Abstract
Chlorophyll catabolism accompanying leaf senescence is one of the most spectacular natural phenomena. Despite this fact, the metabolism of chlorophyll has been largely neglegted until recently. Oilseed rape has been used extensively as a model plant for the recent elucidating of structures of chlorophyll catabolites and for investigation of the enzymic reactions of the chlorophyll breakdown pathway. The key reaction which causes loss of green color is catalyzed in a two-step reaction by pheophorbide a oxygenase and red chlorophyll catabolite reductase. In this Minireview, we summarize the actual knowledge about catabolites and enzymes of chlorophyll catabolism in oilseed rape and discuss the significance of this pathway in respect to chlorophyll degradation during Brassica napus seed development.
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Bortlik K-H, Peisker C and Matile P (1990) A novel type of chlorophyll catabolite in senescent barley leaves. J Plant Physiol 136: 161–165
Brown SB, Houghton JD and Hendry GAF (1991) Chlorophyll breakdown. In: Scheer H (ed) Chlorophylls, pp 465–489. CRC Press, Boca Raton, Florida
Brown SB, Smith KM, Bisset GMF and Troxler RF (1980) Mechanism of photooxidation of bacteriochlorophyll c derivatives. A possible model for natural chlorophyll breakdown. J Biol Chem 255: 8063–8068
Curty C and Engel N (1996) Detection, isolation and structure elucidation of a chlorophyll a catabolite from autumnal senescent leaves of Cercidiphyllum japonicum. Phytochemistry 42: 1531–1536
Curty C and Engel N (1997) Chlorophyll catabolism: high stereoselectivity in the last step of the primary ring cleaving process. Plant Physiol Biochem 35: 707–711
Curty C, Engel N and Gossauer A (1995) Evidence for a monooxygenase-catalyzed primary process in the catabolism of chlorophyll. FEBS Lett 364: 41–44
Engel N, Curty C and Gossauer A (1996) Chlorophyll catabolism in Chlorella protothecoides. 8. Facts and artefacts. Plant Physiol Biochem 34: 77–83
Engel N, Jenny TA, Mooser V and Gossauer A (1991) Chlorophyll catabolism in Chlorella protothecoides. Isolation and structure elucidation of a red bilin derivative. FEBS Lett 293: 131–133
Ginsburg S and Matile P (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol 102: 521–527
Ginsburg S, Schellenberg M and Matile P (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol 105: 545–554
Green BR, Singh S, Babic I, Bladen C and Johnson-Flanagan AM (1998) Relationship of chlorophyll, seed moisture and ABA levels in the maturing Brassica napus seed and effect of a mild freezing stress. Physiol Plant 104: 125–133
Hinder B, Schellenberg M, Rodoni S, Ginsburg S, Vogt E, Martinoia E, Matile P and Hörtensteiner S (1996) How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem 271: 27233–27236
Holden M (1961) The breakdown of chlorophyll by chlorophyllase. Biochem J 78: 359–364
Hörtensteiner S (1998) NCC malonyltransferase catalyses the fi-nal step of chlorophyll breakdown in rape (Brassica napus). Pytochemistry 49: 953–956
Hörtensteiner S (1999) Chlorophyll breakdown in higher plants and algae. Cell Mol Life Sci 56: 330–347
Hörtensteiner S, Vicentini F and Matile P (1995) Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L.: Enzymatic cleavage of phaeophorbide a in vitro. New Phytol 129: 237–246
Hörtensteiner S, Wüthrich KL and Matile P (1998a) New aspects on the catabolic pathway of chlorophyll in senescent rape cotyledons. J Exp Bot 49 (Suppl 65)
Hörtensteiner S, Wüthrich KL, Matile P, Ongania K-H and Kräutler B (1998b) The key step in chlorophyll breakdown in higher plants. Cleavage of pheophorbide a macrocycle by a monooxygenase. J Biol Chem 273: 15335–15339
Hörtensteiner S, Rodoni S, Schellenberg M, Vicentini F, Nandi OI, Qiu Y-L and Matile P (2000) Evolution of chlorophyll degradation: The significance of RCC reductase. Plant Biol 2: 63–67
Ito H, Ohysuka T and Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271: 1475–1479
Iturraspe J, Moyano N and Frydman B (1995) A new 5-formylbilinone as the major chlorophyll a catabolite in tree senescent leaves. J Org Chem 60: 6664–6665
