas M, LaRoche J, 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 92:10237–41 [Google Scholar]
  18. Fey V, Wagner R, Brautigam K, Pfannschmidt T. 2005. Photosynthetic redox control of nuclear gene expression. J. Exp. Bot. 56:1491–98 [Google Scholar]
  19. Fey V, Wagner R, Brautigam K, Wirtz M, Hell R. et al. 2005. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J. Biol. Chem. 280:5318–28 [Google Scholar]
  20. Forsburg SL, Guarente L. 1989. Communication between mitochondria and the nucleus in regulation of cytochrome genes in the yeast Saccharomyces cerevisiae. Annu. Rev. Cell Biol. 5:153–80 [Google Scholar]
  21. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR. 2003. Control of ascorbate peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J. 33:691–705 [Google Scholar]
  22. Goldschmidt-Clermont M. 1998. Coordination of nuclear and chloroplast gene expression in plant cells. Int. Rev. Cytol. 177:115–80 [Google Scholar]
  23. Gray JC, Sornarajah R, Zabron AA, Duckett CM, Khan MS. 1995. Chloroplast control of nuclear gene expression. In Photosynthesis: From Light to Biosphere ed. P Mathis pp. 543–50 The Netherlands: Kluwer Acad. [Google Scholar]
  24. Gray JC, Sullivan JA, Wang JH, Jerome CA, MacLean D. 2003. Coordination of plastid and nuclear gene expression. Philos. Trans. R. Soc. London Ser. B. Biol. Sci. 358:135–44 discussion 44–45 [Google Scholar]
  25. Heddad M, Adamska I. 2000. Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. Proc. Natl. Acad. Sci. USA 97:3741–46 [Google Scholar]
  26. Hess WR, Muller A, Nagy F, Borner T. 1994. Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal. Mol. Gen. Genet. 242:305–12 [Google Scholar]
  27. Hess WR, Schendel R, Börner T, 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. 138:292–98 [Google Scholar]
  28. Hon T, Hach A, Tamalis D, Zhu Y, Zhang L. 1999. The yeast heme-responsive transcriptional activator Hap1 is a preexisting dimer in the absence of heme. J. Biol. Chem. 274:22770–74 [Google Scholar]
  29. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M. 2003. Early light-induced proteins protect Arabidopsis from photooxidative stress. Proc. Natl. Acad. Sci. USA 100:4921–26 [Google Scholar]
  30. Jacobs JM, Jacobs NJ. 1993. Porphyrin accumulation and export by isolated Barley (Hordeum vulgare) plastids (effect of diphenyl ether herbicides). Plant Physiol. 101:1181–87 [Google Scholar]
  31. Jasper F, Quednau B, Kortenjann M, Johanningmeier U. 1991. Control of cab gene expression in synchronized Chlamydomonas reinhardtii cells. J. Photochem. Photobiol. B 11:139–50 [Google Scholar]
  32. Johanningmeier U. 1988. Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur. J. Biochem. 177:417–24 [Google Scholar]
  33. Johanningmeier U, Howell SH. 1984. Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors.. J. Biol. Chem. 259:13541–49 [Google Scholar]
  34. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM. 1997. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–40 [Google Scholar]
  35. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–57 [Google Scholar]
  36. Kimura M, Manabe K, Abe T, Yoshida S, Matsui M, Yamamoto YY. 2003. Analysis of hydrogen peroxide-independent expression of the high-light-inducible ELIP2 gene with the aid of the ELIP2 promoter-luciferase fusions. Photochem. Photobiol. 77:668–74 [Google Scholar]
  37. Kimura M, Yoshizumi T, Manabe K, Yamamoto YY, Matsui M. 2001. Arabidopsis transcriptional regulation by light stress via hydrogen peroxide-dependent and -independent pathways. Genes Cells 6:607–17 [Google Scholar]
  38. Kittsteiner U, Brunner H, Rudiger W. 1991. The greening process in cress seedlings. II. Complexing agents and 5-aminolevulinate inhibit accumulation of cab messenger RNA coding for the light-harvesting chloropyll a/b protein. Physiol. Plant 81:190–96 [Google Scholar]
  39. Kochevar IE. 2004. Singlet oxygen signaling: from intimate to global. Sci. STKE 2004:pe7 [Google Scholar]
  40. Kovtun Y, Chiu W-L, Tena G, Sheen J. 2000. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc. Natl. Acad. Sci. USA 97:2940–45 [Google Scholar]
  41. Kropat J, Oster U, Rudiger W, Beck CF. 1997. Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc. Natl. Acad. Sci. USA 94:14168–72 [Google Scholar]
  42. Kropat J, Oster U, Rudiger W, 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. 24:523–31 [Google Scholar]
  43. Kusnetsov V, Bolle C, Lubberstedt T, Sopory S, Herrmann RG, Oelmüller 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. 252:631–39 [Google Scholar]
