Chlorophyll breakdown in higher plants and algae

Cellular and Molecular Life Sciences

Volumn 56, Issue 3-4, 1999, Pages 330-347

  Hortensteiner S ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Breakdown; Catabolic pathway; Catabolites; Chlorophyll; Detoxification; Pigment; Senescence; Vacuole

Indexed keywords

CHLOROPHYLL; PORPHYRIN;

CATABOLISM; CELL TRANSPORT; CHEMICAL STRUCTURE; CHLORELLA; HIGHER PLANT; HYDROXYLATION; NONHUMAN; PLANT LEAF; REVIEW;

ALGAE, GREEN; CHLORELLA; CHLOROPHYLL; PLANTS;

ALGAE; AUXENOCHLORELLA PROTOTHECOIDES; EMBRYOPHYTA;

EID: 0033569362     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050434     Document Type: Review

References (186)

1. Stoll A. (1912) Über Chlorophyllase und die Chlorophyllide, Ph.D. thesis, ETH Zürich
2. Hendry G. A. F., Houghton J. D. and Brown S. B. (1987) Chlorophyll degradation. A biological enigma. New Phytol. 107: 255-302
3. Matile P. (1992) Chloroplast senescence. In: Crop Photosynthesis: Spatial and Temporal Determinants, pp. 413-440, Baker N. R. and Thomas H. (ed.), Elsevier Science Publishers, Amsterdam
4. Gossauer A. (1994) Catabolism of tetrapyrroles. Chimia 48: 352-361
5. Smart C. M. (1994) Gene expression during leaf senescence. New Phytol. 126: 419-448
6. Matile P., Hörtensteiner S., Thomas H. and Kräutler B. (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol. 112: 1403-1409
7. Gossauer A. and Engel N. (1996) Chlorophyll catabolism. Structures, mechanisms, conversions. J. Photochem. Photobiol. B: Biol. 32: 141-151
8. Buchanan-Wollaston V. (1997) The molecular biology of leaf senescence. J. Exp. Bot. 48: 181-199
9. Gan S. and Amasino R. M. (1997) Making sense of senescence. Molecular genetic regulation and manipulation of leaf senescence. Plant Physiol. 113: 313-319
10. Kräutler B. and Matile P. (1999) Solving the riddle of chlorophyll breakdown. Acc. Chem. Res. 32: 35-43
11. Matile P., Hörtensteiner S. and Thomas H. (1999) Chlorophyll degradation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 67-95
12. Peisker C., Thomas H., Keller F. and Matile P. (1990) Radiolabelling of chlorophyll for studies on catabolism. J. Plant Physiol. 136: 544-549
13. 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
14. Thomas H., Bortlik K.-H., Rentsch D., Schellenberg M. and Matile P. (1989) Catabolism of chlorophyll in vivo: significance of polar chlorophyll catabolites in a non-yellowing senescence mutant of Festuca pratensis Huds. New Phytol. 111: 3-8
15. Bachmann A., Fernández-López J., Ginsburg S., Thomas H., Bouwcamp J. C., Solomos T. et al. (1994) Stay-green genotypes of Phaseolus vulgaris L.: chloroplast proteins and chlorophyll catabolites during foliar senescence. New Phytol. 126: 593-600
16. Maunders M. J., Brown S. B. and Woolhouse H. W. (1983) The appearance of chlorophyll derivatives in senescing tissue. Phytochemistry 22: 2443-2446
17. 2-hydroxychlorophyll a, the first product of the reaction of chlorophyll-oxidase. J. Plant Physiol. 115: 85-89
18. Ziegler R., Blaheta A., Guha N. and Schönegge B. (1988) Enzymatic formation of pheophorbide and pyropheophorbide during chlorophyll degradation in a mutant of Chlorella fusca SHIRIA et KRAUS. J. Plant Physiol. 132: 327-332
19. Schoch S., Scheer H., Schiff J. A., Rüdiger W. and Siegelman H. W. (1981) Pyropheophytin a accompanies pheophytin a in darkened light grown cells of Euglena. Z. Naturforsch. 36e: 827-833
20. Schoch S. and Vielwerth F. X. (1983) Chlorophyll degradation in senescent tobacco cell culture (Nicotiana tabacum var. 'Samsun'). Z. Pflanzenphysiol. 110: 309-317
