Skip to main content
SpringerLink
Log in

High biological variability of plastids, photosynthetic pigments and pigment forms of leaf primordia in buds

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

To study the formation of the photosynthetic apparatus in nature, the carotenoid and chlorophyllous pigment compositions of differently developed leaf primordia in closed and opening buds of common ash (Fraxinus excelsior L.) and horse chestnut (Aesculus hippocastanum L.) as well as in closed buds of tree of heaven (Ailanthus altissima P. Mill.) were analyzed with HPLC. The native organization of the chlorophyllous pigments was studied using 77 K fluorescence spectroscopy, and plastid ultrastructure was investigated with electron microscopy. Complete etiolation, i.e., accumulation of protochlorophyllide, and absence of chlorophylls occurred in the innermost leaf primordia of common ash buds. The other leaf primordia were partially etiolated in the buds and contained protochlorophyllide (0.5–1 μg g−1 fresh mass), chlorophyllides (0.2–27 μg g−1 fresh mass) and chlorophylls (0.9–643 μg g−1 fresh mass). Etio-chloroplasts with prolamellar bodies and either regular or only low grana were found in leaves having high or low amounts of chlorophyll a and b, respectively. After bud break, etioplast–chloroplast conversion proceeded and the pigment contents increased in the leaves, similarly to the greening processes observed in illuminated etiolated seedlings under laboratory conditions. The pigment contents and the ratio of the different spectral forms had a high biological variability that could be attributed to (i) various light conditions due to light filtering in the buds resulting in differently etiolated leaf primordia, (ii) to differences in the light-exposed and inner regions of the same primordia in opening buds due to various leaf folding, and (iii) to tissue-specific slight variations of plastid ultrastructure.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

Ant:

Antheraxanthin

Chl:

Chlorophyll

Chl a/b :

Ratio of Chl a and b

Chlide:

Chlorophyllide

Neo:

Neoxanthin

Pchl:

Protochlorophyll, i.e., protochlorophyllide esters

Pchlide:

Protochlorophyllide

Pchl(ide):

Protochlorophyllide and/or its esters

Pchl(ide)/Chl(ide):

Ratio of protochlorophyllide + protochlorophyll and chlorophyllides + chlorophylls

PLB:

Prolamellar body

Viola:

Violaxanthin

Zea:

Zeaxanthin

References

  • Abdelkader AF, Aronsson H, Solymosi K, Böddi B, Sundqvist C (2007) High salt stress induces swollen prothylakoids in dark-grown wheat and alters both prolamellar body transformation and reformation after irradiation. J Exp Bot 58:2553–2564

    Article  PubMed  CAS  Google Scholar 

  • Amirjani MR, Sundqvist C (2004) Regeneration of protochlorophyllide in green and greening leaves of plants with varying proportions of protochlorophyllide forms in darkness. Physiol Plant 121:377–390

    Article  CAS  Google Scholar 

  • Barry P, Young AJ, Britton G (1991) Accumulation of pigments during the greening of etiolated seedlings of Hordeum vulgare L. J Exp Bot 42:229–234

    Article  CAS  Google Scholar 

  • Bennett J, Schwender JR, Shaw EK, Tempel N, Ledbetter M, Williams RS (1987) Failure of corn leaves to acclimate to low irradiance. Role of protochlorophyllide reductase in regulating levels of five chlorophyll-binding proteins. Biochim Biophys Acta 892:118–129

    Article  CAS  Google Scholar 

  • Berry DR, Smith H (1971) Red-light stimulation of prolamellar body recrystallization and thylakoid formation in barley etioplasts. J Cell Sci 8:188–200

    Google Scholar 

  • Bertrand M, Schoefs B (1999) Photosynthetic pigment metabolism in plants during stress. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 527–544

    Google Scholar 

  • Biswal UC, Biswal B, Raval MK (2003) Chloroplast biogenesis from proplastid to gerontoplast. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Böddi B, Lindsten A, Ryberg M, Sundqvist C (1989) On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol Plant 76:135–143

    Article  Google Scholar 

  • Böddi B, McEwen B, Ryberg M, Sundqvist C (1994) Protochlorophyllide forms in non-greening epicotyls of dark-grown pea (Pisum sativum). Physiol Plant 92:706–713

