, Volume 254, Issue 5, pp 1857–1866 | Cite as

Chloroplast differentiation in the growing leaves of Arabidopsis thaliana

Original Article


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.


Transmission electron microscopy Thylakoids Leaf development Chloroplast differentiation Arabidopsis thaliana 


  1. Avramova V, Sprangers K, Beemster GTS (2015) The maize leaf: another perspective on growth regulation. Trends Plant Sci 20:787–797CrossRefPubMedGoogle Scholar
  2. Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 24:1143–1157CrossRefPubMedPubMedCentralGoogle Scholar
  4. Diers L, Schötz F (1966) Über die dreidimensionale Gestaltung des Thylakoidsystems in den Chloroplasten. Planta 70:322–343CrossRefPubMedGoogle Scholar
  5. Embley TM, Martin W (2006) Eukaryotic evolution: changes and challenges. Nature 440:623–630CrossRefPubMedGoogle Scholar
  6. Fasse-Franzisket U (1955) Die Teilung der Proplastiden und Chloroplasten bei Agapanthus umbellatus L’Hérit. Protoplasma 45:194–227CrossRefGoogle Scholar
  7. Freeling M (1992) A conceptual frameword for maize leaf development. Dev Biol 153:44–58CrossRefPubMedGoogle Scholar
  8. Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340CrossRefPubMedGoogle Scholar
  9. Gunning BES (1965) The greening process in plastids. Protoplasma 60:111–130CrossRefGoogle Scholar
  10. Kirk JTO, Tilney-Bassett RAE (1978) The plastids: their chemistry, structure, growth and inheritance. Elsevier, Amsterdam. ISBN 0–444–8022-0Google Scholar
  11. 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 22:433–442CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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):875–891PubMedPubMedCentralGoogle Scholar
  13. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Menke W (1940) Die Lamellarstruktur der Chloroplasten im ultravioletten Licht. Die Naturwissenschaften 28:158–159CrossRefGoogle Scholar
  15. Meyer A (1883) Das Chlorophyllkorn in chemischer, morphologischer und biologischer Beziehung. Arthur Felix, LeipzigGoogle Scholar
  16. Mullet JE (1988) Chloroplast development and gene expression. Ann Rev Plant Phys Plant Mol Biol 39:475–502CrossRefGoogle Scholar
  17. 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. 767–770Google Scholar
  18. Possingham JV (1980) Plastid replication and development in the life cycle of higher plants. Ann Rev Plant Physiol 31:113–129CrossRefGoogle Scholar
  19. Possingham JV, Saurer W (1969) Changes in chloroplast number per cell during leaf development in spinach. Planta 86:186–194CrossRefPubMedGoogle Scholar
  20. Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556CrossRefPubMedPubMedCentralGoogle Scholar
  21. Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93CrossRefPubMedGoogle Scholar
  22. Schimper A (1885) Untersuchungen über die Chlorophyllkörper und die ihnen homologen Gebilde. Jahrb wiss Bot 16:1–27Google Scholar
  23. 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 17:2580–2586CrossRefPubMedPubMedCentralGoogle Scholar
  24. Strugger S (1951) Die Strukturordnung im Chloroplasten. Ber Deut Bot Ges 54:69–83Google Scholar
  25. Tsiantis M, Langdale JA (1998) The formation of leaves. Curr Opin Plant Biol 1:43–48CrossRefPubMedGoogle Scholar
  26. Van Dingenen J, Blomme J, Gonzalez N, Inzé D (2016) Plants grow with a little help from their organelle friends. J Exp Bot 67:6267–6281CrossRefPubMedGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. von Wettstein D (1957) Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden. Exp Cell Res 12:427–506Google Scholar
  29. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Wehrmeyer W, Röbbelen G (1965) Räumliche Aspekte zur Membranschichtung in den Chloroplasten einer Arabidopsis-Mutante unter Auswertung von Serienschnitten. Planta 64:312–329CrossRefGoogle Scholar
  31. Whatley JM (1993) The endosymbiotic origin of chloroplasts. Int Rev Cytol 144:259–299CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Munich Centre for Integrated Protein Science, CIPSMLudwig-Maximilians-Universität MünchenMunichGermany
  2. 2.Department of Biology I, BotanyLudwig-Maximilians-Universität MünchenPlanegg-MartinsriedGermany

Personalised recommendations