21. Amir-Shapira D., Goldschmidt E. E. and Altman A. (1987) Chlorophyll catabolism in senescing plant tissues: in vivo breakdown intermediates suggest different degradative pathways for Citrus fruit and parsley leaves. Proc. Natl. Acad. Sci. USA 84: 1901-1905
22. Shimokawa K., Hashizume A. and Shioi Y. (1990) Pyropheophorbide a, a catabolite of ethylene-induced chlorophyll a degradation. Photochemistry 29: 2105-2106
23. Shioi Y., Tatsumi Y. and Shimokawa K. (1991) Enzymatic degradation of chlorophyll in Chenopodium album. Plant Cell Physiol. 32: 87-93
24. Engel N., Curty C. and Gossauer A. (1996) Chlorophyll catabolism in Chlorella protothecoides. 8. Facts and artefacts. Plant Physiol. Biochem. 34: 77-83
25. Janave M. T. (1997) Enzymic degradation of chlorophyll in cavendish bananas: in vitro evidence for two independent degradative pathways. Plant Physiol. Biochem. 35: 837-846
26. Lüthy B., Matile P. and Thomas H. (1986) Properties of linolenic acid-dependent chlorophyll oxidation activity in thylakoid membranes. J. Plant Physiol. 123: 169-180
27. Thomas H., Schellenberg M., Vicentini F. and Matile P. (1996) Gregor Mendel's green and yellow pea seeds. Bot. Acta 109: 3-4
28. 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
29. Rontani J.-F., Cuny P. and Grossi V. (1996) Photodegradation of chlorophyll phytol chain in senescent leaves of higher plants. Phytochemistry 42: 347-351
30. Molinatorres J. and Martínez M. L. (1991) Tocopherols and leaf age in Xanthium strumarium I., New Phytol. 118: 95-99
31. Rise M., Cojocaru M., Gottlieb H. E. and Goldschmidt E. E. (1989) Accumulation of α-tocopherol in senescing organs as related to chlorophyll degradation. Plant Physiol. 89: 1028-1030
32. Soll J. (1987) α-Tocopherol and plastochinone synthesis in chloroplast membranes. Methods Enzymol. 148: 383-392
33. Norris S. R., Barrette T. R. and DellaPenna D. (1995) Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7: 2139-2149
34. Bortlik K.-H. (1990) Chlorophyllabbau: Charakterisierung von Kataboliten in seneszenten Gerstenblättern, Ph.D. thesis, University of Zürich
35. Sitte P., Falk H. and Liedvogel B. (1980) Chromoplasts. In: Pigments in Plants, pp. 117-148, Czygan F.-C. (ed.), Gustav Fischer, Stuttgart
36. Csupor L. (1971) Das Phytol in vergilbten Blättern. Planta Med. 19: 37-41
37. Patterson G. W., Hugly S. and Harrison D. (1993) Sterols and phytyl esters of Arabidopsis thaliana under normal and chilling temperatures. Phytochemistry 33: 1381-1383
38. Ginsburg S. (1993) Chlorophyllabbau in seneszenten Rapscotyledonen, Ph.D. thesis, University of Zürich
39. Schellenberg M., Mutile P. and Thomas H. (1990) Breakdown of chlorophyll in chloroplasts of senescent barley leaves depends on ATP. J. Plant Physiol. 136: 564-568
40. 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
41. Matile P., Ginsburg S., Schellenberg M. and Thomas H. (1987) Catabolites of chlorophyll in senescent leaves. J. Plant Physiol. 129: 219-228
42. Düggelin T., Bortlik K.-H., Gut H., Matile P. and Thomas H. (1988) Leaf senescence in a non-yellowing mutant of Festuca pratensis: accumulation of lipofuscin-like compounds. Physiol. Plant. 74: 131-136
43. Düggelin T., Schellenberg M., Bortlik K.-H. and Matile P. (1988) Vacuolar location of lipofuscin-and proline-like compounds in senescent barley leaves. J. Plant Physiol. 133: 492-497
44. Rodoni S., Vicentini F., Schellenberg M., Matile P. and Hörtensteiner S. (1997) Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chlorophyll breakdown. Plant Physiol. 115: 677- 682
45. Ginsburg S., Schellenberg M. and Matile P. (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol. 105: 545-554
46. 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
