Skip to main content

Development-Dependent Changes in the Amount and Structural Organization of Plastid DNA

  • Chapter
  • First Online:

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

Plastids usually contain numerous copies of their genome. The reason of maintaining high copy numbers of the plastome and their changes resulting from developmental, cellular (e.g., nuclear ploidy levels), and environmental cues remains elusive. The DNA is contained in certain regions of the plastids, the nucleoids. Number and shape of nucleoids change during leaf and chloroplast development. Generally, a substantial increase of nucleoids and therefore plastome copy numbers per organelle and cell occurs very early in leaf development, which later on provides not only enough plastomes for the distribution during plastid division, but may also meet the increasing demand for plastid gene products during chloroplast biogenesis. Later in leaf development the fate of chloroplast DNA seems to be regulated in a species-specific manner. While some species further increase the amount of plastid DNA (at least per cell), others seem to decrease plastome copy numbers per cell and per organelle during chloroplast maturation. The amount of chloroplast DNA decreases during senescence.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   329.99
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

Learn about institutional subscriptions

Abbreviations

CND41 –:

41 kDa chloroplast nucleoid DNA binding protein;

DAPI –:

4′,6-diamidino-2-phenylindole;

NEP –:

Nuclear-encoded plastid RNA-polymerase;

PEND –:

Plastid envelope DNA-binding protein;

PEP –:

Plastid-encoded plastid RNA-polymerase;

ppGpp –:

Guanosine 5′-diphosphate 3′-diphosphate;

qPCR –:

Quantitative real-time PCR;

RubBisCO –:

Ribulose-1,5-bisphosphate carboxylase oxygenase;

SN-type –:

Scattered nucleoid type; TAC – Transcriptionally active chromosome

References

  • Aguettaz P, Seyer P, Pesey H, Lescure A-M (1987) Relations between the plastid gene dosage and the levels of 16S rRNA and rbcL gene transcripts during amyloplast to chloroplast change in mixotrophic spinach cell suspensions. Plant Mol Biol 8:169–177

    CAS  Google Scholar 

  • Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci USA 101:7805–7808

    PubMed  CAS  Google Scholar 

  • Backert S, Dorfel P, Börner T (1995) Investigation of plant organellar DNAs by pulsed-field gel electrophoresis. Curr Genet 28:390–399

    PubMed  CAS  Google Scholar 

  • Barow M (2006) Endopolyploidy in seed plants. Bioessays 28:271–281

    PubMed  CAS  Google Scholar 

  • Baumgartner BJ, Mullet JE (1991) Plastid DNA synthesis and nucleic acid-binding proteins in developing barley chloroplasts. J Photochem Photobiol B 11:203–218

    PubMed  CAS  Google Scholar 

  • Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018

    PubMed  CAS  Google Scholar 

  • Bendich AJ (1987) Why do chloroplasts and mitochondria contain so many copies of their genome? Bioessays 6:279–282

    PubMed  CAS  Google Scholar 

  • Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666

    PubMed  CAS  Google Scholar 

  • Bendich AJ (2007) The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts. Bioessays 29:474–483

    PubMed  CAS  Google Scholar 

  • Bennett J, Radcliffe C (1975) Plastid DNA replication and plastid division in the garden pea. FEBS Lett 56:222–225

    PubMed  CAS  Google Scholar 

  • Boffey SA, Leech RM (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol 69:1387–1391

    PubMed  CAS  Google Scholar 

  • Boffey SA, Ellis JR, Selldén G, Leech RM (1979) Chloroplast division and DNA synthesis in light-grown wheat leaves. Plant Physiol 64:502–505

    PubMed  CAS  Google Scholar 

  • Briat JF, Gigot C, Laulhere JP, Mache R (1982) Visualization of a spinach plastid transcriptionally active DNA-protein complex in a highly condensed structure. Plant Physiol 69:1205–1211

    PubMed  CAS  Google Scholar 

  • Briat JF, Letoffe S, Mache R, Rouviere-Yaniv J (1984) Similarity between the bacterial histone-like protein HU and a protein from spinach chloroplasts. FEBS Lett 172:75–79

    CAS  Google Scholar 

  • Bülow S, Reiss T, Link G (1987) DNA-binding proteins of the transcriptionally active chromosome from mustard (Sinapis alba L.) chloroplasts. Curr Genet 12:157–159

