Skip to main content

Chloroplast differentiation in the growing leaves of Arabidopsis thaliana

Protoplasma volume 254, pages 1857–1866 (2017)Cite this article

Abstract

Here, we describe the development of chloroplasts and the buildup of the thylakoid membranes in growing Arabidopsis leaves. Organelles were analyzed from three distinct positions, namely, at the tip, the upper leaf margin, and the base from leaves 1, 3, 5, and 7 of 14-day-old plants. Clear developmental gradients are described within a given leaf and between leaves of different age. Chloroplasts at the tip of every leaf are always the most matured within a given leaf, while already at the upper leaf margin a differentiation gradient can be observed from the edge of the leaf toward the midrib. The data presented here can serve as a standard for a subcellular phenotypic analysis in chloroplast biogenesis mutants.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

References

  • Avramova V, Sprangers K, Beemster GTS (2015) The maize leaf: another perspective on growth regulation. Trends Plant Sci 20:787–797

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charuvi D, Kiss V, Nevo R, Shimoni E, Adam Z, Reich Z (2012) Gain and loss of photosynthetic membranes during plastid differentiation in the shoot apex of Arabidopsis. Plant Cell 24:1143–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diers L, Schötz F (1966) Über die dreidimensionale Gestaltung des Thylakoidsystems in den Chloroplasten. Planta 70:322–343

    Article  CAS  PubMed  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution: changes and challenges. Nature 440:623–630

    Article  CAS  PubMed  Google Scholar 

  • Fasse-Franzisket U (1955) Die Teilung der Proplastiden und Chloroplasten bei Agapanthus umbellatus L’Hérit. Protoplasma 45:194–227

    Article  Google Scholar 

  • Freeling M (1992) A conceptual frameword for maize leaf development. Dev Biol 153:44–58

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340

    Article  CAS  PubMed  Google Scholar 

  • Gunning BES (1965) The greening process in plastids. Protoplasma 60:111–130

    Article  Google Scholar 

  • Kirk JTO, Tilney-Bassett RAE (1978) The plastids: their chemistry, structure, growth and inheritance. Elsevier, Amsterdam. ISBN 0–444–8022-0

  • Klein S, Bryan G, Bogorad L (1964) Early stages in the development of plastid fine structure in red and far-red light. J Cell Biol 22:433–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kowalewska L, Mazur R, Suski S, Garstka M, Mostowska A (2016) Three- dimensional visualisation of the tubular-lamellar transformation of the internal plastid membrane network during runner bean chloroplast biogenesis. Plant Cell 28(4):875–891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Gügel IL, Giavalisco P, Zeisler V, Schreiber L, Soll J, Philippar K (2015) FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biol 13(2):e1002053. doi:10.1371/journal.pbio.1002053

    Article  PubMed  PubMed Central  Google Scholar 

  • Menke W (1940) Die Lamellarstruktur der Chloroplasten im ultravioletten Licht. Die Naturwissenschaften 28:158–159

    Article  CAS  Google Scholar 

  • Meyer A (1883) Das Chlorophyllkorn in chemischer, morphologischer und biologischer Beziehung. Arthur Felix, Leipzig

    Google Scholar 

  • Mullet JE (1988) Chloroplast development and gene expression. Ann Rev Plant Phys Plant Mol Biol 39:475–502

    Article  CAS  Google Scholar 

  • Mustárdy L, Buttle K, Steinbach G, Garab G (2008) Three-dimensional architecture of the granum-stroma thylakoid membrane system revealed by electron tomography. In Photosynthesis. Energy from the sun: 14th International Congress on Photosynthesis, Allen JF, Gantt E, Goldbeck JH, B and Osmond, eds (Heidelberg, Germany, Springer), pp. 767–770

  • Possingham JV (1980) Plastid replication and development in the life cycle of higher plants. Ann Rev Plant Physiol 31:113–129

    Article  CAS  Google Scholar 

  • Possingham JV, Saurer W (1969) Changes in chloroplast number per cell during leaf development in spinach. Planta 86:186–194

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93

    Article  CAS  PubMed  Google Scholar 

  • Schimper A (1885) Untersuchungen über die Chlorophyllkörper und die ihnen homologen Gebilde. Jahrb wiss Bot 16:1–27

    Google Scholar 

  • 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 17:2580–2586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strugger S (1951) Die Strukturordnung im Chloroplasten. Ber Deut Bot Ges 54:69–83

    Google Scholar 

  • Tsiantis M, Langdale JA (1998) The formation of leaves. Curr Opin Plant Biol 1:43–48

    Article  CAS  PubMed  Google Scholar 

  • Van Dingenen J, Blomme J, Gonzalez N, Inzé D (2016) Plants grow with a little help from their organelle friends. J Exp Bot 67:6267–6281

    Article  CAS  PubMed  Google Scholar 

  • Vanhaeren H, Gonzales N, Inzé D (2015) A journey through a leaf: Phenomics analysis of leaf growth in Arabidopsis thaliana. The Arabidopsis Book 13:e0181. doi:10.1199/tab.0181

    Article  PubMed  PubMed Central  Google Scholar 

  • von Wettstein D (1957) Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden. Exp Cell Res 12:427–506

  • Walter A, Liebisch F, Hund A (2015) Plant phenotyping: from bean weighing to image analysis. Plant Methods 11:14. doi:10.1186/s13007-015-0056-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Wehrmeyer W, Röbbelen G (1965) Räumliche Aspekte zur Membranschichtung in den Chloroplasten einer Arabidopsis-Mutante unter Auswertung von Serienschnitten. Planta 64:312–329

    Article  Google Scholar 

  • Whatley JM (1993) The endosymbiotic origin of chloroplasts. Int Rev Cytol 144:259–299

    Article  Google Scholar 

Download references

Acknowledgements

This paper is dedicated to the late Prof. P. Sitte University of Freiburg. We gratefully acknowledge the invaluable ongoing discussion and scientific support by Prof. G. Schultz. This work was in parts financed by the Deutsche Forschungsgemeinschaft Cluster of Excellence CIPSM.

Author information

Authors and Affiliations

  1. Munich Centre for Integrated Protein Science, CIPSM, Ludwig-Maximilians-Universität München, Feodor-Lynen- Straße 25, D-81377, Munich, Germany

    Irene L. Gügel & Jürgen Soll

  2. Department of Biology I, Botany, Ludwig-Maximilians-Universität München, Großhaderner Str. 2-4, D-82152, Planegg-Martinsried, Germany

    Irene L. Gügel & Jürgen Soll

Authors
  1. Irene L. Gügel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jürgen Soll
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jürgen Soll.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: Peter Nick

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gügel, I.L., Soll, J. Chloroplast differentiation in the growing leaves of Arabidopsis thaliana . Protoplasma 254, 1857–1866 (2017). https://doi.org/10.1007/s00709-016-1057-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-016-1057-9

Keywords

  • Transmission electron microscopy
  • Thylakoids
  • Leaf development
  • Chloroplast differentiation
  • Arabidopsis thaliana