47. Moser D. and Matile P. (1997) Chlorophyll breakdown in ripening fruits of Capsicum annuum. J. Plant Physiol. 150: 759-761
48. Rodoni S., Mühlecker W., Anderl M., Kräutler B., Moser D., Thomas H. et al. (1997) Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps. Plant Physiol. 115: 669-676
49. Kräutler B., Mühlecker W., Anderl M. and Gerlach B. (1997) Breakdown of chlorophyll: partial synthesis of a putative intermediary catabolite. Helv. Chim. Ada 80: 1355-1362
50. 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
51. 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. II. Mode of formation of the red pigments. Plant Cell Physiol. 10: 51-59
52. Engel N., Jenny T. A., 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
53. Iturraspe J., Engel N., Matzinger P., Mooser V. and Gossauer A. (1993) Chlorophyll catabolism. Part 3. Structure elucidation and partial synthesis of a new red bilin derivative from Chlorella protothecoides. Photochem. Photobiol. 58: 116-119
54. Iturraspe J., Engel N. and Gossauer A. (1994) Chlorophyll catabolism. Isolation and structure elucidation of chlorophyll b catabolites in Chlorella protothecoides. Phytochemistry 35: 1387-1390
55. 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
56. Ginsburg S. and Matile P. (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol. 102: 521-527
57. 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
58. 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
59. 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
60. 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
61. Tenhunen R., Marver H. S. and Schmid R. (1969) Microsomal heme oxygenase. Characterization of the enzyme. J. Biol. Chem. 244: 6388-6394
62. Beale S. I. (1993) Biosynthesis of phycobilins. Chem. Rev. 93: 785-802
63. Doi M., Shima S., Egashira T., Nakamura K. and Okayama S. (1997) New bile pigment excreted by a Chlamoydomonas reinhardtii mutant: a possible breakdown catabolite of chlorophyll a. J. Plant Physiol. 150: 504-508
64. Miyake K., Ohtomi M., Yoshizawa H., Sakamoto Y., Nakayama K. and Okada M. (1995) Water soluble pigments containing xylose and glucose in gametangia of the green alga, Bryopsis maxima. Plant Cell Physiol. 36: 109-113
65. Nakamura H., Musicki B., Kishi Y. and Shimomura O. (1988) Structure of the light emitter in krill (Euphausia pacifica) bioluminescence. J. Am. Chem. Soc. 110: 2683- 2685
66. Nakamura H., Kishi Y., Shimomura O., Morse D. and Hastings J. W. (1989) Structure of dinoflagellate luciferin and its enzymatic and nonenzymatic air-oxidation products. J. Am. Chem. Soc. 111: 7607-7611
67. Holden M. (1961) The breakdown of chlorophyll by chlorophyllase. Biochem. J. 78: 359-364
68. Shioi Y. and Sasa T. (1986) Purification of solubilized chlorophyllase from Chlorella protothecoides. Methods Enzymol. 123: 421-427
69. Drazkiewicz M. (1994) Chlorophyllase: occurrence, functions, mechanism of action, effects of external and internal factors. Photosynthetica 30: 321-331
70. Michalski T. J., Hunt J. E., Bradshow C., Wagner A. M., Norris J. R. and Katz J. J. (1988) Enzyme-catalyzed organic synthesis: transesterification reactions of chlorophyll a, bacteriochlorophyll a, and derivatives with chlorophyllase. J. Am. Chem. Sci. 110: 5888-5891
71. Fiedor L., Rosenbach-Belkin V. and Scherz A. (1992) The stercospecific interaction between chlorophylls and chlorophyllase. Possible implication for chlorophyll biosynthesis and degradation. J. Biol. Chem. 267: 22043-22047
72. Fiedor L., Rosenbach-Belkin V., Sai M. and Scherz A. (1996) Preparation of tetrapyrrole-amino acid covalent complexes. Plant Physiol. Biochem. 34: 393-398