  44. La Rocca N, Rascio N, Oster U, Rudiger W. 2001. Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 213:101–8 [Google Scholar]
  45. Larkin RM, Alonso JM, Ecker JR, Chory J. 2003. GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–6 [Google Scholar]
  46. Leister D. 2003. Chloroplast research in the genomic age. Trends Genet. 19:47–56 [Google Scholar]
  47. Leon P, Arroyo A, Mackenzie S. 1998. Nuclear control of plastid and mitochondrial development in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49:453–80 [Google Scholar]
  48. Martinez-Hernandez A, Lopez-Ochoa L, Arguello-Astorga G, Herrera-Estrella L. 2002. Functional properties and regulatory complexity of a minimal RBCS light-responsive unit activated by phytochrome, cryptochrome, and plastid signals. Plant Physiol. 128:1223–33 [Google Scholar]
  49. Masuda T, Tanaka A, Melis A. 2003. Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol. Biol. 51:757–71 [Google Scholar]
  50. Maxwell DP, Laudenbach DE, Huner NPA. 1995. Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol. 109:787–95 [Google Scholar]
  51. Mayfield SP, Taylor WC. 1984. Carotenoid-deficient maize seedlings fail to accumulate light-harvesting chlorophyll a/b binding protein (LHCP) mRNA. Eur. J. Biochem. 144:79–84 [Google Scholar]
  52. McCormac AC, Fischer A, Kumar AM, Soll D, Terry MJ. 2001. Regulation of HEMA1 expression by phytochrome and a plastid signal during de-etiolation in Arabidopsis thaliana. Plant J. 25:549–61 [Google Scholar]
  53. McCormac AC, Terry MJ. 2004. The nuclear genes Lhcb and HEMA1 are differentially sensitive to plastid signals and suggest distinct roles for the GUN1 and GUN5 plastid-signaling pathways during de-etiolation. Plant J. 40:672–85 [Google Scholar]
  54. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7:405–10 [Google Scholar]
  55. Moan J. 1990. On the diffusion length of singlet oxygen in cells and tissues. J. Photochem. Photobiol. 6:343–47 [Google Scholar]
  56. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 2001. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl. Acad. Sci. USA 98:2053–58 [Google Scholar]
  57. Montane MH, Kloppstech K. 2000. The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function. Gene 258:1–8 [Google Scholar]
  58. Montane MH, Tardy F, Kloppstech K, Havaux M. 1998. Differential control of xanthophylls and light-induced stress proteins, as opposed to light-harvesting chlorophyll a/b proteins, during photosynthetic acclimation of Barley leaves to light irradiance. Plant Physiol. 118:227–35 [Google Scholar]
  59. Mou Z, Fan W, Dong X. 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–44 [Google Scholar]
  60. Niyogi KK. 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Biol. 50:333–59 [Google Scholar]
  61. Niyogi KK. 2000. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3:455–60 [Google Scholar]
  62. Oelmüller R, Levitan I, Bergfeld R, Rajasekhar VK, Mohr H. 1986. Expression of nuclear genes as affected by treatments acting on the plastids. Planta 168:482–92 [Google Scholar]
  63. Oelmüller R, Mohr H. 1986. Photooxidative destruction of chloroplast and its consequences for expression of nuclear genes. Planta 167:106–13 [Google Scholar]
  64. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C. et al. 2001. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J. 20:2835–43 [Google Scholar]
  65. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C. et al. 2003. Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–32 [Google Scholar]
  66. Oster U, Brunner H, Rudiger 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 36:255–61 [Google Scholar]
  67. Oswald O, Martin T, Dominy PJ, Graham IA. 2001. Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc. Natl. Acad. Sci. USA 98:2047–52 [Google Scholar]
  68. Petracek ME, Dickey LF, Huber SC, Thompson WF. 1997. Light-regulated changes in abundance and polyribosome association of ferredoxin mRNA are dependent on photosynthesis. Plant Cell 9:2291–300 [Google Scholar]
  69. Petracek ME, Dickey LF, Nguyen TT, Gatz C, Sowinski DA. et al. 1998. Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc. Natl. Acad. Sci. USA 95:9009–13 [Google Scholar]
  70. Pfannschmidt T. 2003. Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci. 8:33–41 [Google Scholar]
  71. Pfannschmidt T, Nilsson A, Allen JF. 1999. Photosynthetic control of chloroplast gene expression. Nature 397:625–28 [Google Scholar]
