Skip to main content
Log in

Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit

  • Perspective
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Chlorophyll metabolism probably is the most visible manifestation of life. Total annual turnover of chlorophyll has been estimated to involve more than 1000 million tons. Surprisingly, chlorophyll catabolism has remained an enigma until less than twenty years ago, when a colorless chlorophyll catabolite from senescent plant leaves was identified and its structure was elucidated. In the meantime, chlorophyll breakdown products have been identified in a variety of plant leaves and their structural features have been elucidated. Most recently, chlorophyll breakdown products have also been identified in some ripening fruit. Chlorophyll breakdown in vascular plants only fleetingly involves enzyme-bound colored intermediates. The stage of fluorescent catabolites is also passed rapidly, as these isomerize further to colorless nonfluorescent tetrapyrrolic catabolites. The latter accumulate in the vacuoles of de-greened leaves and are considered the final products of controlled chlorophyll breakdown. The same tetrapyrroles are also found in ripening fruit and are effective antioxidants. Chlorophyll breakdown leads to tetrapyrroles that appear to have physiologically beneficial chemical properties, and it may thus not merely be a detoxification process.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Chlorophylls and Bacteriochlorophylls, Advances in Photosynthesis and Respiration, ed. B. Grimm, R. Porra, W. Rüdiger and H. Scheer, Springer, Dordrecht, 2006, vol. 25

    Google Scholar 

  2. B. Kräutler and P., Matile, Solving the riddle of chlorophyll breakdown Acc. Chem. Res. 1999 32 35–43

    Article  Google Scholar 

  3. S. B. Brown, J. D. Houghton and G. A. F. Hendry, in Chlorophylls, ed. H. Scheer, CRP Press, Boca Raton, USA, 1991, pp. 465-489

  4. B. Kräutler, B. Jaun, K. Bortlik, M. Schellenberg and P., Matile, On the Enigma of Chlorophyll Degradation - The Constitution of a Secoporphinoid Catabolite Angew. Chem., Int. Ed. 1991 30 1315–1318

    Article  Google Scholar 

  5. B. Kräutler and S. Hörtensteiner, in Chlorophylls and Bacteriochlorophylls, ed. B. Grimm, R. Porra, W. Rüdiger and H. Scheer, Advances in Photosynthesis and Respiration, Springer, Dordrecht, The Netherlands, 2006, vol. 25, pp. 237-260

    Google Scholar 

  6. S. Hörtensteiner Chlorophyll Degradation During Senescence Annu. Rev. Plant Biol. 2006 57 55–77

    Article  PubMed  CAS  Google Scholar 

  7. P. Matile, S. Ginsburg, M. Schellenberg and H., Thomas, Catabolites of Chlorophyll in Senescent Leaves J. Plant Physiol. 1987 129 219–228

    Article  CAS  Google Scholar 

  8. H. Thomas, K. Bortlik, D. Rentsch, M. Schellenberg and P., Matile, Catabolism of Chlorophyll In vivo - Significance of Polar Chlorophyll Catabolites in a Non-Yellowing Senescence Mutant of Festuca Pratensis Huds New Phytol. 1989 111 3–8

    Article  CAS  Google Scholar 

  9. P. Matile, S. Ginsburg, M. Schellenberg and H., Thomas, Catabolites of Chlorophyll in Senescing Barley Leaves Are Localized in the Vacuoles of Mesophyll-Cells Proc. Natl. Acad. Sci. USA 1988 85 9529–9532

    Article  CAS  PubMed  Google Scholar 

  10. C. Peisker, H. Thomas, F. Keller and P., Matile, Radiolabeling of Chlorophyll for Studies on Catabolism J. Plant Physiol. 1990 136 544–549

    Article  CAS  Google Scholar 

  11. K. Bortlik, C. Peisker and P., Matile, A Novel Type of Chlorophyll Catabolite in Senescent Barley Leaves J. Plant Physiol. 1990 136 161–165

