Skip to main content

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 21))

  • 1449 Accesses

Summary

The chloroplast proteome is encoded by genes that reside in both the chloroplast and the nucleus. This separation of genetic material necessitates a system for coordinating the expression of genes that reside in each compartment. Because the overwhelming majority of genes that encode chloroplast proteins reside in the nucleus, the regulation of nuclear genes by developmental and environmental cues plays a dominant role in chloroplast development and function. However, the chloroplast is not indifferent to its own protein composition. In fact, the chloroplast generates signals that have dramatic effects on the expression of nuclear genes that encode particular chloroplast proteins. Currently it is known that plastids produce at least a few distinct signals during chloroplast development that are required for proper expression of particular nuclear genes that encode components of the photosynthetic machinery. In response to certain environmental signals, mature chloroplasts send additional signals that regulate nuclear gene expression. The molecular nature of most of these plastid-to-nucleus signaling pathways is not well established. However, a number of studies have suggested that accumulation of certain chlorophyll precursors within plastids is a signal that regulates nuclear gene expression during chloroplast development and during the diurnal cycle. Future work in this area should provide detailed molecular information on the influence of chlorophyll synthesis and other plastid-localized metabolism on nuclear gene expression and how plants utilize this formof interorganellar communication during their lifecycles.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Anderson SL and Kay SA (1995) Functional dissection of circadian clock- and phytochrome-regulated transcription of the Arabidopsis CAB2 gene. Proc Natl Acad Sci USA 92: 1500– 1504

    Article  Google Scholar 

  • Anderson SL, Teakle GR, Martino-Catt SJ and 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: 457–470

    Article  PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815

    Article  Google Scholar 

  • Beale SI (1999) Enzymes of chlorophyll synthesis. Photosynth Res 60: 43–73

    Article  CAS  Google Scholar 

  • Block MA, Tewari AK, Albrieux C, Marechal E and Joyard J (2002) The plant S-adenosyl-L-methionine:Mgprotoporphyrin IX methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur J Biochem 269: 240–248

    Article  PubMed  CAS  Google Scholar 

  • Bolle C, Sopory S, Lubberstedt T, Klosgen RB, Herrmann RG and Oelmüller R (1994) The role of plastids in the expression of nuclear genes for thylakoid proteins studied with chimeric β-glucuronidase gene fusions. Plant Physiol 105:1355–1364

    PubMed  CAS  Google Scholar 

  • Bolle C, Kusnetsov VV, Herrmann RG and 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

    Article  PubMed  CAS  Google Scholar 

  • Brusslan JA and Peterson MP (2002) Tetrapyrrole regulation of nuclear gene expression. Photosynth Res 71: 185–194

    Article  PubMed  CAS  Google Scholar 

  • Chen JJ and London IM (1995) Regulation of protein synthesis by heme-regulated eIF-2 alpha kinase. Trends Biochem Sci 20: 105–108

    Article  PubMed  CAS  Google Scholar 

  • Cornah JE, Roper JM, Pal Singh D and Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.). Biochem J 362: 423–432

    Article  PubMed  CAS  Google Scholar 

  • Cornah JE, Terry MJ and Smith AG (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8: 224–230

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ, Kurepa J and Vierstra RD (1999) The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci USA 96: 6541–6546

    Article  PubMed  CAS  Google Scholar 

  • Foster R, Izawa T and Chua N-H (1994) Plant bZIP proteins gather at ACGT elements. FASEB J 8: 192–200

    PubMed  CAS  Google Scholar 

  • Franklin KA, Linley PJ, Montgomery BL, Lagarias JC, Thomas B, Jackson SD and Terry MJ (2003) Misregulation of tetrapyrrole biosynthesis in transgenic tobacco seedlings expressing mammalian biliverdin reductase. Plant J 35: 717– 728

    Article  PubMed  CAS  Google Scholar 

  • Gibson LC, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M and 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 

  • Gough S (1972) Defective synthesis of porphyrins in barley plastids caused by mutation in nuclear genes. Biochem Biophys Acta 286: 36–54

    PubMed  CAS  Google Scholar 

  • Granick S (1959) Magnesium porphyrins formed by barley seedlings treated with $δ$-aminolevulinic acid. Plant Physiol 34: XVIII

    Google Scholar 

  • Gray JC, Sullivan JA, Wang JH, Jerome CA and MacLean D (2003) Coordination of plastid and nuclear gene expression. Philos Trans R Soc Lond B Biol Sci 358: 135–144

    Article  PubMed  CAS  Google Scholar 

  • Hahn D and Kück U (1999) Identification of DNA sequences controlling light- and chloroplast-dependent expression of the lhcb1 gene from Chlamydomonas reinhardtii. Curr Genet 34: 459–466