    Article  Google Scholar 

  • Böddi B, Lindsten A, Sundqvist C (1999) Chlorophylls in dark-grown epicotyl and stipula of pea. J Photochem Photobiol B Biol 48:11–16

    Article  Google Scholar 

  • Böddi B, Bóka K, Sundqvist C (2004) Tissue specific protochlorophyll(ide) forms in dark-forced shoots of grapevine (Vitis vinifera L.). Photosynth Res 82:141–150

    Article  PubMed  Google Scholar 

  • Darko E, Schoefs B, Lemoine Y (2000) Improved liquid chromatographic method for the analysis of photosynthetic pigments of higher plants. J Chromatography A 876:111–116

    Article  CAS  Google Scholar 

  • Fodor F, Böddi B, Sárvári É, Záray G, Cseh E, Láng F (1995) Correlation of iron content, spectral forms of chlorophyll and chlorophyll-proteins in iron deficient cucumber (Cucumis sativus). Physiol Plant 93:750–756

    Article  CAS  Google Scholar 

  • Franck F (1990) Development of PS II photochemistry after a single white flash in etiolated barley leaves. In: Baltscheffsky M (ed) Current research in photosynthesis, vol 3. Kluwer Academic Publisher, Dordrecht, pp 751–754

    Google Scholar 

  • Franck F, Strzałka K (1992) Detection of the photoactive protochlorophyllide–protein complex in the light during the greening of barley. FEBS Lett 309:73–77

    Article  PubMed  CAS  Google Scholar 

  • Franck F, Barthélemy X, Strzałka K (1993) Spectroscopic characterization of protochlorophyllide photoreduction in the greening leaf. Photosynthetica 29:185–194

    CAS  Google Scholar 

  • Franck F, Schoefs B, Barthélemy X, Myśliwa-Kurdziel B, Strzałka K, Popovic R (1995) Protection of native chlorophyll(ide) forms and of photosystem II against photodamage during the early stages of chloroplast differentiation. Acta Physiol Plant 17:123–132

    CAS  Google Scholar 

  • Grumbach KH (1981) Formation of photosynthetic pigments and quinones and development of photosynthetic activity in barley etioplasts during greening in intermittent and continuous white light. Physiol Plant 51:53–62

    Article  CAS  Google Scholar 

  • Gunning BES (1965) The greening process in plastids. 1. The structure of the prolamellar body. Protoplasma 60:111–130

    Article  Google Scholar 

  • He Z-H, Li J, Sundqvist C, Timko MP (1994) Leaf developmental age controls expression of genes encoding enzymes of chlorophyll and heme biosynthesis in pea (Pisum sativum). Plant Physiol 106:537–546

    PubMed  CAS  Google Scholar 

  • Hoober JK, Eggink LL, Chen M (2007) Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynth Res 94:387–400

    Article  PubMed  CAS  Google Scholar 

  • Kasemir H, Bergfeld R, Mohr H (1975) Phytochrome-mediated control of prolamellar body reorganization and plastid size in mustard cotyledons. Photochem Photobiol 21:111–120

    Article  PubMed  CAS  Google Scholar 

  • Klein S, Schiff JK (1972) The correlated appearance of prolamellar bodies, protochlorophyllide species, and the Shibata shift during development of bean etioplasts in the dark. Plant Physiol 49:619–626

    Article  PubMed  CAS  Google Scholar 

  • Kruk J (2005) Occurrence of chlorophyll precursors in leaves of cabbage heads—the case of natural etiolation. J Photochem Photobiol B Biol 80:187–194

    Article  CAS  Google Scholar 

  • Lancer HA, Cohen CE, Schiff JA (1976) Changing ratios of phototransformable protochlorophyll and protochlorophyllide of bean seedlings developing in the dark. Plant Physiol 57:369–374

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Becker K (1970) Inhibition of the light-induced vitamin K1 and pigment synthesis by abscisic acid. Phytochemistry 9:2109–2113

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Meier D, Buschmann C (1984) Development of chloroplasts at high and low light quanta fluence rates. Isr J Bot 33:185–194

    CAS  Google Scholar 

  • Minkov IN, Ryberg M, Sundqvist C (1988) Properties of reformed prolamellar bodies from illuminated and redarkened etiolated wheat plants. Physiol Plant 72:725–732