    Article  CAS  Google Scholar 

  12. B. Kräutler Unravelling chlorophyll catabolism in higher plants Biochem. Soc. Trans. 2002 30 625–630

    Article  PubMed  Google Scholar 

  13. B. Kräutler, B. Jaun, W. Amrein, K. Bortlik, M. Schellenberg and P., Matile, Breakdown of Chlorophyll - Constitution of a Secoporphinoid Chlorophyll Catabolite Isolated from Senescent Barley Leaves Plant Physiol. Biochem. 1992 30 333–346

    Google Scholar 

  14. P. Matile, S. Hörtensteiner, H. Thomas, B. Kräutler Chlorophyll breakdown in senescent leaves Plant Physiol. 1996 112 1403–1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. B. Kräutler, in The Porphyrin Handbook, ed. K. M. Kadish, K. M. Smith and R. Guilard, Elsevier Science, Oxford, 2003, vol. 13, pp. 183-209

  16. T. Müller, S. Moser, K. H. Ongania, A. Pruzinska, S. Hörtensteiner, B. Kräutler A Divergent Path of Chlorophyll Breakdown in the Model Plant Arabidopsis thaliana ChemBioChem 2006 7 40–42

    Article  PubMed  CAS  Google Scholar 

  17. W. Rüdiger and B. Grimm, in Chlorophylls and Bacteriochlorophylls, Advances in Photosynthesis and Respiration, ed. B. Grimm, R. J. Porra, W. Rüdiger and H. Scheer, Springer, Dordrecht, 2006, vol. 25, pp. 133-146

  18. H. Ito, T. Ohtsuka and A., Tanaka, Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll J. Biol. Chem. 1996 271 1475–1479

    Article  CAS  PubMed  Google Scholar 

  19. Y. Shioi, N. Tomita, T. Tsuchiya and K., Takamiya, Conversion of chlorophyllide to pheophorbide by Mg-dechelating substance in extracts of Chenopodium album Plant Physiol. Biochem. 1996 34 41–47

    CAS  Google Scholar 

  20. T. Suzuki and Y., Shioi, Re-examination of Mg-dechelation reaction in the degradation of chlorophylls using chlorophyllin a as a substrate Photosynth. Res. 2002 74 217–223

    Article  CAS  PubMed  Google Scholar 

  21. S. Ginsburg and P., Matile, Identification of Catabolites of Chlorophyll-Porphyrin in Senescent Rape Cotyledons Plant Physiol. 1993 102 521–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. W. Mühlecker, K. H. Ongania, B. Kräutler, P. Matile, S. Hörtensteiner Tracking down chlorophyll breakdown in plants: Elucidation of the constitution of a “fluorescent” chlorophyll catabolite Angew. Chem., Int. Ed. 1997 36 401–404

    Article  Google Scholar 

  23. S. Hörtensteiner, F. Vicentini and P., Matile, Chlorophyll Breakdown in Senescent Cotyledons of Rape, Brassica napus L - Enzymatic Cleavage of Phaeophorbide ain vitro New Phytol. 1995 129 237–246

    Article  PubMed  Google Scholar 

  24. S. Hörtensteiner, K. L. Wüthrich, P. Matile, K. H. Ongania, B. Kräutler The key step in chlorophyll breakdown in higher plants - Cleavage of pheophorbide a macrocycle by a monooxygenase J. Biol. Chem. 1998 273 15335–15339

    Article  PubMed  Google Scholar 

  25. A. Pružinska, G. Tanner, I. Anders, M. Roca, S. Hörtensteiner Chlorophyll breakdown: Pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene Proc. Natl. Acad. Sci. USA 2003 100 15259–15264

    Article  PubMed  CAS  Google Scholar 

  26. P. Matile, S. Hörtensteiner and H., Thomas, Chlorophyll degradation Ann. Rev. Plant Physiol. Plant Mol. Biol. 1999 50 67–95

    Article  CAS  Google Scholar 

  27. B. Kräutler, W. Mühlecker, M. Anderl and B., Gerlach, Breakdown of chlorophyll: Partial synthesis of a putative intermediary catabolite - Preliminary communication Helv. Chim. Acta 1997 80 1355–1362

