Advertisement

Biogenesis of Chloroplasts

  • Simon Geir MøllerEmail author
  • Jodi Maple
  • Daniela Gargano
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)

Summary

Chloroplasts belong to a diverse family of plant organelles called plastids that perform essential functions, including important steps in many biosynthetic pathways. All plastids differentiate from proplastids through a complex process, in which numerous events must be coordinated and integrated into the overall developmental pathway of the cell. Due to the overwhelming importance of chloroplasts as sites of oxygenic photosynthesis the differentiation of chloroplasts from proplastids has been most studied. Chloroplast biogenesis begins with the perception of light, which triggers the coordinated expression of genetic information contained in both the nuclear and plastid genomes. Subsequently the chloroplast protein import machinery plays a major role in organelle biogenesis, mediating the import of nuclear-encoded proteins into the organelle. This process is challenged by the complex organization of the chloroplast sub-compartments. The conversion of sunlight into chemical energy by the photosynthetic machinery requires thylakoid membranes, a specialized membrane system found in chloroplasts, and this process involving a complex cascade of biochemical and structural events. Here we will address the major molecular events following the initiation of chloroplast biogenesis, culminating in the formation of the mature chloroplast and the segregation of plastids to daughter cells during cell division.

Keywords

Thylakoid Membrane Chloroplast Development Chloroplast Division Division Site Plastid Division 
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:

ARC

– Accumulation and replication of chloroplast;

ATP

– Adenosine-5’-triphosphate;

Cry

– Cryptochromes;

GTP

– Guanosine-5’-triphosphate;

LHCII

– Light harvesting complex II;

NADPH

– Nicotinamide adenine dinucleotide phosphate;

NEP

– Nuclear encoded polymerase;

PDV

– Plastid division proteins;

PEP

– Plastid encoded polymerase;

PIFs

– phytochrome-interacting factor;

PSI

– Photosystem I;

PSII

– Photosystem II;

TIC

– Translocon at the inner envelope membrane of chloroplasts;

TOC

– Translocon at the outer envelope membrane of chloroplasts;

VIPP

– Vesicle-inducing protein in plastids

Notes

Acknowledgments

Plastid division research in our laboratory is funded by the Norwegian Research Council.