  72. Pfannschmidt T, Schutze K, Brost M, Oelmüller R. 2001. A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J. Biol. Chem. 276:36125–30 [Google Scholar]
  73. Pontoppidan B, Kannangara CG. 1994. Purification and partial characterisation of barley glutamyl-tRNA(Glu) reductase, the enzyme that directs glutamate to chlorophyll biosynthesis. Eur. J. Biochem. 225:529–37 [Google Scholar]
  74. Puente P, Wei N, Deng XW. 1996. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15:3732–43 [Google Scholar]
  75. Rapp JC, Mullet JE. 1991. Chloroplast transcription is required to express the nuclear genes rbcS and cab. Plastid DNA copy number is regulated independently. Plant Mol. Biol. 17:813–23 [Google Scholar]
  76. Reiß T, Bergfeld R, Link G, Thien W, Mohr H. 1983. Photooxidative destruction of chloroplast and its consequence for cytosolic enzyme levels and plant development. Planta 159:518–28 [Google Scholar]
  77. Richly E, Dietzmann A, Biehl A, Kurth J, Laloi C. et al. 2003. Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch. EMBO Rep. 4:491–98 [Google Scholar]
  78. Rissler HM, Collakova E, DellaPenna D, Whelan J, Pogson BJ. 2002. Chlorophyll biosynthesis. Expression of a second chl I gene of magnesium chelatase in Arabidopsis supports only limited chlorophyll synthesis. Plant Physiol 128:770–79 [Google Scholar]
  79. Sherameti I, Nakamura M, Yamamoto YY, Pfannschmidt T, Obokata J, Oelmüller R. 2002. Polyribosome loading of spinach mRNAs for photosystem I subunits is controlled by photosynthetic electron transport. A crucial cis element in the spinach PsaD gene is located in the 5′-untranslated region. Plant J. 32:631–39 [Google Scholar]
  80. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T. et al. 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53:1305–19 [Google Scholar]
  81. Simpson J, Van Montagu M, Herrera-Estrella L. 1986. Photosynthesis-associated gene families: differences in response to tissue-specific and environmental factors. Science 233:34–38 [Google Scholar]
  82. Strand A. 2004. Plastid-to-nucleus signalling. Curr. Opin. Plant Biol. 7:621–25 [Google Scholar]
  83. Strand A, Asami T, Alonso J, Ecker JR, Chory J. 2003. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83 [Google Scholar]
  84. Sullivan JA, 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 11:901–10 [Google Scholar]
  85. Susek RE, Ausubel FM, Chory J. 1993. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–99 [Google Scholar]
  86. Taylor WC. 1989. Regulatory interactions between nuclear and plastid genomes. Ann. Rev. Plant Physiol. Plant Mol. Biol. 40:211–33 [Google Scholar]
  87. Terry MJ, Kendrick RE. 1999. Feedback inhibition of chlorophyll synthesis in the phytochrome chromophore-deficient aurea and yellow-green-2 mutants of tomato. Plant Physiol. 119:143–52 [Google Scholar]
  88. Trebst A. 1980. Inhibitors in electron flow: tools for the functional and structural localization of carriers and energy conservation sites. In Photosynthesis and Nitrogen Fixation–Part C. pp. 675–715 New York: Academic Press [Google Scholar]
  89. Vorst O, Kock P, Lever A, Weterings B, Weisbeek P, Smeekens S. 1993. The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J. 4:933–45 [Google Scholar]
  90. Vothknecht UC, Kannangara CG, von Wettstein D. 1996. Expression of catalytically active barley glutamyl tRNAGlu reductase in Escherichia coli as a fusion protein with glutathione S-transferase. Proc. Natl. Acad. Sci. USA 93:9287–91 [Google Scholar]
  91. Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F. et al. 2004. The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–85 [Google Scholar]
  92. Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B. 2004. The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett. 571:119–23 [Google Scholar]
  93. Yabuta Y, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S. 2004. Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol. 45:1586–94 [Google Scholar]
  94. Yang D-H, Andersson B, Aro E-M, Ohad I. 2001. The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation. Photosynth. Res. 68:163–74 [Google Scholar]
  95. Zhang L, Hach A, Wang C. 1998. Molecular mechanism governing heme signaling in yeast: a higher-order complex mediates heme regulation of the transcriptional activator HAP1. Mol. Cell Biol. 18:3819–28 [Google Scholar]
/content/journals/10.1146/annurev.arplant.57.032905.105310
Loading
/content/journals/10.1146/annurev.arplant.57.032905.105310
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error