    Article  Google Scholar 

  28. N. Engel, T. A. Jenny, V. Mooser and A., Gossauer, Chlorophyll Catabolism in Chlorella-Protothecoides - Isolation and Structure Elucidation of a Red Bilin Derivative FEBS Lett. 1991 293 131–133

    Article  CAS  PubMed  Google Scholar 

  29. N. Engel, C. Curty and A., Gossauer, Chlorophyll catabolism in Chlorella protothecoides. 8. Facts and artefacts Plant Physiol. Biochem. 1996 34 77–83

    CAS  Google Scholar 

  30. A. Gossauer, Catabolism of tetrapyrroles Chimia 1994 48 352–361

    CAS  Google Scholar 

  31. S. Rodoni, W. Mühlecker, M. Anderl, B. Kräutler, D. Moser, H. Thomas, P. Matile, S. Hörtensteiner Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps Plant Physiol. 1997 115 669–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. S. Rodoni, M. Schellenberg and P., Matile, Chlorophyll breakdown in senescing barley leaves as correlated with phaeophorbide a oxygenase activity J. Plant Physiol. 1998 152 139–144

    Article  CAS  Google Scholar 

  33. S. Rodoni, F. Vicentini, M. Schellenberg, P. Matile, S. Hörtensteiner Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chlorophyll breakdown Plant Physiol. 1997 115 677–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. K. L. Wüthrich, L. Bovet, P. E. Hunziker, I. S. Donnison, S. Hörtensteiner Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism Plant J. 2000 21 189–198

    Article  PubMed  Google Scholar 

  35. W. Mühlecker, B. Kräutler, D. Moser, P. Matile, S. Hörtensteiner Breakdown of chlorophyll: a fluorescent chlorophyll catabolite from sweet pepper (Capsicum annuum) Helv. Chim. Acta 2000 83 278–286

    Article  Google Scholar 

  36. S. Hörtensteiner, S. Rodoni, M. Schellenberg, F. Vicentini, O. I. Nandi, Y. L. Qui and P., Matile, Evolution of chlorophyll degradation: the significance of RCC reductase Plant Biol. 2000 2 63–67

    Article  Google Scholar 

  37. A. Pružinska, I. Anders, S. Aubry, N. Schenk, E. Tapernoux-Lüthi, T. Müller, B. Kräutler, S. Hörtensteiner In Vivo Participation of Red Chlorophyll Catabolite Reductase in Chlorophyll Breakdown and in Detoxification of Photodynamic Chlorophyll Catabolites Plant Cell 2007 19 369–387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. M. Oberhuber, B. Kräutler Breakdown of chlorophyll: Electrochemical bilin reduction provides synthetic access to fluorescent chlorophyll catabolites ChemBioChem 2002 3 104–107

    Article  CAS  PubMed  Google Scholar 

  39. M. Oberhuber, J. Berghold, B. Kräutler Chlorophyll Breakdown by a Biomimetic Route Angew. Chem., Int. Ed. 2008 47 3057–3061

    Article  CAS  Google Scholar 

  40. N. Frankenberg and J. C. Lagarias, in The Porphyrin Handbook, ed. K. M. Kadish, K. M. Smith and R. Guilard, Elsevier Science, Oxford, UK, 2003, vol. 13, pp. 211-235

  41. M. Oberhuber, J. Berghold, K. Breuker, S. Hörtensteiner, B. Kräutler Breakdown of chlorophyll: A nonenzymatic reaction accounts for the formation of the colorless “nonfluorescent” chlorophyll catabolites Proc. Natl. Acad. Sci. USA 2003 100 6910–6915

    Article  CAS  PubMed  Google Scholar 

  42. J. Berghold, K. Breuker, M. Oberhuber, S. Hörtensteiner, B. Kräutler Chlorophyll breakdown in spinach: on the structure of five nonfluorescent chlorophyll catabolites Photosynth. Res. 2002 74 109–119