    Google Scholar 

  • Butterfass T (1979) Patterns of chloroplast reproduction. A developmental approach to protoplasmic plant anatomy. Springer, Wien

    Google Scholar 

  • Cahoon AB, Harris FM, Stern DB (2004) Analysis of developing maize plastids reveals two mRNA stability classes correlating with RNA polymerase type. EMBO Rep 5:801–806

    PubMed  CAS  Google Scholar 

  • Cannon G, Heinhorst S, Weissbach A (1986) Plastid DNA content in a cultured soybean line capable of photoautotrophic growth. Plant Physiol 80:601–603

    PubMed  CAS  Google Scholar 

  • Cannon GC, Ward LN, Case CI, Heinhorst S (1999) The 68 kDa DNA compacting nucleoid protein from soybean chloroplasts inhibits DNA synthesis in vitro. Plant Mol Biol 39:835–845

    PubMed  CAS  Google Scholar 

  • Cappadocia L, Maréchal A, Parent J-S, Lepage E, Sygusch J, Brisson N (2010) Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 22:1849–1867

    PubMed  CAS  Google Scholar 

  • Chi-Ham CL, Keaton MA, Cannon GC, Heinhorst S (2002) The DNA-compacting protein DCP68 from soybean chloroplasts is ferredoxin:sulfite reductase and co-localizes with the organellar nucleoid. Plant Mol Biol 49:621–631

    PubMed  CAS  Google Scholar 

  • Cho HS, Lee SS, Kim KD, Hwang I, Lim J-S, Park Y-I, Pai H-S (2004) DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell 16:2665–2682

    PubMed  CAS  Google Scholar 

  • Coleman AW (1978) Visualization of chloroplast DNA with two fluorochromes. Exp Cell Res 114:95–100

    PubMed  CAS  Google Scholar 

  • Coleman AW (1979) Use of the fluorochrome 4′6-diamidino-2-phenylindole in genetic and developmental studies of chloroplast DNA. J Cell Biol 82:299–305

    PubMed  CAS  Google Scholar 

  • Crevel G, Laine B, Sautière P, Galleron C (1989) Isolation and characterization of DNA-binding proteins from the cyanobacterium Synechococcus sp. PCC 7002 (Agmenellum quadruplicatum) and from spinach chloroplasts. Biochim Biophys Acta 1007:36–43

    PubMed  CAS  Google Scholar 

  • Dann O, Bergen G, Demant E, Volz G (1971) Trypanocide Diamidine des 2-Phenyl-benzofurans, 2-Phenyl-indens und 2-Phenyl-indols. Liebigs Ann Chem 749:68–89

    CAS  Google Scholar 

  • Dean C, Leech RM (1982) Genome expression during normal leaf development: I. cellular and chloroplast numbers and DNA, RNA, and protein levels in tissues of different ages within a seven-day-old wheat leaf. Plant Physiol 69:904–910

    PubMed  CAS  Google Scholar 

  • Draper CK, Hays JB (2000) Replication of chloroplast, mitochondrial and nuclear DNA during growth of unirradiated and UVB-irradiated Arabidopsis leaves. Plant J 23:255–265

    PubMed  CAS  Google Scholar 

  • Eberhard S, Drapier D, Wollman F-A (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149–160

    PubMed  CAS  Google Scholar 

  • Evans IM, Rus AM, Belanger EM, Kimoto M, Brusslan JA (2010) Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence. Plant Biol 12:1–12

    PubMed  CAS  Google Scholar 

  • Fujie M, Kuroiwa H, Kawano S, Mutoh S, Kuroiwa T (1994) Behavior of organelles and their nucleoids in the shoot apical meristem during leaf development in Arabidopsis thaliana L. Planta 194:395–405

    CAS  Google Scholar 

  • Fulgosi H, Jezic M, Lepedus H, Peharec Stefanic P, Curkovic-Perica M, Cesar V (2012) Degradation of chloroplast DNA during natural senescence of maple leaves. Tree Physiol 32:346–354

    PubMed  CAS  Google Scholar 

  • Grasser KD, Ritt C, Krieg M, Fernández S, Alonso JC, Grimm R (1997) The recombinant product of the Chryptomonas phi plastid gene hlpA is an architectural HU-like protein that promotes the assembly of complex nucleoprotein structures. Eur J Biochem 249:70–76