73. Hynninen P. H. (1991) Chemistry of chlorophylls: modifications. In: Chlorophylls, pp. 145-209, Scheer H. (ed.), CRC Press, Boca Raton, FL
74. McFeeters R. F. (1975) Substrate specificity of chlorophyllase. Plant Physiol. 55: 377-381
75. Matile P., Schellenberg M. and Vicentini F. (1997) Localization of chlorophyllase in the chloroplast envelope. Planta 201: 96-99
76. Schneider H. (1980) Chlorophyll biosynthesis. Enzymes and regulation of enzyme activities. In: Pigments in Plants, pp. 237-307. Czygan F.-C. (ed.), Gustav Fischer, Stuttgart
77. Rüdiger W., Benz J. and Guthoff C. (1980) Detection and partial characterization of activity of chlorophyll synthase in etioplast membranes. Eur. J. Biochem. 109: 193-200
78. Soll J., Schultz G., Rüdiger W. and Benz J. (1983) Hydrogenation of geranylgeraniol: two pathways exist in spinach chloroplasts. Plant Physiol. 71: 849-854
79. Bollivar D. W., Wang S., Allen J. P. and Bauer C. E. (1994) Molecular genetic analysis of terminal steps in bacteriochlorophyll a biosynthesis: characterization of a Rhodobacter capsulatus strain that synthesizes geranylgeraniolesterified bacteriochlorophyll a. Biochemistry 33: 12763-12768
80. Oster U. and Rüdiger W. (1997) The G4 gene of Arabidopsis thaliana encodes a chlorophyll synthase of etiolated plants. Bot. Acta 110: 420-423
81. Trebitsh T., Goldschmidt E. E. 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
82. Ichinose N. and Tsutomu S. (1973) Studies on chlorophyllase of Chlorella protothecoides. III. Purification and catalytic properties. Plant Cell Physiol. 14: 1157-1166
83. Brandis A., Vainstein A. and Goldschmidt E. E. (1996) Distribution of chlorophyllase among components of chloroplast membranes in Citrus sinensis organs. Plant Physiol. Biochem. 34: 49-54
84. Purohit S. S. (1982) Prevention by kinetin of ethylene-induced chlorophyllase activity in senescing detached leaves of Helianthus annuus. Biochem. Physiol. Pflanzen 177: 625-627
85. Fang Z., Bouwkamp J. C. and Solomos T. (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wildtype of Phaseolus vulgaris L. J. Exp. Bot. 49: 503-510
86. Shimokawa K. (1982) Hydrophobic chromatographic purification of ethylene-enhanced chlorophyllase from Citrus unshiu fruits. Phytochemistry 21: 543-545
87. Nishiyama Y., Kitamura M., Tamura S. and Watanabe T. (1994) Purification and substrate specificity of chlorophyllase from Chlorella regularis. Chem. Lett. 69-72
88. Tamai H., Shioi Y. and Sasa T. (1979) Studies on chlorophyllase of Chlorella protothecoides. IV. Some properties of the purified enzyme. Plant Cell Physiol. 20: 1141-1145
89. Terpstra W. (1981) Identification of chlorophyllase as a glycoprotein. FEBS Lett. 126: 231-235
90. Tanaka K., Kakuno T., Yamashita J. and Horio T. (1982) Purification and properties of chlorophyllase from greened rye seedlings. J. Biochem. 92: 1763-1773
91. Tsuchiya T., Ohta H., Masuda T., Mikami B., Kita N., Shioi Y. and Takamiya K. (1997) Purification and characterization of two isozymes of chlorophyllase from mature leaves of Chenopodium album. Plant Cell Physiol. 38: 1026-1031
92. Vicentini F., Hörtensteiner S., Schellenberg M., Thomas H. and Matile P. (1995) Chlorophyll breakdown in senescent leaves: identification of the biochemical lesion in a stay-green genotype of Festuca pratensis Huds. New Phytol. 129: 247-252
93. Haidl H., Knödlmayer K., Rüdiger W., Scheer H., Schoch S. and Ulrich J. (1985) Degradation of bacteriochlorophyll a in Rhodopseudomonas sphaeroides R26. Z. Naturforsch. 40c: 685-692
94. Owens T. G. and Falkowski P. G. (1982) Enzymatic degradation of chlorophyll a by marine phytoplankton in vitro. Phytochemistry 21: 979-984