Jacob-Wilk D, Holland D, Goldschmidt EE, Riov J and Eyal Y (1999) Chlorophyll breakdown by chlorophyllase: Isolation and functional expression of the Chlase1 gene from ethylene-treated Citrus fruit and its regulation during development. Plant J 20: 653–661
Johnson-Flanagan AM and McLachlan G (1990) The role of chlorophyllase in degreening canola (Brassica napus) seeds and its activity by sublethal freezing. Physiol Plant 80: 460–466
Johnson-Flanagan AM and Spencer MS (1994) Ethylene production during degreening of maturing seeds of mustard and canola. Plant Physiol 106: 601–606
Johnson-Flanagan AM and Thiagarajah MR (1990) Degreening in canola (Brassica napus cv. Westar) embryos under optimum conditions. J Plant Physiol 136: 180–186
Kräutler B and Matile P (1999) Solving the riddle of chlorophyll breakdown. Acc Chem Res 32: 35–43
Kräutler B, Jaun B, Amrein W, Bortlik K, Schellenberg M and Matile P (1992) Breakdown of chlorophyll: Constitution of a secoporphinoid chlorophyll catabolite isolated from senescent barley leaves. Plant Physiol Biochem 30: 333–346
Kräutler B, Jaun B, Bortlik K-H, Schellenberg M and Matile P (1991) On the enigma of chlorophyll degradation: The constitution of a secoporphinoid catabolite. Angew Chem Int Ed Engl 30: 1315–1318
Kräutler B, Mühlecker W, Anderl M and Gerlach B (1997) Breakdown of chlorophyll: partial synthesis of a putative intermediary catabolite. Helv Chim Acta 80: 1355–1362
Kreuz K, Tommasini R and Martinoia E (1996) Old enzymes for a new job. Herbicide detoxification in plants. Plant Physiol 111: 349–353
Langmeier M, Ginsburg S and Matile P (1993) Chlorophyll breakdown in senescent leaves: Demonstration of Mg-dechelatase activity. Physiol Plant 89: 347–353
Levadoux WL, Kalmokoff ML, Pickard MD and Groot-Wassink JWD (1987) Pigment removal from canola oil using chlorophyllase. J Am Oil Chem Soc 64: 139–144
Lu Y-P, Li Z-S, Drozdowicz Y-M, Hörtensteiner S, Martinoia E and Rea PA (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: Functional comparisons with AtMRP1. Plant Cell 10: 267–282
Matile P (1987) Seneszenz bei Pflanzen und ihre Bedeutung für den Stickstoffhaushalt. Chimia 41: 376–381
Matile P (1992) Chloroplast senescence. In: Baker NR and Thomas H (eds) Crop Photosynthesis: Spatial and Temporal Determinants, pp 413–440. Elsevier Science Publishers, Amsterdam
Matile P and Kräutler B (1995) Wie und warum bauen Pflanzen das Chlorophyll ab. Chem unserer Zeit 29: 298–306
Matile P and Schellenberg M (1996) The cleavage of pheophorbide a is located in the envelope of barley gerontoplasts. Plant Physiol Biochem 34: 55–59
Matile P, Ginsburg S, Schellenberg M and Thomas H (1987) Catabolites of chlorophyll in senescent leaves. J Plant Physiol 129: 219–228
Matile P, Schellenberg M and Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187: 230–235
Matile P, Hörtensteiner S, Thomas H and Kräutler B (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol 112: 1403–1409
Matile P, Schellenberg M and Vicentini F (1997) Localization of chlorophyllase in the chloroplast envelope. Planta 201: 96–99
Matile P, Hörtensteiner S and Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50: 67–95
Mühlecker W and Kräutler B (1996) Breakdown of chlorophyll: Constitution of nonfluorescing chlorophyll-catabolites from senescent cotyledons of the dicot rape. Plant Physiol Biochem 34: 61–75
Mühlecker W, Kräutler B, Ginsburg S and Matile P (1993) Breakdown of chlorophyll: The constitution of a secoporphinoid chlorophyll catabolite from senescent rape leaves. Helv Chim Acta 76: 2976–2980
Mühlecker W, Ongania K-H, Kräutler B, Matile P and Hörtensteiner S (1997) Tracking down chlorophyll breakdown in plants: elucidation of the constitution of a 'fluorescent' chlorophyll catabolite. Angew Chem Int Ed Engl 36: 401–404
Mühlecker W, Kräutler B, Moser D, Matile P and Hörtensteiner S (2000) Breakdown of chlorophyll: A fluorescent chlorophyll catabolite from sweet pepper (Capsicum annuum). Helv Chim Acta 83: 278–286
Nishiyama Y, Kitamura M, Tamura S and Watanabe T (1994) Purification and substrate specificity of chlorophyllase from Chlorella regularis. Chem Lett 69–72