    PubMed  CAS  Google Scholar 

  • Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66:34–44

    PubMed  CAS  Google Scholar 

  • Gruissem W, Tonkyn JC (1993) Control mechanisms of plastid gene expression. Crit Rev Plant Sci 12:19–55

    CAS  Google Scholar 

  • Hansmann P, Falk H, Ronai K, Sitte P (1985) Structure, composition, and distribution of plastid nucleoids in Narcissus pseudonarcissus. Planta 164:459–472

    CAS  Google Scholar 

  • Hanson MR, Sattarzadeh A (2011) Stromules: recent insights into a long neglected feature of plastid morphology and function. Plant Physiol 155:1486–1492

    PubMed  CAS  Google Scholar 

  • Hashimoto H (1985) Changes in distribution of nucleoids in developing and dividing chloroplasts and etioplasts of Arena sativa. Protoplasma 127:119–127

    Google Scholar 

  • Hashimoto H, Possingham J (1989a) DNA levels in dividing and developing plastids in expanding primary leaves of Avena sativa. J Exp Bot 40:257–262

    CAS  Google Scholar 

  • Hashimoto H, Possingham JV (1989b) Effect of light on the chloroplast division cycle and DNA synthesis in cultured leaf discs of spinach. Plant Physiol 89:1178–1183

    PubMed  CAS  Google Scholar 

  • Herrmann RG (1970) Multiple amounts of DNA related to the size of chloroplasts. I. An autoradiographic study. Planta 90:80–96

    CAS  Google Scholar 

  • Herrmann RG, Kowallik KV (1970) Multiple amounts of DNA related to the size of chloroplasts. II. Comparison of electron-microscopic and autoradiographic data. Protoplasma 69:365–372

    PubMed  CAS  Google Scholar 

  • Herrmann RG, Possingham JV (1980) Plastid DNA – the plastome. In: Reinert J (ed) Results and Problems in Cell Differentiation, vol 10 Chloroplasts, pp. 45–96. Springer Verlag, Berlin/Heidelberg/New York

    Google Scholar 

  • Isono K, Niwa Y, Satoh K, Kobayashi H (1997) Evidence for transcriptional regulation of plastid photosynthesis genes in Arabidopsis thaliana roots. Plant Physiol 114:623–630

    PubMed  CAS  Google Scholar 

  • James TW, Jope C (1978) Visualization by fluorescence of chloroplast DNA in higher plants by means of the DNA-specific probe 4′6-diamidino-2-phenylindole. J Cell Biol 79:623–630

    PubMed  CAS  Google Scholar 

  • Jeong SY, Rose A, Meier I (2003) MFP1 is a thylakoid-associated, nucleoid-binding protein with a coiled-coil structure. Nucl Acids Res 31:5175–5185

    PubMed  CAS  Google Scholar 

  • Jiang CZ, Rodermel SR, Shibles RM (1993) Photosynthesis, RuBisCO activity and amount, and their regulation by transcription in senescing soybean leaves. Plant Physiol 101:105–112

    PubMed  CAS  Google Scholar 

  • Jope CA, Hirai A, Wildman SG (1978) Evidence that the amount of chloroplast DNA exceeds that of nuclear DNA in mature leaves. J Cell Biol 79:631–636

    PubMed  CAS  Google Scholar 

  • Kabeya Y, Nakanishi H, Ishikawa T, Kondou Y, Matsui M, Miyagishima S-Y (2010) The YlmG protein has a conserved function related to the distribution of nucleoids in chloroplasts and cyanobacteria. BMC Plant Biol 10:57

    PubMed  Google Scholar 

  • Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F (2004) The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220:97–104

    PubMed  CAS  Google Scholar 

  • Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144:952–960

    PubMed  CAS  Google Scholar 

  • Khanna NC, Lakhani S, Tewari KK (1992) Identification of the template binding polypeptide in the pea chloroplast transcriptional complex. Nucleic Acids Res 20:69–74

    PubMed  CAS  Google Scholar 

  • Kinoshita I, Tsuji H (1984) Benzyladenine-induced increase in DNA content per chloroplast in intact bean leaves. Plant Physiol 76:575–578

    PubMed  CAS  Google Scholar 

  • Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138

    PubMed  CAS  Google Scholar 

  • Kobayashi T, Takahara M, Miyagishima S-Y, Kuroiwa H, Sasaki N, Ohta N, Matsuzaki M, Kuroiwa T (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14:1579–1589