95. Langmeier M., Ginsburg S. and Mutile P. (1993) Chlorophyll breakdown in senescent leaves: demonstration of Mg-dechelatase activity. Physiol. Plant. 89: 347-353
96. Shioi Y., Tomita N., Tsuchiya T. and Takamiya K. (1996) Conversion of chlorophyllide to pheophorbide by Mg- dechelating substance in extracts of Chenopodium album. Plant Physiol. Biochem. 34: 41-47
97. Vicentini F., Iten F. and Matile P. (1995) Development of an assay for Mg-dechelatase of oilseed rape cotyledons, using chlorophyllin as the substrate. Physiol. Plant. 94: 57-63
98. Schellenberg M. and Matile P. (1995) Association of components of the chlorophyll catabolic system with pigment-protein complexes from solubilized chloroplast membranes. J. Plant Physiol. 146: 604-608
99. Vicentini F. (1996) Seneszenz und Blattgrün: Enzyme des Chlorophyllabbaus, Ph.D. thesis, University of Zurich
100. Schellenberg M., Matile P. and Thomas H. (1993) Production of a presumptive chlorophyll catabolite in vitro: requirement for reduced ferredoxin. Planta 191: 417-420
101. Schuler M. A. (1996) Plant cytochrome P450 monooxygenases. Critical Rev. Plant Sci. 15: 235-284
102. Halkier B. A. (1996) Catalytic reactivities and structure/function relationships of cytochrome P450 enzymes. Phytochemistry 43: 1-21
103. Hörtensteiner S., Wüthrich K. L., Matile P., Ongania K.-H. and Kräutler B. (1998) The key step in chlorophyll breakdown in higher plants. Cleavage of pheophorbide a macrocycle by a monooxygenase. J. Biol. Chem. 273: 15335-15339
104. 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
105. Lau S. M. C., Harder P. A. and O'Keefe P. A. (1993) Low carbon monoxide affinity allene oxide synthase is the pre- dominant cytochrome P450 in many plant tissues. Biochemistry 32: 1945-1950
106. Laudert D., Pfannschmidt U., Lottspeich F., Holländer- Cytko H. and Weiler E. W. (1996) Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates. Plant Mol. Biol. 31: 323-335
107. Song W. C. and Brash A. R. (1991) Purification of an allene oxide synthase and identification of the enzyme as a cytochrome P450. Science 253: 781-784
108. Hörtensteiner S. (1998) NCC malonyltransferase catalyses the final step of chlorophyll breakdown in rape (Brassica napus). Pytochemistry 49: 953-956
109. Kionka C. and Amrhein N. (1984) The enzymatic malonylation of 1-aminocyclopropane-1-carboxylic acid in homogenates of mung-bean hypocotyls. Planta 162: 226-235
110. Shioi Y., Watanabe K. and Takamiya K. (1996) Enzymatic conversion of pheophorbide a to a precursor of pyropheophorbide a in leaves of Chenopodium album. Plant Cell Physiol. 37: 1143-1149
111. Jencks W. P. (1987) Catalysis in Chemistry and Enzymology, Dover, New York
112. Hörtensteiner S., Wüthrich K. and Matile P. (1998) New aspects on the catabolic pathway of chlorophyll in senescent rape cotyledons. J. Exp. Bot. 49 (Suppl.): 65
113. Matile P., Ginsburg S., Schellenberg M. and Thomas H. (1988) Catabolites of chlorophyll in senescing barley leaves are localized in the vacuoles of mesophyll cells. Proc. Natl. Acad. Sci. USA 85: 9529-9532
114. Hinder B., Schellenberg M., Rodoni S., Ginsburg S., Vogt E., Martinoia E. et al. (1996) How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J. Biol. Chem. 271: 27233-27236
115. Eschenmoser A. (1988) Vitamin B12. Experiments concerning the origin of its molecular structure. Angew. Chem. Int. Ed. Engl. 27: 5-39
116. Hiller R. G., Anderson J. M. and Larkum W. D. (1991) The chlorophyll-protein complexes of algae. In: Chlorophylls, pp. 529-547, Scheer H. (ed.), CRC Press, Boca Raton, FL
117. Thornber J. P., Morishige D. T., Anandan S. and Peter G. F. (1991) Chlorophyll-carotenoid proteins of higher plant thyakoids. In: Chlorophylls, pp. 549-585, Schecr H. (ed.), CRC Press, Boca Raton, FL