    Article  CAS  Google Scholar 

  • Oliver RP, Griffiths WT (1982) Pigment–protein complexes of illuminated etiolated leaves. Plant Physiol 70:1019–1025

    Article  PubMed  CAS  Google Scholar 

  • Ouazzani-Chahdi MA, Schoefs B, Franck F (1998) Isolation and characterisation of photoactive complexes of NADPH:protochlorophyllide oxidoreductase from wheat. Planta 206:673–680

    Article  Google Scholar 

  • Pukacki P, Giertych M, Chalupka W (1980) Light filtering function of bud scales in woody plants. Planta 140:132–133

    Article  Google Scholar 

  • Ryberg M, Sundqvist C (1982) Spectral forms of protochlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol Plant 56:133–138

    Article  CAS  Google Scholar 

  • Ryberg H, Axelsson L, Widell K-O, Virgin HI (1980) Chlorophyll b accumulation and grana formation in low intensities of red light. Physiol Plant 49:431–436

    Article  CAS  Google Scholar 

  • Schiff JA, Epstein HT (1966) The relative aspect of chloroplast continuity in Euglena. In: Goodwin TW (ed) Biochemistry of chloroplasts, vol I. Academic Press, London, New York, pp 341–353

    Google Scholar 

  • Schoefs B (2004) Determination of pigments in vegetables. J Chromatography A 1054:217–226

    Article  CAS  Google Scholar 

  • Schoefs B, Franck F (1991) Photosystem II assembly in 2-day-old bean leaves during the first 16 h of greening. C R Acad Sci Paris Série III 314:441–445

    Google Scholar 

  • Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolution. Photochem Photobiol 78:543–557

    Article  PubMed  CAS  Google Scholar 

  • Schoefs B, Franck F (2008) The photoenzymatic cycle of NADPH:protochlorophyllide oxidoreductase in primary bean leaves (Phaseolus vulgaris) during the first days of photoperiodic growth. Photosynth Res 96:15–26

    Article  PubMed  CAS  Google Scholar 

  • Schoefs B, Bertrand M, Franck F (1992) Plant greening—biogenesis of photosynthetic apparatus in bean leaves irradiated shortly after germination. Photosynthetica 27:497–504

    CAS  Google Scholar 

  • Schoefs B, Garnir HP, Bertrand M (1994) Comparison of the photoreduction of protochlorophyllide to chlorophyllide in leaves and cotyledons from dark-grown bean as a function of age. Photosynth Res 41:405–417

    Article  CAS  Google Scholar 

  • Schoefs B, Bertrand M, Lemoine Y (1995) Separation of photosynthetic pigments and their precursors by reversed-phase high-performance liquid chromatography using a photodiode array detector. J Chromatography A 692:239–245

    Article  CAS  Google Scholar 

  • Schoefs B, Bertrand M, Lemoine Y (1998) Changes in the photosynthetic pigments in bean leaves during the first photoperiod of greening and the subsequent dark-phase. Comparison between old (10 day-old) leaves and young (2 day-old) leaves. Photosynth Res 57:203–213

    Article  Google Scholar 

  • Schoefs B, Bertrand M, Franck F (2000a) Spectroscopic properties of protochlorophyllide analyzed in situ in the course of etiolation and in illuminated leaves. Photochem Photobiol 72:85–93

    Article  PubMed  CAS  Google Scholar 

  • Schoefs B, Bertrand M, Funk C (2000b) Photoactive protochlorophyllide regeneration in cotyledons and leaves from higher plants. Photochem Photobiol 72:660–668

    Article  PubMed  CAS  Google Scholar 

  • Sironval C, Kuyper Y, Michel JM, Brouers M (1967) The primary photoact in the conversion of protochlorophyllide into chlorophyllide. Stud Biophys 5:43–50

    Google Scholar 

  • Solymosi K, Böddi B (2006) Optical properties of bud scales and protochlorophyll(ide) forms in leaf primordia of closed and opened buds. Tree Physiol 26:1075–1085

    Article  PubMed  CAS  Google Scholar 

  • Solymosi K, Schoefs B (2008) Prolamellar body: a unique plastid compartment, which does not only occur in dark-grown leaves. In: Schoefs B (ed) Plant cell organelles—selected topics. Research Signpost, Trivandrum, pp 151–202

