The stay-green revolution: Recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants

Plant Science

Volumn 176, Issue 3, 2009, Pages 325-333

  Barry, Cornelius S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Chlorophyll degradation; Fruit ripening; Pigment protein complex; Senescence; Stay green

Indexed keywords

ARABIDOPSIS; EMBRYOPHYTA;

EID: 58749107860     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2008.12.013     Document Type: Review

References (75)

1. Hortensteiner S. Chlorophyll degradation during senescence. Annu. Rev. Plant Biol. 57 (2006) 55-77
2. Thomas H., and Howarth C.J. Five ways to stay green. J. Exp. Bot. 51 (2000) 329-337
3. Jacob-Wilk D., Holland D., Goldschmidt E.E., Riov J., and Eyal Y. 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 (1999) 653-661
4. Tsuchiya T., Ohta H., Okawa K., Iwamatsu A., Shimada H., Masuda T., and Takamiya K. Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 15362-15367
5. Pruzinska A., Tanner G., Anders I., Roca M., and Hortensteiner S. Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 15259-15264
6. Gray J., Close P.S., Briggs S.P., and Johal G.S. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89 (1997) 25-31
7. Wuthrich K.L., Bovet L., Hunziker P.E., Donnison I.S., and Hortensteiner S. Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. Plant J. 21 (2000) 189-198
8. Mach J.M., Castillo A.R., Hoogstraten R., and Greenberg J.T. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 771-776
9. Suzuki T., Kunieda T., Murai F., Morioka S., and Shioi Y. Mg-dechelation activity in radish cotyledons with artificial and native substrates, Mg-chlorophyllin a and chlorophyllide a. Plant Physiol. Biochem. 43 (2005) 459-464
10. Suzuki T., and Shioi Y. Re-examination of Mg-dechelation reaction in the degradation of chlorophylls using chlorophyllin a as a substrate. Photosynth. Res. 74 (2002) 217-223
11. Rudiger W. Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth. Res. 74 (2002) 187-193
12. Tsuchiya T., Suzuki T., Yamada T., Shimada H., Masuda T., Ohta H., and Takamiya K. Chlorophyllase as a serine hydrolase: identification of a putative catalytic triad. Plant Cell Physiol. 44 (2003) 96-101
13. Harpaz-Saad S., Azoulay T., Arazi T., Ben-Yaakov E., Mett A., Shiboleth Y.M., Hortensteiner S., Gidoni D., Gal-On A., Goldschmidt E.E., and Eyal Y. Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19 (2007) 1007-1022
14. Fujii H., Shimada T., Sugiyama A., Nishikawa F., Endo T., Nakano M., Ikoma Y., Shimizu T., and Omura M. Profiling ethylene-responsive genes in mature mandarin fruit using a citrus 22K oligoarray. Plant Sci. 173 (2007) 340-348
15. Shemer T.A., Harpaz-Saad S., Belausov E., Lovat N., Krokhin O., Spicer V., Standing K.G., Goldschmidt E.E., and Eyal Y. Citrus chlorophyllase dynamics at ethylene-induced fruit color-break: a study of chlorophyllase expression, posttranslational processing kinetics, and in situ intracellular localization. Plant Physiol. 148 (2008) 108-118
16. Brandis A., Vainstein A., and Goldschmidt E.E. Distribution of chlorophyllase among components of chloroplast membranes in Citrus sinensis organs. Plant Physiol. Biochem. 34 (1996) 49-54
17. Matile P., Schellenberg M., and Vicentini F. Localization of chlorophyllase in the chloroplast envelope. Planta 201 (1997) 96-99
18. Schellenberg M., and Matile P. Association of components of the chlorophyll catabolic system with pigment-protein complexes from solubilized chloroplast membranes. J. Plant Physiol. 146 (1995) 604-608
19. Trebitsh T., Goldschmidt E.E., and Riov J. Ethylene induces de novo synthesis of chlorophyllase, a chlorophyll degrading enzyme, in citrus fruit peel. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 9441-9445
20. Schenk N., Schelbert S., Kanwischer M., Goldschmidt E.E., Dormann P., and Hortensteiner S. The chlorophyllases AtCLH1 and AtCLH2 are not essential for senescence-related chlorophyll breakdown in Arabidopsis thaliana. FEBS Lett. 581 (2007) 5517-5525