118. Tanaka A., Ito H., Tanaka R., Tanaka N. K., Yoshida K. and Okada K. (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl. Acad. Sci. USA 95: 12719-12723
119. Schneegurt M. A. and Beale S. I. (1992) Origin of the chlorophyll b formyl oxygen in Chlorella vulgaris. Biochemistry 31: 11677-11683
120. 2in greening maize leaves. Eur. J. Biochem. 219: 671-679
121. 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
122. 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
123. Ito H., Tanaka Y., Tsuji H. and Tanaka A. (1993) Conversion of chlorophyll b to chlorophyll a by isolated cucumber etioplasts. Arch. Biochem. Biophys. 306: 148-151
124. Ito H., Takaichi S., Tsuji H. and Tanaka A. (1994) Properties of synthesis of chlorophyll a from chlorophyll b in cucumber etioplasts. J. Biol. Chem, 269: 22034-22038
125. Scheumann V., Schoch S. and Rüdiger W. (1998) Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J. Biol. Chem. 273: 35102- 35108
126. Matile P., Schellenberg M. and Peisker C. (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187: 230-235
127. Tanaka A., Yamamoto Y. and Tsuji H. (1991) Formation of chlorophyll-protein complexes during greening. 2. Redistribution of chlorophyll among apoproteins. Plant Cell Physiol. 32: 195-204
128. Ohtsuka T., Ito H. and Tanaka A. (1997) Conversion of chlorophyll b to chlorophyll a and the assembly of chlorophyll with apoproteins by isolated chloroplasts. Plant Physiol. 113: 137-147
129. Ahmed I. and Hellebust J. A. (1990) Regulation of chloroplast development by nitrogen source and growth conditions in a Chlorella protothecoides strain. Plant Physiol. 94: 944-949
130. Oshio Y. and Hase K. (1972) Changes in ribulose 1,5-diphosphate carboxylase level during processes of degeneration and regeneration of chloroplasts in Chlorella protothecoides. Plant Cell Physiol. 13: 955-963
131. Shihira-Ishikawa I. and Hase E. (1964) Nutritional control of cell pigmentation in Chlorella protothecoides with special reference to the degeneration of chloroplast induced by glucose. Plant Cell Physiol. 5: 227-240
132. Tevini M. and Steinmüller D. (1985) Composition and function of plastoglobuli. II. Lipid composition of leaves and plastoglobuli during beech leaf senescence. Planta 163: 91- 96
133. Thomas H. (1997) Chlorophyll: a symptom and a regulator of plastid development. New Phytol. 136: 163-181
134. Thomas H. and Hilditch P. (1987) Metabolism of thylakoid membrane proteins during foliar senescence. In: Plant Senescence: Its Biochemistry and Physiology, pp. 114-122. Thomson W. W., Nothnagel E. A. and Huffaker R. C. (eds)., American Society of Plant Physiologists, Rockville, MD
135. Anastassiou R. and Argyroudi-Akoyunoglou J. H. (1995) Thylakoid-bound proteolytic activity vs. exogenous azocoll substrate during chloroplast development in bean. J. Plant Physiol. 145: 24-30
136. Roulin S. and Feller U. (1998) Light-independent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: requirement for divalent cations. Planta 205: 297-304
137. Sasidharan A. and Gnanam A. (1990) Immunological identification and quantification of light harvesting chlorophyll a/b protein of Chlorella protothecoides. Indian J. Biochem. Biophys. 27: 1-4
138. 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
139. Sauer N. and Tanner W. (1985) Selection and characterization of Chlorella mutants deficient in amino acid transport. Plant Physiol. 79: 760-764
140. Jarvis E. E. and Brown L. M. (1991) Transient expression of firefly luciferase in protoplasts of the green alga Chlorella ellipsoidea. Curr. Genet. 19: 317-321