    PubMed  CAS  Google Scholar 

  • Kowallik KV, Herrmann RG (1972) Variable amounts of DNA related to the size of chloroplasts. IV. Three-dimensional arrangement of DNA in fully differentiated chloroplasts of Beta vulgaris L. J Cell Sci 11:357–377

    Google Scholar 

  • Krause K, Krupinska K (2000) Molecular and functional properties of highly purified transcriptionally active chromosomes from spinach chloroplasts. Physiol Plant 109:188–195

    CAS  Google Scholar 

  • Krause K, Falk J, Humbeck K, Krupinska K (1998) Responses of the transcriptional apparatus of barley chloroplasts to a prolonged dark period and to subsequent reillumination. Physiol Plant 104:143–152

    CAS  Google Scholar 

  • Krause K, Kilbienski I, Mulisch M, Rodiger A, Schafer A, Krupinska K (2005) DNA-binding proteins of the Whirly family in Arabidopsis thaliana are targeted to the organelles. FEBS Lett 579:3707–3712

    PubMed  CAS  Google Scholar 

  • Krupinska K, Falk J (1994) Changes in RNA-polymerase activity during biogenesis, maturation and senescence of barley chloroplasts. Comparative analysis of transcripts synthesized either in run-on assays or by transcriptionally active chromosomes. J Plant Physiol 143:298–305

    CAS  Google Scholar 

  • Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62

    CAS  Google Scholar 

  • Kuroiwa T, Suzuki T (1981) Circular nucleoids isolated from chloroplasts in a brown alga Ectocarpus siliculosus. Exp Cell Res 134:457–461

    PubMed  CAS  Google Scholar 

  • Kuroiwa T, Suzuki T, Ogawa K, Kawano S (1981) The chloroplast nucleus: distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol 22:381–396

    Google Scholar 

  • Lam E, Hanley-Bowdoin L, Chua NH (1988) Characterization of a chloroplast sequence-specific DNA binding factor. J Biol Chem 263:8288–8293

    PubMed  CAS  Google Scholar 

  • Lamppa GK, Bendich AJ (1979) Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol 64:126–130

    PubMed  CAS  Google Scholar 

  • Lamppa G, Elliot L, Bendich A (1980) Changes in chloroplast number during pea leaf development. Planta 148:437–443

    CAS  Google Scholar 

  • Landoulsi A, Malki A, Kern R, Kohiyama M, Hughes P (1990) The E. coli cell surface specifically prevents the initiation of DNA replication at oriC on hemimethylated DNA templates. Cell 63:1053–1060

    PubMed  CAS  Google Scholar 

  • Lawrence ME, Possingham JV (1986) Microspectro­fluorometric measurement of chloroplast DNA in dividing and expanding leaf cells of Spinacia oleracea. Plant Physiol 81:708–710

    Google Scholar 

  • Leutwiler LS, Hough-Evans BR, Meyerowitz EM (1984) The DNA of Arabidopsis thaliana. Mol Gen Genet 194:15–23

    CAS  Google Scholar 

  • Li W, Ruf S, Bock R (2006) Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol Genet Genomics 275:185–192

    PubMed  CAS  Google Scholar 

  • Liere K, Börner T (2007) Transcription of plastid genes. In: Grasser KD (ed) Regulation of transcription in plants, vol. Blackwell Publishing, Oxford, pp 184–224

    Google Scholar 

  • Lindbeck A, Rose R, Lawrence ME, Possingham JV (1987) The role of chloroplast membranes in the location of chloroplast DNA during the greening of Phaseolus vulgaris etioplasts. Protoplasma 139:92–99

    CAS  Google Scholar 

  • Mache R, Lerbs-Mache S (2001) Chloroplast genetic system of higher plants: chromosome replication, chloroplast division and elements of the transcriptional apparatus. Curr Sci 80:217–224

    CAS  Google Scholar 

  • Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, Watkins KP, Barkan A, van Wijk KJ (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 158:156–189

    PubMed  CAS  Google Scholar 

  • Maréchal A, Parent JS, Véronneau-Lafortune F, Joyeux A, Lang BF, Brisson N (2009) Whirly proteins maintain plastid genome stability in Arabidopsis. Proc Natl Acad Sci USA 106:14693–14698