    Google Scholar 

  • Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions—the dark side of chlorophyll biosynthesis. Photosynth Res 105:143–166

    Article  PubMed  CAS  Google Scholar 

  • Solymosi K, Martinez K, Kristóf Z, Sundqvist C, Böddi B (2004) Plastid differentiation and chlorophyll biosynthesis in different leaf layers of white cabbage (Brassica oleracea cv. capitata). Physiol Plant 121:520–529

    Article  CAS  Google Scholar 

  • Solymosi K, Bóka K, Böddi B (2006) Transient etiolation: protochlorophyll(ide) and chlorophyll forms in differentiating plastids of closed and breaking leaf buds of horse chestnut (Aesculus hippocastanum). Tree Physiol 26:1087–1096

    Article  PubMed  CAS  Google Scholar 

  • Solymosi K, Vitányi B, Hideg É, Böddi B (2007) Etiolation symptoms in sunflower (Helianthus annuus) cotyledons partially covered by the pericarp of the achene. Ann Bot 99:857–867

    Article  PubMed  CAS  Google Scholar 

  • 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 10:283–296

    Article  PubMed  CAS  Google Scholar 

  • Srivastava LM (1966) On the fine structure of the cambium of Fraxinus americana L. J Cell Biol 31:79–93

    Article  PubMed  CAS  Google Scholar 

  • Sundqvist C, Dahlin C (1997) With chlorophyll pigments from prolamellar bodies to light-harvesting complexes. Physiol Plant 100:748–759

    Article  CAS  Google Scholar 

  • Treffry T (1973) Chloroplast development in etiolated peas: reformation of prolamellar bodies in red light without accumulation of protochlorophyllide. J Exp Bot 24:185–195

    Article  CAS  Google Scholar 

  • Valadon LRG, Mummery RS (1969) The effect of light on carotenoids of etiolated mung bean seedlings. J Exp Bot 20:732–742

    Article  CAS  Google Scholar 

  • Wiktorsson B, Engdahl S, Zhong LB, Böddi B, Ryberg M, Sundqvist C (1993) The effect of cross-linking of the subunits of NADPH:protochlorophyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica 29:205–218

    CAS  Google Scholar 

  • Yin L, Lundin B, Bertrand M, Nurmi M, Solymosi K, Kangasjärvi S, Aro E-M, Schoefs B, Spetea C (2010) Role of thylakoid ATP/ADP carrier in photoinhibition and photoprotection of photosystem II in Arabidopsis. Plant Physiol 153:666–677

    Article  PubMed  CAS  Google Scholar 

  • Younis S, Ryberg M, Sundqvist C (1995) Plastid development in germinating wheat (Triticum aestivum) is enhanced by gibberellic acid and delayed by gabaculine. Physiol Plant 95:336–346

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Csilla Jónás for her technical assistance. Katalin Solymosi thanks the Embassy of France in Hungary for her visiting grant to Dijon, and the University of Burgundy in Dijon for the temporary position as assistant lecturer, which enabled her to run the HPLC experiments in Dijon.

Author information

Author notes

  1. Benoît Schoefs

    Present address: Mer, Molécules, Santé (EA2160), Université du Maine à Le Mans, Faculté des Sciences et Techniques, Avenue Olivier Messiaen, 72085, Le Mans Cedex 9, France

Authors and Affiliations

  1. Department of Plant Anatomy, Institute of Biology, Eötvös University, H-1117, Pázmány P. s. 1/C, Budapest, Hungary

    Katalin Solymosi, Károly Bóka & Béla Böddi

  2. UMR CNRS 5184/INRA 1088/Université de Bourgogne, Plante Microbe Environnement, INRA-CMSE, BP 86510, 21065, Dijon cedex, France

    Dominique Morandi & Benoît Schoefs

Authors
  1. Katalin Solymosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dominique Morandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Károly Bóka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Béla Böddi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Benoît Schoefs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katalin Solymosi.

Additional information

B. Böddi and B. Schoefs share senior authorship (these two authors have contributed equally to the work).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Solymosi, K., Morandi, D., Bóka, K. et al. High biological variability of plastids, photosynthetic pigments and pigment forms of leaf primordia in buds. Planta 235, 1035–1049 (2012). https://doi.org/10.1007/s00425-011-1559-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1559-9

Keywords

Search

Navigation