    Article  PubMed  CAS  Google Scholar 

  • Herrmann RG, Maier RM and Schmitz-Linneweber C (2003) Eukaryotic genome evolution: rearrangement and coevolution of compartmentalized genetic information. Philos TransRSoc Lond B Biol Sci 358: 87–97

    Article  CAS  Google Scholar 

  • Jasper F, Quednau B, Kortenjann M and Johanningmeier U (1991) Control of cab gene expression in synchronized Chlamydomonas reinhardtii cells. Photochem Photobiol 11: 139–150

    Article  CAS  Google Scholar 

  • Johanningmeier U (1988) Possible control of transcript levels by chlorophyll precursors in Chlamydomonas. Eur J Biochem 177: 417–424

    Article  PubMed  CAS  Google Scholar 

  • Johanningmeier U and Howell SH (1984) Regulation of lightharvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardtii. Possible involvement of chlorophyll synthesis precursors. J Biol Chem 259: 13541– 13549

    PubMed  CAS  Google Scholar 

  • Karger GA, Reid JD and Hunter CN (2001) Characterization of the binding of deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex. Biochemistry 40: 9291–9299

    Article  PubMed  CAS  Google Scholar 

  • Kittsteiner U, Brunner H and Rüdiger 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 chlorophyll a/b protein. Physiol Plant 81: 190–196

    Article  CAS  Google Scholar 

  • Kohchi T, Mukougawa K, Frankenberg N, Masuda M, Yokota A and Lagarias JC (2001) The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13: 425–436

    Article  PubMed  CAS  Google Scholar 

  • Köster W (2001) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 152: 291–301

    Article  PubMed  Google Scholar 

  • Kropat J, Oster U, Rüdiger W and 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: 14168–14172

    Article  PubMed  CAS  Google Scholar 

  • Kropat J, Oster U, Rüdiger W and Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24: 523–531

    Article  PubMed  CAS  Google Scholar 

  • Kusnetsov V, Bolle C, Lubberstedt T, Sopory S, Herrmann RG and 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– 639

    PubMed  CAS  Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902–906

    Article  PubMed  CAS  Google Scholar 

  • La Rocca N, Rascio N, Oster U and RüdigerW(2001) Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes. Planta 213: 101–108

    Article  PubMed  Google Scholar 

  • Lübberstedt T, Oelmüller R, Wanner G and Herrmann RG (1994) Interacting cis-elements in the plastocyanin promoter from spinach ensure regulated high-level expression. Mol Gen Genet 242: 602–613

    Article  PubMed  Google Scholar 

  • Martin W and Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118: 9–17

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Hernandez A, Lopez-Ochoa L, Arguello-Astorga G and 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: 1223–1233

    Article  PubMed  CAS  Google Scholar 

  • Mascia P (1978) An analysis of precursors accumulated by several chlorophyll biosynthetic mutants of maize. Mol Gen Genet 161: 237–244

    Article  CAS  Google Scholar 

  • Mayfield SP and 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

    Article  PubMed  CAS  Google Scholar 

  • McCormac AC and Terry MJ (2002) Loss of nuclear gene expression during the phytochrome A-mediated far-red block of greening response. Plant Physiol 130: 402–414

    Article  PubMed  CAS  Google Scholar 

  • 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: 549–561

    Article  PubMed  CAS  Google Scholar 

  • MochizukiN, Susek R and Chory J (1996) An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol 112: 1465–1469

    Article  PubMed  CAS  Google Scholar 

  • 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 Natl Acad Sci USA 98: 2053–2058

    Article  PubMed  CAS  Google Scholar 

  • Møller SG,Kunkel T and Chua N-H (2001)AplastidicABCprotein involved in intercompartmental communication of light signaling. Genes Dev 15: 90–103

    Article  PubMed  Google Scholar 

  • Mullineaux P and Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5: 43–48

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Karpinski S and Creissen GP (2005) Integration of signaling in antioxidant defenses. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 223–239. Springer, Dordrecht

    Google Scholar 

  • Muramoto T, Kohchi T, Yokota A, Hwang I and Goodman, HM (1999) The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11: 335–348

    Article  PubMed  CAS  Google Scholar 

  • Nakayama M, Masuda T, Bando T, Yamagata H, Ohta H and Takamiya K (1998) Cloning and expression of the soybean chlH gene encoding a subunit of Mg-chelatase and localization of the Mg2+ concentration-dependent ChlH protein within the chloroplast. Plant Cell Physiol 39: 275–284

    PubMed  CAS  Google Scholar 

  • O’Brian MR and Thony-Meyer L (2002) Biochemistry, regulation and genomics of heme biosynthesis in prokaryotes. Adv Microb Physiol 46: 257–318

    Article  PubMed  CAS  Google Scholar 

  • Oelmüller, R (1989) Photooxidative destruction of chloroplasts and its effect on nuclear gene expression and extraplastidic enzyme levels. Photochem Photobiol 49: 229–239