References

  1. Adam Z, Charuvi D, Tsabari O, Knopf RR, Reich Z (2010) Biogenesis of thylakoid networks in angiosperms: knowns and unknowns. Plant Mol Biol. doi: 10.1007/s11103-010-9693-5 PubMedGoogle Scholar
  2. Al-Sady B, Ni W, Kircher S, Schafer E, Quail PH (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23:439–446PubMedCrossRefGoogle Scholar
  3. Asano T, Yoshioka Y, Kurei S, Sakamoto W, Machida Y (2004) A mutation of the CRUMPLED LEAF gene that encodes a protein localized in the outer envelope membrane of plastids affects the pattern of cell division, cell differentiation, and plastid division in Arabidopsis. Plant J 38:448–459PubMedCrossRefGoogle Scholar
  4. Austin J II, Webber AN (2005) Photosynthesis in Arabidopsis thaliana mutants with reduced chloroplast number. Photosynth Res 85:373–384CrossRefGoogle Scholar
  5. Azevedo J, Courtois F, Hakimi MA, Demarsy E, Lagrange T, Alcaraz JP, Jaiswal P, Marechal-Drouard L, Lerbs-Mache S (2008) Intraplastidial trafficking of a phage-type RNA polymerase is mediated by a thylakoid RING-H2 protein. Proc Natl Acad Sci U S A 105:9123–9128PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203–207PubMedCrossRefGoogle Scholar
  7. Block MA, Dorne AJ, Joyard J, Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts II. Biochemical characterization. J Biol Chem 258:13281–13286PubMedGoogle Scholar
  8. Bohne AV, Weihe A, Borner T (2009) Transfer RNAs inhibit Arabidopsis phage-type RNA polymerases. Endocytobiosis Cell Res 19:63–69, 7pGoogle Scholar
  9. Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521PubMedCrossRefGoogle Scholar
  10. Chen Y, Asano T, Fujiwara MT, Yoshida S, Machida Y, Yoshioka Y (2009) Plant cells without detectable plastids are generated in the crumpled leaf mutant of Arabidopsis thaliana. Plant Cell Physiol 50:956–969PubMedCrossRefGoogle Scholar
  11. Chen M, Galvao RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141:1230–1240PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chory J (2010) Light signal transduction: an infinite spectrum of possibilities. Plant J 61:982–991PubMedCentralPubMedCrossRefGoogle Scholar
  13. Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, Li HM (2003) Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J 22:2970–2980PubMedCentralPubMedCrossRefGoogle Scholar
  14. Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516PubMedCrossRefGoogle Scholar
  15. Constan D, Froehlich JE, Rangarajan S, Keegstra K (2004) A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 136:3605–3615PubMedCentralPubMedCrossRefGoogle Scholar
  16. Cran DG, Possingham JV (1972) Variation of plastid types in spinach. Protoplasma 74:345–356CrossRefGoogle Scholar
  17. Fujiwara M, Nagashima A, Kanamaru K, Tanaka K, Takahashi H (2000) Three new nuclear genes, sigD, sigE and sigF, encoding putative plastid RNA polymerase sigma factors in Arabidopsis thaliana. FEBS Lett 481:47–52PubMedCrossRefGoogle Scholar
  18. Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci U S A 100:4328–4333PubMedCentralPubMedCrossRefGoogle Scholar
  19. Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470PubMedCentralPubMedCrossRefGoogle Scholar
  20. Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711PubMedCrossRefGoogle Scholar
  21. Hajdukiewicz PT, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16:4041–4048PubMedCentralPubMedCrossRefGoogle Scholar
  22. Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep 6:545–550PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hinnah SC, Wagner R, Sveshnikova N, Harrer R, Soll J (2002) The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys J 83:899–911PubMedCentralPubMedCrossRefGoogle Scholar
  24. Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll-protein complex. FEBS Lett 292:1–4PubMedCrossRefGoogle Scholar
  25. Inaba T, Li M, Alvarez-Huerta M, Kessler F, Schnell DJ (2003) atTic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. J Biol Chem 278:38617–38627PubMedCrossRefGoogle Scholar
  26. Isono K, Shimizu M, Yoshimoto K, Niwa Y, Satoh K, Yokota A, Kobayashi H (1997) Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of sigma70 factors of bacterial RNA polymerases in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94:14948–14953PubMedCentralPubMedCrossRefGoogle Scholar
  27. Ivanova Y, Smith MD, Chen K, Schnell DJ (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 15:3379–3392PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kakizaki T, Inaba T (2010) New insights into the retrograde signaling pathway between the plastids and the nucleus. Plant Signal Behav 5:196–199PubMedCentralPubMedCrossRefGoogle Scholar
  29. Kessler F, Blobel G, Patel HA, Schnell DJ (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266:1035–1039PubMedCrossRefGoogle Scholar
  30. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci U S A 98:4238–4242PubMedCentralPubMedCrossRefGoogle Scholar
  31. Kubis S, Baldwin A, Patel R, Razzaq A, Dupree P, Lilley K, Kurth J, Leister D, Jarvis P (2003) The Arabidopsis pp i1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 15:1859–1871PubMedCentralPubMedCrossRefGoogle Scholar
  32. Lopez-Juez E, Dillon E, Magyar Z, Khan S, Hazeldine S, de Jager SM, Murray JA, Beemster GT, Bogre L, Shanahan H (2008) Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20:947–968PubMedCentralPubMedCrossRefGoogle Scholar
  33. Lubeck J, Soll J, Akita M, Nielsen E, Keegstra K (1996) Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J 15:4230–4238PubMedCentralPubMedGoogle Scholar