    Article  CAS  PubMed  Google Scholar 

  43. J. Berghold, C. Eichmüller, S. Hörtensteiner, B. Kräutler Chlorophyll breakdown in tobacco: On the structure of two nonfluorescent chlorophyll catabolites Chem. Biodiv. 2004 1 657–668

    Article  CAS  Google Scholar 

  44. J. Berghold, T. Müller, M. Ulrich, S. Hörtensteiner, B. Kräutler Chlorophyll Breakdown in Maize: On the Structure of Two Nonfluorescent Chlorophyll Catabolites Monatsh. Chem. 2006 137 751–763

    Article  CAS  Google Scholar 

  45. W. Mühlecker, B. Kräutler, S. Ginsburg and P., Matile, Breakdown of Chlorophyll - a Tetrapyrrolic Chlorophyll Catabolite from Senescent Rape Leaves Helv. Chim. Acta 1993 76 2976–2980

    Article  Google Scholar 

  46. W. Mühlecker, B. Kräutler Breakdown of chlorophyll: Constitution of nonfluorescing chlorophyll-catabolites from senescent cotyledons of the dicot rape Plant Physiol. Biochem. 1996 34 61–75

    Google Scholar 

  47. C. Curty and N., Engel, Chlorophyll catabolism. 9. Detection, isolation and structure elucidation of a chlorophyll a catabolite from autumnal senescent leaves of Cercidiphyllum japonicum Phytochem. 1996 42 1531–1536

    Article  CAS  Google Scholar 

  48. M. Oberhuber, J. Berghold, W. Mühlecker, S. Hörtensteiner, B. Kräutler Chlorophyll breakdown - on a nonfluorescent chlorophyll catabolite from spinach Helv. Chim. Acta 2001 84 2615–2627

    Article  CAS  Google Scholar 

  49. S. Hörtensteiner, B. Kräutler Chlorophyll breakdown in oilseed rape Photosynth. Res. 2000 64 137–146

    Article  PubMed  Google Scholar 

  50. J. Iturraspe, N. Moyano and B., Frydman, A New 5-Formylbilinone as the Major Chlorophyll a Catabolite in Tree Senescent Leaves J. Org. Chem. 1995 60 6664–6665

    Article  CAS  Google Scholar 

  51. A. Pružinska, G. Tanner, S. Aubry, I. Anders, S. Moser, T. Müller, K.-H. Ongania, B. Kräutler, J.-Y. Youn, S. J. Liljegren, S. Hörtensteiner Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction Plant Physiol. 2005 139 52–63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. P. Matile, in Advances in Botanical Research, ed. J. A. Callow, Academic Press, New York, 1997, vol. 25, pp. 87-112

  53. A. Bachmann, J. Fernandezlopez, S. Ginsburg, H. Thomas, J. C. Bouwkamp, T. Solomos and P., Matile, Stay-Green Genotypes of Phaseolus vulgaris L - Chloroplast Proteins and Chlorophyll Catabolites during Foliar Senescence New Phytol. 1994 126 593–600

    Article  CAS  Google Scholar 

  54. F. G. Losey and N., Engel, Isolation and characterization of a urobilinogenoidic chlorophyll catabolite from Hordeum vulgare J. Biol. Chem. 2001 276 8643–8647

    Article  CAS  PubMed  Google Scholar 

  55. P. Matile, Senescence in Plants and Its Importance for Nitrogen-Metabolism Chimia 1987 41 376–381

    CAS  Google Scholar 

  56. H. Thomas, H. Ougham, S. Hörtensteiner Recent advances in the cell biology of chlorophyll catabolism Adv. Bot. Res. 2001 35 1–52

    Article  CAS  Google Scholar 

  57. S. Hörtensteiner The loss of green color during chlorophyll degradation - a prerequisite to prevent cell death? Planta 2004 219 191–194