    PubMed  Google Scholar 

  • Margulis L (1970) Origin of eukaryotic cells: evidence and research implications for a theory. Yale University Press, New Haven, Conn

    Google Scholar 

  • 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 18:651–662

    PubMed  CAS  Google Scholar 

  • Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci USA 100:8612–8614

    PubMed  CAS  Google Scholar 

  • Miyagishima S-Y (2011) Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol 155:1533–1544

    PubMed  CAS  Google Scholar 

  • Miyamura S, Nagata T, Kuroiwa T (1986) Quantitative fluorescence microscopy on dynamic changes of plastid nucleoids during wheat development. Protoplasma 133:66–72

    CAS  Google Scholar 

  • Miyamura S, Kuroiwa T, Nagata T (1990) Multiplication and differentiation of plastid nucleoids during development of chloroplasts and etioplasts from proplastids in Triticum aestivum. Plant Cell Physiol 31:597–602

    CAS  Google Scholar 

  • Murakami S, Kondo Y, Nakano T, SATO F (2000) Protease activity of CND41, a chloroplast nucleoid DNA-binding protein, isolated from cultured tobacco cells. FEBS Lett 468:15–18

    PubMed  CAS  Google Scholar 

  • Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65

    PubMed  CAS  Google Scholar 

  • Nakano T, Sato F, Yamada Y (1993) Analysis of nucleoid-proteins in tobacco chloroplasts. Plant Cell Physiol 34:873–880

    CAS  Google Scholar 

  • Nakano T, Murakami S, Shoji T, Yoshida S, Yamada Y, SATO F (1997) A novel protein with DNA binding activity from tobacco chloroplast nucleoids. Plant Cell 9:1673–1682

    PubMed  CAS  Google Scholar 

  • Nemoto Y, Kawano S, Nakamura S, Mita T, Nagata T, Kuroiwa T (1988) Studies on plastid-nuclei (nucleoids) in Nicotiana tabacum L. I. Isolation of proplastid-nuclei from cultured cells and identification of proplastid-nuclear proteins. Plant Cell Physiol 29:167–177

    CAS  Google Scholar 

  • Nemoto Y, Kawano S, Kondoh K, Nagata T, Kuroiwa T (1990) Studies on plastid-nuclei (nucleoids) in Nicotiana tabacum L. III. Isolation of chloroplast-nuclei from mesophyll protoplasts and identification of chloroplast DNA-binding proteins. Plant Cell Physiol 31:767–776

    CAS  Google Scholar 

  • Nemoto Y, Kawano S, Nagata T, Kuroiwa T (1991) Studies on plastid-nuclei (nucleoids) in Nicotiana tabacum L. IV. Association of chloroplast-DNA with proteins at several specific sites in isolated chloroplast-nuclei. Plant Cell Physiol 32:131–141

    CAS  Google Scholar 

  • Ogden GB, Pratt MJ, Schaechter M (1988) The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54:127–135

    PubMed  CAS  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2004) Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. J Mol Biol 344:1311–1330

    PubMed  CAS  Google Scholar 

  • Oldenburg D, Rowan B, Zhao L, Walcher C, Schleh M, Bendich A (2006) Loss or retention of chloroplast DNA in maize seedlings is affected by both light and genotype. Planta 225:41–55

    PubMed  CAS  Google Scholar 

  • Parent J-S, Lepage E, Brisson N (2011) Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis thaliana. Plant Physiol 156:254–262

    PubMed  CAS  Google Scholar 

  • Pascoe MJ, Ingle J (1978) Distinction between nuclear satellite DNAs and chloroplast DNA in higher plants. Plant Physiol 62:975–977

    PubMed  CAS  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz K-J, Oelmüller R (2006) pTAC2, -6 and −12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197

    PubMed  CAS  Google Scholar 

  • Phinney BS, Thelen JJ (2005) Proteomic characterization of a triton-insoluble fraction from chloroplasts defines a novel group of proteins associated with macromolecular structures. J Proteome Res 4:497–506

    PubMed  CAS  Google Scholar 

  • Preuten T, Cincu E, Fuchs J, Zoschke R, Liere K, Börner T (2010) Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells. Plant J 64:948–959