141. Singh S., Letham D. S. and Palni L. M. S. (1992) Effect of growth substances and mineral nutrients on cytokinin levels and senescence of tobacco (Nicotiana rustica) leaves. In: Progress in Plant Growth Regulation, pp. 628-634, Karseen C. M., van Loon L. C. and Vreugdenhil D. (eds), Kluwer, Dordrecht
142. Smart C. M., Scofield S. R., Bevan M. W. and Dyer T. A. (1991) Delayed leaf senescence in tobacco plants transformed with tmr, a gene for cytokinin production in Agrobacterium. Plant Cell 3: 647-656
143. Richmond A. E. and Lang A. (1957) Effect of kinetin on protein content and survival of detached Xanthium leaves. Science 125: 650-651
144. Rodoni S., Schellenberg M. and Matile P. (1998) Chlorophyll breakdown in senescing barley leaves as correlated with pheophorbide a oxygenase activity. J. Plant Physiol. 152: 139-144
145. Sabater B. and Rodriguez M. A. (1978) Control of chlorophyll degradation in detached leaves of barley and oat through effect of kinetin on chloropyllase levels. Physiol. Plant. 43: 274-276
146. Brady C. J. (1987) Fruit ripening. Ann. Rev. Plant Physiol. 38: 155-178
147. Oeller P. A., Min-Wong L., Taylor L., Pike D. A. and Theologis A. (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science 254: 437-439
148. Picton S., Barton S. L., Bouzayen M., Hamilton A. J. and Grierson D. (1993) Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme. Plant J. 3: 469-481
149. Aharoni N., Liebermann M. and Sisler H. D. (1979) Patterns of ethylene production in senescing leaves. Plant Physiol. 64: 796-800
150. Gepstein S. and Thimann K. V. (1981) The role of ethylene in the senescence of oat plants. Plant Physiol. 68: 349-354
151. Sacher J. A. (1959) Studies on auxin-membrane permeability relations in fruit and leaf tissues. Plant Physiol. 34: 365-372
152. Fletcher R. A. and Osborne D. J. (1966) Gibberellin as a regulator of protein and ribonucleic acid synthesis during senescence of leaf cells of Taraxacum officinale. Can. J. Bot. 44: 739-745
153. Chandler P. M. and Robertson M. (1994) Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45: 113-141
154. Parthier B. (1990) Jasmonates. Hormonal regulators or stress factors in leaf senescence. J. Plant Growth Regul. 9: 57-63
155. Weidhase R., Kramell H.-M., Lehmann J., Liebisch H.-W., Lerbs W. and Parthier B. (1987) Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci. 51: 177-186
156. Sembdner G. and Parthier B. (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 569- 589
157. Davies K. M. and Grierson D. (1989) Identification of cDNA clones for tomato (Lycopersicon esculentum Mill.) mRNAs that accumulate during fruit ripening and leaf senescence in response to ethylene. Planta 179: 73-80
158. Lohman K. N., Gan S., John M. C. and Amasino R. M. (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol. Plant. 92: 322-328
159. Buchanan-Wollaston V. and Ainsworth C. (1997) Leaf senescence in Brassica napus: cloning of senescence-related genes by subtractive hybridization. Plant Mol. Biol. 33: 821-834
160. Manning K. (1998) Isolation of a set of ripening-related genes from strawberry: their identification and possible relationship to fruit quality traits. Planta 205: 622-631
161. Kleber-Janke T. and Krupinska K. (1997) Isolation of cDNA clones for genes showing enhanced expression in barley leaves during dark-induced senescence as well as during senescence under field conditions. Planta 203: 332- 340
162. Smart C. M., Hosken S. E., Thomas H., Greaves J. A., Blair B. G. and Schuch W. (1995) The timing of maize leaf senescence and characterisation of senescence-related cDNAs. Physiol. Plant. 93: 673-682