    Article  PubMed  CAS  Google Scholar 

  58. P. Matile, in Regulation of Photosynthesis, ed. E.-M. 3 and B. Andersson, Kluwer Academic Publishers, Dordrecht, The Netherlands, 2001, pp. 277-296

  59. T. Müller, M. Ulrich, K. H. Ongania, B. Kräutler Colorless Tetrapyrrolic Chlorophyll Catabolites Found in Ripening Fruit Are Effective Antioxidants Angew. Chem., Int. Ed. 2007 46 8699–8702

    Article  CAS  Google Scholar 

  60. J. L. Dangl, R. A. Dietrich and H. Thomas, in Biochemistry & Molecular Biology of Plants, ed. B. B. Buchanan, W. Gruissem and R. L. Jones, Am. Soc. Plant Physiol., Rockville, Md, USA, 2001, pp. 1044-1100

  61. R. Stocker, Y. Yamamoto, A. F. Mcdonagh, A. N. Glazer and B. N., Ames, Bilirubin Is an Antioxidant of Possible Physiological Importance Science 1987 235 1043–1046

    Article  CAS  PubMed  Google Scholar 

  62. P. R. Ortiz de Montellano and K. Auclair, in The Porphyrin Handbook, ed. K. M. Kadish, K. M. Smith and R. Guilard, Academic Press, Amsterdam, 2003, vol. 12, pp. 183-210

  63. D. E. Baranano, M. Rao, C. D. Ferris and S. H., Snyder, Biliverdin reductase: A major physiologic cytoprotectant Proc. Natl. Acad. Sci. USA 2002 99 16093–16098

    Article  CAS  PubMed  Google Scholar 

  64. J. M. Mach, A. R. Castillo, R. Hoogstraten and J. T., Greenberg, The Arabidopsis accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms Proc. Natl. Acad. Sci. USA 2001 98 771–776

    Article  CAS  PubMed  Google Scholar 

  65. D. A., Greenberg, The jaundice of the cell Proc. Natl. Acad. Sci. USA 2002 99 15837–15839

    Article  CAS  PubMed  Google Scholar 

  66. H. Nakamura, B. Musicki, Y. Kishi and O., Shimomura, Structure of the Light Emitter in Krill (Euphausia pacifica) Bioluminescence J. Am. Chem. Soc. 1988 110 2683–2685

    Article  CAS  Google Scholar 

  67. H. Nakamura, Y. Kishi, O. Shimomura, D. Morse and J. W., Hastings, Structure of Dinoflagellate Luciferin and Its Enzymatic and Nonenzymatic Air-Oxidation Products J. Am. Chem. Soc. 1989 111 7607–7611

    Article  CAS  Google Scholar 

  68. Y. Suzuki and Y., Shioi, Detection of chlorophyll breakdown products in the senescent leaves of higher plants Plant Cell Physiol. 1999 40 909–915

    Article  CAS  Google Scholar 

  69. E. Riboli and T., Norat, Epidemiologic evidence of the protective effect of fruit and vegetables on cancer risk Am. J. Clin. Nutr. 2003 78 559S–569S

    Article  CAS  PubMed  Google Scholar 

  70. J. W. Jonker, M. Buitelaar, E. Wagenaar, M. A. van der Valk, G. L. Scheffer, R. J. Scheper, T. Plosch, F. Kuipers, R. P. J. O. Elferink, H. Rosing, J. H. Beijnen and A. H., Schinkel, The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria Proc. Natl. Acad. Sci. USA 2002 99 15649–15654

    Article  CAS  PubMed  Google Scholar 

  71. M. V. Eberhardt, C. Y. Lee and R. H., Liu, Nutrition - Antioxidant activity of fresh apples Nature 2000 405 903–904

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This paper was published as part of the themed issue of contributions from the 7th International Conference on Tetrapyrrole Photoreceptors in Photosynthetic Organisms held in Kyoto, December 2007.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kräutler, B. Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit. Photochem Photobiol Sci 7, 1114–1120 (2008). https://doi.org/10.1039/b802356p

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b802356p

Navigation