    PubMed  CAS  Google Scholar 

  • Prikryl J, Watkins KP, Friso G, van Wijk KJ, Barkan A (2008) A member of the Whirly family is a multifunctional RNA- and DNA-binding protein that is essential for chloroplast biogenesis. Nucleic Acids Res 36:5152–5165

    PubMed  CAS  Google Scholar 

  • Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556

    PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99:1005–1008

    PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207

    PubMed  CAS  Google Scholar 

  • Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106:1169–1177

    PubMed  CAS  Google Scholar 

  • Rauwolf U, Golczyk H, Greiner S, Herrmann RG (2010) Variable amounts of DNA related to the size of chloroplasts III. Biochemical determinations of DNA amounts per organelle. Mol Genet Genomics 283:35–47

    PubMed  CAS  Google Scholar 

  • Reiss T, Link G (1985) Characterization of transcriptionally active DNA-protein complexes from chloroplasts and etioplasts of mustard (Sinapis alba L.). Eur J Biochem 148:207–212

    PubMed  CAS  Google Scholar 

  • Renner O (1934) Die pflanzlichen Plastiden als selbständige Elemente der genetischen Konstitution. Ber. sächs. Akad. Wiss. Leipzig, Math.-phys. K1 86:241–266

    Google Scholar 

  • Ris H, Plaut W (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13:383–391

    PubMed  CAS  Google Scholar 

  • Rowan BA, Bendich AJ (2009) The loss of DNA from chloroplasts as leaves mature: fact or artefact? J Exp Bot 60:3005–3010

    PubMed  CAS  Google Scholar 

  • Rowan BA, Oldenburg DJ, Bendich AJ (2004) The demise of chloroplast DNA in Arabidopsis. Curr Genet 46:176–181

    PubMed  CAS  Google Scholar 

  • Rowan B, Oldenburg D, Bendich A (2009) A multiple-method approach reveals a declining amount of chloroplast DNA during development in Arabidopsis. BMC Plant Biol 9:3

    PubMed  Google Scholar 

  • Sakai A, Saito C, Inada N, Kuroiwa T (1998) Tran­scriptional activities of the chloroplast-nuclei and proplastid-nuclei isolated from tobacco exhibit different sensitivities to tagetitoxin: implication of the presence of distinct RNA polymerases. Plant Cell Physiol 39:928–934

    PubMed  CAS  Google Scholar 

  • Sato N, Albrieux C, Joyard J, Douce R, Kuroiwa T (1993) Detection and characterization of a plastid envelope DNA-binding protein which may anchor plastid nucleoids. EMBO J 12:555–561

    PubMed  CAS  Google Scholar 

  • Sato N, Ohshima K, Watanabe A, Ohta N, Nishiyama Y, Joyard J, Douce R (1998) Molecular characterization of the PEND protein, a novel bZIP protein present in the envelope membrane that Is the site of nucleoid replication in developing plastids. Plant Cell 10:859–872

    PubMed  CAS  Google Scholar 

  • Sato M, Takahashi K, Ochiai Y, Hosaka T, Ochi K, Nabeta K (2009) Bacterial alarmone, guanosine 5′-diphosphate 3′-diphosphate (ppGpp), predominantly binds the β′ subunit of plastid-encoded plastid RNA polymerase in chloroplasts. Chembiochem 10:1227–1233

    PubMed  CAS  Google Scholar 

  • Scharff LB, Koop H-U (2007) Targeted inactivation of the tobacco plastome origins of replication A and B. Plant J 50:782–794

    PubMed  CAS  Google Scholar 

  • Scott NS, Possingham JV (1980) Chloroplast DNA in expanding spinach leaves. J Exp Bot 31:1081–1092

    Google Scholar 

  • Scott NS, Possingham JV (1983) Changes in chloroplast DNA levels during growth of spinach leaves. J Exp Bot 34:1756–1767

    CAS  Google Scholar 

  • Scott NS, Cain P, Possingham JV (1982) Plastid DNA levels in albino and green leaves of the ‘albostrians’ mutant of Hordeum vulgare. Z Pflanzenphysiol 108:187–192

    CAS  Google Scholar 

  • Scott NS, Tymms MJ, Possingham JV (1984) Plastid-DNA levels in the different tissues of potato. Planta 161:12–19

    CAS  Google Scholar 

  • Sekine K, Hase T, Sato N (2002) Reversible DNA compaction by sulfite reductase regulates transcriptional activity of chloroplast nucleoids. J Biol Chem 277:24399–24404