163. Thomas H. (1987) Sid: a Mendelian locus controlling thylakoid membrane disassembly in senescing leaves of Festuca pratensis. Theor. Appl. Genet. 73: 551-555
164. Thomas H., Evans C., Thomas H. M., Humphreys M. W., Morgan G., Hauck B. et al. (1997) Introgression, tagging and expression of a leaf senescence gene in Festulolium. New Phytol. 137: 29-34
165. Thomas H. M., Morgan W. G., Meredith M. R., Humphreys M. W., Thomas H. and Legget J. M. (1994) Identification of parental recombined chromosomes of Lolium multiflorum x Festuca pratensis by genomic in situ hybridisation. Theor. Appl. Genet. 88: 909-913
166. Thomas H. and Smart C. M. (1993) Crops that stay green. Ann. Appl. Biol. 123: 193-219
167. Noodén L. D. and Guiamét J. J. (1996) Genetic control of senescence and aging in plants. In: Handbook of the Biology of Aging, pp. 94-117, Schneider E. L. and Rowe J. W. (eds), Academic Press, New York
168. Oh S. A., Park J.-H., Lee G. I., Pack K. H., Park S. K. and Nam H. G. (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 12: 527-535
169. Fukuda H. (1996) Xylogenesis: initiation, progression and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 299-325
170. Orzaez D. and Granell A. (1997) DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J. 11: 137-144
171. Pennell I. R. and Lamb C. (1997) Programmed cell death in plants. Plant Cell 9: 1157-1168
172. Yen C.-H. and Yang C.-H. (1998) Evidence for programmed cell death during leaf senescence in plants. Plant Cell Physiol. 39: 922-927
173. Wittenbach V. A. (1977) Induced senescence of intact wheat seedlings and its reversibility. Plant Physiol. 59: 1039-1042
174. Venkatarayappa T., Fletcher R. A. and Thompson J. E. (1984) Retardation and reversal of senescence in bean leaves by benzyladenine and decapitation. Plant Cell Physiol. 25: 407-418
175. Mothes K. (1960) Über das Altern der Blätter und die Möglichkeit ihrer Wiederverjungung. Naturwissenschaften 47: 337-351
176. Matile P. (1997) The vacuole and cell senecence. In: Advances in Botanical Research: Incorporating Advances in Plant Pathology, pp. 87-112, Callow J. A. (ed.), Academic Press, New York
177. Matile P. (1975) The Lytic Compartment of Plant Cells, Springer, Berlin
178. 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
179. Satoh H., Nakayama K. and Okada M. (1998) Molecular cloning and functional expression of a water-soluble chlorophyll protein, a putative carrier of chlorophyll molecules in cauliflower. J. Biol. Chem. 273: 30568-30575
180. Martinoia E., Grill E., Tommasini R., Kreuz K. and Amrhein N. (1993) An ATP-dependent glutathione S-conjugate 'export' pump in the vacuolar membrane of plants. Nature 364: 247-249
181. Hörtensteiner S., Vogt E., Hagenbuch B., Meier P. J., Amrhein N. and Martinoia E. (1993) Direct energization of bile acid transport into plant vacuoles. J. Biol. Chem. 268: 18446-18449
182. Kreuz K., Tommasini R. and Martinoia E. (1996) Old enzymes for a new job. Herbicide detoxification in plants. Plant Physiol. 111: 349-353
183. Rea P. A., Li Z.-S., Lu Y.-P., Drozdowicz Y. M. and Martinoia E. (1998) From vacuolar GS-X pumps to multi- specific ABC transporters. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 727-760
184. Lu Y.-P., Li Z.-S., Drozdowicz Y.-M., Hörtensteiner S., Martinoia E. and Rea P. A. (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
185. Tommasini R., Vogt E., Fromenteau M., Hörtensteiner S., Matile P., Amrhein N. et al. (1998) An ABC transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J. 13: 773- 780
186. Hilditch P. I., Thomas H., Thomas B. J. and Rogers L. J. (1989) Leaf senescence in a non-yellowing mutant of Festuca pratensis: proteins of photosystem II. Planta 177: 265-272