  34. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607PubMedCentralPubMedCrossRefGoogle Scholar
  35. Maple J, Chua NH, Moller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31:269–277PubMedCrossRefGoogle Scholar
  36. Marrison JL, Rutherford SM, Robertson EJ, Lister C, Dean C, Leech RM (1999) The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J 18:651–662PubMedCrossRefGoogle Scholar
  37. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99:12246–12251PubMedCentralPubMedCrossRefGoogle Scholar
  38. McFadden GI (2001) Chloroplast origin and integration. Plant Physiol 125:50–53PubMedCentralPubMedCrossRefGoogle Scholar
  39. Miras S, Salvi D, Piette L, Seigneurin-Berny D, Grunwald D, Reinbothe C, Joyard J, Reinbothe S, Rolland N (2007) Toc159- and Toc75-independent import of a transit sequence-less precursor into the inner envelope of chloroplasts. J Biol Chem 282:29482–29492PubMedCrossRefGoogle Scholar
  40. Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517–2530PubMedCentralPubMedCrossRefGoogle Scholar
  41. Morre DJ, Sellden G, Sundqvist C, Sandelius AS (1991) Stromal low temperature compartment derived from the inner membrane of the chloroplast envelope. Plant Physiol 97:1558–1564PubMedCentralPubMedCrossRefGoogle Scholar
  42. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667PubMedCrossRefGoogle Scholar
  43. Ni M, Tepperman JM, Quail PH (1999) Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400:781–784PubMedCrossRefGoogle Scholar
  44. Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima SY (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21:1769–1780PubMedCentralPubMedCrossRefGoogle Scholar
  45. Osterlund MT, Wei N, Deng XW (2000) The roles of photoreceptor systems and the COP1-targeted destabilization of HY5 in light control of Arabidopsis seedling development. Plant Physiol 124:1520–1524PubMedCentralPubMedCrossRefGoogle Scholar
  46. Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004PubMedCentralPubMedGoogle Scholar
  47. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197PubMedCentralPubMedCrossRefGoogle Scholar
  48. Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556PubMedCentralPubMedCrossRefGoogle Scholar
  49. Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93PubMedCrossRefGoogle Scholar
  50. Raynaud C, Perennes C, Reuzeau C, Catrice O, Brown S, Bergounioux C (2005) Cell and plastid division are coordinated through the prereplication factor AtCDT1. Proc Natl Acad Sci U S A 102:8216–8221PubMedCentralPubMedCrossRefGoogle Scholar
  51. Robinson C, Thompson SJ, Woolhead C (2001) Multiple pathways used for the targeting of thylakoid proteins in chloroplasts. Traffic 2:245–251PubMedCrossRefGoogle Scholar
  52. Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, Rubio V, Ma L, Hoecker U, Deng XW (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17:2642–2647PubMedCentralPubMedCrossRefGoogle Scholar
  53. Schroeder DF, Gahrtz M, Maxwell BB, Cook RK, Kan JM, Alonso JM, Ecker JR, Chory J (2002) De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr Biol 12:1462–1472PubMedCrossRefGoogle Scholar
  54. Shiina T, Tsunoyama Y, Nakahira Y, Khan MS (2005) Plastid RNA polymerases, promoters, and transcription regulators in higher plants. Int Rev Cytol 244:1–68PubMedCrossRefGoogle Scholar
  55. Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17:2580–2586PubMedCentralPubMedCrossRefGoogle Scholar
  56. Simidjiev I, Stoylova S, Amenitsch H, Javorfi T, Mustardy L, Laggner P, Holzenburg A, Garab G (2000) Self-assembly of large, ordered lamellae from non-bilayer lipids and integral membrane proteins in vitro. Proc Natl Acad Sci U S A 97:1473–1476PubMedCentralPubMedCrossRefGoogle Scholar
  57. Sperling U, Franck F, van Cleve B, Frick G, Apel K, Armstrong GA (1998) Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10:283–296PubMedCentralPubMedGoogle Scholar
  58. Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326PubMedCrossRefGoogle Scholar
  59. Tetlow IJ, Rawsthorne S, Rines C, Emes MJ (2005) Plastid metabolic pathways. In: Moller SG (ed) Plastids. Blackwell, Oxford, pp 60–109Google Scholar
  60. Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933PubMedCentralPubMedCrossRefGoogle Scholar
  61. von Arnim A, Deng XW (1996) Light control of seedling development. Annu Rev Plant Physiol Plant Mol Biol 47:215–243CrossRefGoogle Scholar
  62. Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101PubMedCrossRefGoogle Scholar
  63. Waters MT, Moylan EC, Langdale JA (2008) GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J 56:432–444PubMedCrossRefGoogle Scholar
  64. Westphal S, Heins L, Soll U, Vothknecht UC (2001) Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis. Proc Natl Acad Sci U S A 98:4243–4248PubMedCentralPubMedCrossRefGoogle Scholar
  65. Yanagawa Y, Sullivan JA, Komatsu S, Gusmaroli G, Suzuki G, Yin J, Ishibashi T, Saijo Y, Rubio V, Kimura S, Wang J, Deng XW (2004) Arabidopsis COP10 forms a complex with DDB1 and DET1 in vivo and enhances the activity of ubiquitin conjugating enzymes. Genes Dev 18:2172–2181PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  • Simon Geir Møller
    • 1
    Email author
  • Jodi Maple
    • 2
  • Daniela Gargano
    • 2
  1. 1.Department of Biological SciencesSt. John’s UniversityNew YorkUSA
  2. 2.Faculty of Science and Technology, Centre for Organelle ResearchUniversity of StavangerStavangerNorway

Personalised recommendations