    PubMed  CAS  Google Scholar 

  • Shaver J, Oldenburg D, Bendich A (2006) Changes in chloroplast DNA during development in tobacco, Medicago truncatula, pea, and maize. Planta 224:72–82

    Google Scholar 

  • Shaver JM, Oldenburg DJ, Bendich AJ (2008) The structure of chloroplast DNA molecules and the effects of light on the amount of chloroplast DNA during development in Medicago truncatula. Plant Physiol 146:1064–1074

    PubMed  CAS  Google Scholar 

  • Sheahan MB, McCurdy DW, Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44:744–755

    PubMed  CAS  Google Scholar 

  • Siemenroth A, Wollgiehn R, Neumann D, Börner T (1981) Synthesis of ribosomal RNA in ribosome-deficient plastids of the mutant “albostrians” of Hordeum vulgare L. Planta 153:547–555

    CAS  Google Scholar 

  • Sodmergen KS, Tano S, Kuroiwa T (1989) Preferential digestion of chloroplast nuclei (nucleoids) during senescence of the coleoptile of Oryza sativa. Protoplasma 152:65–68

    Google Scholar 

  • Sodmergen KS, Tano S, Kuroiwa T (1991) Degrada­tion of chloroplast DNA in 2nd leaves of rice (Oryza sativa) before leaf yellowing. Protoplasma 160:89–98

    Google Scholar 

  • Steiner S, Schröder Y, Pfalz J, Pfannschmidt T (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157:1043–1055

    PubMed  CAS  Google Scholar 

  • Suck R, Zeltz P, Falk J, Acker A, Kössel H, Krupinska K (1996) Transcriptionally active chromosomes (TACs) of barley chloroplasts contain the α-subunit of plastome encoded RNA polymerase. Curr Genet 30:515–521

    PubMed  CAS  Google Scholar 

  • Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168

    PubMed  CAS  Google Scholar 

  • Sugiura M (1995) The chloroplast genome. Essays Biochem 30:49–57

    PubMed  CAS  Google Scholar 

  • Terasawa K, Sato N (2005) Occurrence and characterization of PEND proteins in angiosperms. J Plant Res 118:111–119

    PubMed  CAS  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    PubMed  CAS  Google Scholar 

  • Tymms MJ, Scott NS, Possingham JV (1983) DNA content of Beta vulgaris chloroplasts during leaf cell expansion. Plant Physiol 71:785–788

    PubMed  CAS  Google Scholar 

  • Wang D-Y, Zhang Q, Liu Y, Lin Z-F, Zhang S-X, Sun M-X, Sodmergen (2010) The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance. Plant Cell 22:2402–2416

    PubMed  CAS  Google Scholar 

  • Weber P, Fulgosi H, Piven I, Müller L, Krupindka K, Turini P (2006) TCP34, a nuclear-encoded response regulator-like TPR protein of higher plant chloroplasts. J Mol Biol 357:535–549

    PubMed  CAS  Google Scholar 

  • Wycliffe P, Sitbon F, Wernersson J, Ezcurra I, Ellerstrom M, Rask L (2005) Continuous expression in tobacco leaves of a Brassica napus PEND homologue blocks differentiation of plastids and development of palisade cells. Plant J 44:1–15

    PubMed  CAS  Google Scholar 

  • Yurina NP, Belkina GG, Karapetyan NV, Odintsova MS (1995) Nucleoids of pea chloroplasts: microscopic and chemical characterization. Occurrence of histone-like proteins. Biochem Mol Biol Int 36:145–154

    PubMed  CAS  Google Scholar 

  • Zheng Q, Oldenburg DJ, Bendich AJ (2011) Independent effects of leaf growth and light on the development of the plastid and its DNA content in Zea species. J Exp Bot 62:2715–2730

    PubMed  CAS  Google Scholar 

  • Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50:710–722

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work of the authors was supported by Deutsche Forschungsgemeinschaft (SFB 429). We are thankful to Reinhold G. Herrmann (Munich) and Hieronim Golczyk (Lublin) for providing Fig. 11.1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Börner .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Liere, K., Börner, T. (2013). Development-Dependent Changes in the Amount and Structural Organization of Plastid DNA. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_11

Download citation

Publish with us

Policies and ethics