Oshio Y and Hase E (1969) Studies on red pigments excreted by cells of Chlorella protothecoides during the process of bleaching induced by glucose or acetate. I. Chemical properties of the red pigments. Plant Cell Physiol 10: 41–49
Peisker C, Düggelin T, Rentsch D and Matile P (1989) Phytol and the breakdown of chlorophyll in senescent leaves. J Plant Physiol 135: 428–432
Peisker C, Thomas H, Keller F and Matile P (1990) Radiolabelling of chlorophyll for studies on catabolism. J Plant Physiol 136: 544–549
Rodoni S, Mühlecker W, Anderl M, Kräutler B, Moser D, Thomas H, Matile P and Hörtensteiner S (1997a) Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps. Plant Physiol 115: 669–676
Rodoni S, Vicentini F, Schellenberg M, Matile P and Hörtensteiner S (1997b) Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chlorophyll breakdown. Plant Physiol 115: 677–682
Schellenberg M, Matile P and Thomas H (1993) Production of a presumptive chlorophyll catabolite in vitro: Requirement for reduced ferredoxin. Planta 191: 417–420
Scheumann V, Ito H, Tanaka A, Schoch S and Rüdiger W (1996) Substrate specificity of chlorophyll(ide) b reductase in etioplasts of barley (Hordeum vulgare). Eur J Biochem 242: 163–170
Scheumann V, Schoch S and Rüdiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209: 364–370
Schoch S, Scheer H, Schiff JA, Rüdiger W and Siegelman HW (1981) Pyropheophytin a accompanies pheophytin a in darkened light grown cells of Euglena. Z Naturforsch 36c: 827–833
Schoch S, Rüdiger W, Lüthy B and Matile P (1984) 132-hydroxychlorophyll a, the first product of the reaction of chlorophyll-oxidase. J Plant Physiol 115: 85–89
Schuler MA (1996) Plant cytochrome P450 monooxygenases. Critical Rev Plant Sci 15: 235–284
Shimokawa K, Hashizume A and Shioi Y (1990) Pyropheophorbide a, a catabolite of ethylene-induced chlorophyll a degradation. Phytochemistry 29: 2105–2106
Shioi Y, Tomita N, Tsuchiya T and Takamiya K (1996a) Conversion of chlorophyllide to pheophorbide by Mg-dechelating substance in extracts of Chenopodium album. Plant Physiol Biochem 34: 41–47
Shioi Y, Watanabe K and Takamiya K (1996b) Enzymatic conversion of pheophorbide a to a precursor of pyropheophorbide a in leaves of Chenopodium album. Plant Cell Physiol 37: 1143–1149
Thomas H (1997) Chlorophyll: A symptom and a regulator of plastid development. New Phytol 136: 163–181
Thomas H, Schellenberg M, Vicentini F and Matile P (1996) Gregor Mendel's green and yellow pea seeds. Bot Acta 109: 3–4
Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N and Martinoia E (1998) An ABC transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13: 773–780
Trebitsh T, Goldschmidt EE and Riov J (1993) Ethylene induces de novo synthesis of chlorophyllase, a chlorophyll degrading enzyme, in Citrus fruit peel. Proc Natl Acad Sci USA 90: 9441–9445
Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T and Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: Finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci 96: 15362–15367
Vicentini F, Hörtensteiner S, Schellenberg M, Thomas H and Matile P (1995) Chlorophyll breakdown in senescent leaves: Identi-fication of the biochemical lesion in a stay-green genotype of Festuca pratensis Huds. New Phytol 129: 247–252
von Wettstein D, Gough S and Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7: 1039–1057
Willstätter R and Stoll A (1913) Die Wirkungen der Chlorophyllase. In: Willstätter R and Stoll A (eds) Untersuchungen über Chlorophyll, pp 172–187. Verlag Julius Springer, Berlin
Woodward RB and Skaric V (1961) A new aspect of the chemistry of chlorins. J Am Chem Soc 83: 4676–4678
Wüthrich KL, Bovet L, Hunziker PE, Donnison IS and Hörtensteiner S (2000) Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. Plant J 21: 189–198
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Hörtensteiner, S., Kräutler, B. Chlorophyll breakdown in oilseed rape. Photosynthesis Research 64, 137–146 (2000). https://doi.org/10.1023/A:1006456310193
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DOI: https://doi.org/10.1023/A:1006456310193