    Article  Google Scholar 

  • 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 lightregulated expression ofLhc genes. Photochem Photobiol 36: 255–261

    Article  CAS  Google Scholar 

  • OsterlundMT, Hardtke CS, WeiNand DengXW(2000)Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462–466

    Article  PubMed  CAS  Google Scholar 

  • Papenbrock J, Mock H-P, Kruse E and Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208: 264–273

    Article  CAS  Google Scholar 

  • Pfannschmidt, T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8: 33–41

    Article  PubMed  CAS  Google Scholar 

  • 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: 40–45

    Google Scholar 

  • Puente P, Wei N and Deng X-W (1996) Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J 15: 3732–3743

    PubMed  CAS  Google Scholar 

  • Qi Z and O’Brian MR (2002) Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol Cell 9: 155–162

    Article  PubMed  CAS  Google Scholar 

  • Reinbothe C and Reinbothe S (2005) Regulation of photosynthetic gene expression by the environment: from seedling deetiolation to leaf senescence. In: Demmig-Adams B, Adams WW III and Mattoo AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, pp 333–365. Springer, Dordrecht

    Google Scholar 

  • Reinbothe S, Reinbothe C, Apel K and Lebedev N (1996) Evolution of chlorophyll biosynthesis-the challenge to survive photooxidation. Cell 86: 703–705

    Article  PubMed  CAS  Google Scholar 

  • 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: 491–498

    Article  PubMed  CAS  Google Scholar 

  • Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6: 471–478

    Article  PubMed  CAS  Google Scholar 

  • Rodermel S and Park S (2003) Pathways of intracellular communication: Tetrapyrroles and plastid-to-nucleus signaling. Bioessays 25: 631–636

    Article  PubMed  CAS  Google Scholar 

  • Sassa S and Nagai T (1996) The role of heme in gene expression. Int J Hematol 63: 167–178

    Article  PubMed  CAS  Google Scholar 

  • Seo HS,Yang JY, Ishikawa M, Bolle C, BallesterosML and Chua N-H (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 424: 995–999

    Article  CAS  Google Scholar 

  • Seo HS, Watanabe E, Tokutomi S, Nagatani A and Chua N-H (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev In press

    Google Scholar 

  • Shirihai OS, Gregory T, Yu C, Orkin SH and Weiss MJ (2000) ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation. EMBO J 19: 2492– 2502

    Article  PubMed  CAS  Google Scholar 

  • Strand A ˆ, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421: 79–83

    Article  PubMed  CAS  Google Scholar 

  • 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: 901–910

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JA and Gray JC (2000) The pea light-independent photomorphogenesis1 mutant results from partial duplication of COP1 generating an internal promoter and producing two distinct transcripts. Plant Cell 12: 1927–1938

    Article  PubMed  CAS  Google Scholar 

  • Surpin M, Larkin RM and Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14: S327– S338

    PubMed  CAS  Google Scholar 

  • Susek R and Chory J (1992) A tale of two genomes: role of a chloroplast signal in coordinating nuclear and plastid genome expression. Aust J Plant Physiol 19: 387–399

    Article  CAS  Google Scholar 

  • 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: 787–799

    Article  PubMed  CAS  Google Scholar 

  • Takamiya KI, Tsuchiya T, and Ohta H (2000) Degradation pathway( s) of chlorophyll:what has gene cloning revealed? Trends Plant Sci 5: 426–431

    Article  PubMed  CAS  Google Scholar 

  • Terry MJ, Wahleithner JA and Lagarias JC (1993) Biosynthesis of the plant photoreceptor phytochrome. Arch Biochem Biophys 306: 1–15

    Article  PubMed  CAS  Google Scholar 

  • Terzaghi WB and Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46: 445–474

    Article  CAS  Google Scholar 

  • Thomas J and Weinstein JD (1990) Measurement of heme efflux and heme content in isolated developing cotyledons. Plant Physiol 94: 1414–1423

    Article  PubMed  CAS  Google Scholar 

  • Tottey S, BlockMA,Allen M,WestergrenT, 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: 16119–16124.

    Article  PubMed  CAS  Google Scholar 

  • Vinti G, Hills A, Campbell S, Bowyer JR, Mochizuki N, Chory J and Lopez-Juez E (2000) Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signaling. Plant J 24: 883– 894

    Article  PubMed  CAS  Google Scholar 

  • Whyte BJ and Castelfranco PA (1993) Breakdown of thylakoid pigments by soluble proteins of developing chloroplasts. Biochem J 290: 361–367

    PubMed  CAS  Google Scholar 

  • 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– 426

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Larkin, R.M. (2008). Intracellular Signaling and Chlorophyll Synthesis. In: Demmig-Adams, B., Adams, W.W., Mattoo, A.K. (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration, vol 21. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3579-9_18

Download citation

Publish with us

Policies and ethics