21. Kariola T., Brader G., Li J., and Palva E.T. Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17 (2005) 282-294
22. Chen L.F.O., Lin C.H., Kelkar S.M., Chang Y.M., and Shaw J.F. Transgenic broccoli (Brassica oleracea var. italicia) with antisense chlorophyllase (BoCLH1) delays postharvest yellowing. Plant Sci. 174 (2008) 25-31
23. Pruzinska A., Anders I., Aubry S., Schenk N., Tapernoux-Luthi E., Muller T., Krautler B., and Hortensteiner S. In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19 (2007) 369-387
24. Pruzinska A., Tanner G., Aubry S., Anders I., Moser S., Muller T., Ongania K.H., Krautler B., Youn J.Y., Liljegren S.J., and Hortensteiner S. Chlorophyll breakdown in senescent Arabidopsis leaves, characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol. 139 (2005) 52-63
25. Kleffmann T., Russenberger D., von Zychlinski A., Christopher W., Sjolander K., Gruissem W., and Baginsky S. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14 (2004) 354-362
26. Yao N., and Greenberg J.T. Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18 (2006) 397-411
27. Suzuki Y., Amano T., and Shioi Y. Characterization and cloning of the chlorophyll-degrading enzyme pheophorbidase from cotyledons of radish. Plant Physiol. 140 (2006) 716-725
28. Hilditch P.I., Thomas H., Thomas B.J., and Rogers L.J. Leaf senescence in a non-yellowing mutant of Festuca pratensis-proteins of photosystem II. Planta 177 (1989) 265-272
29. Thomas H. Sid-a Mendelian locus controlling thylakoid membrane disassembly in senescing leaves of Festuca pratensis. Theor. Appl. Genet. 73 (1987) 551-555
30. Thomas H., Morgan W.G., Thomas A.M., and Ougham H.J. Expression of the stay-green character introgressed into Lolium temulentum Ceres from a senescence mutant of Festuca pratensis. Theor. Appl. Genet. 99 (1999) 92-99
31. Moore B.J., Donnison I.S., Harper J.A., Armstead I.P., King J., Thomas H., Jones R.N., Jones T.H., Thomas H.M., Morgan W.G., Thomas A., Ougham H.J., Huang L., Fentem T., Roberts L.A., and King I.P. Molecular tagging of a senescence gene by introgression mapping of a stay-green mutation from Festuca pratensis. New Phytol. 165 (2005) 801-806
32. Armstead I., Donnison I., Aubry S., Harper J., Hortensteiner S., James C., Mani J., Moffet M., Ougham H., Roberts L., Thomas A., Weeden N., Thomas H., and King I. From crop to model to crop: identifying the genetic basis of the staygreen mutation in the Lolium/Festuca forage and amenity grasses. New Phytol. 172 (2006) 592-597
33. Armstead I., Donnison I., Aubry S., Harper J., Hortensteiner S., James C., Mani J., Moffet M., Ougham H., Roberts L., Thomas A., Weeden N., Thomas H., and King I. Cross-species identification of Mendel's/locus. Science 315 (2007) 73-173
34. Park S.Y., Yu J.W., Park J.S., Li J., Yoo S.C., Lee N.Y., Lee S.K., Jeong S.W., Seo H.S., Koh H.J., Jeon J.S., Park Y.I., and Paek N.C. The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19 (2007) 1649-1664
35. Ren G.D., An K., Liao Y., Zhou X., Cao Y.J., Zhao H.F., Ge X.C., and Kuai B.K. Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 144 (2007) 1429-1441
36. Aubry S., Mani J., and Hortensteiner S. Stay-green protein, defective in Mendel's green cotyledon mutant, acts independent and upstream of pheophorbide a oxygenase in the chlorophyll catabolic pathway. Plant Mol. Biol. 67 (2008) 243-256
37. Barry C.S., McQuinn R.P., Chung M.-Y., Besuden A., and Giovannoni J.J. Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol. 147 (2008) 179-187
38. Borovsky Y., and Paran I. Chlorophyll breakdown during pepper fruit ripening in the chlorophyll retainer mutation is impaired at the homolog of the senescence-inducible stay-green gene. Theor. Appl. Genet. 117 (2008) 235-240
39. Jiang H.W., Li M.R., Liang N.B., Yan H.B., Wei Y.L., Xu X., Liu J.F., Xu Z., Chen F., and Wu G.J. Molecular cloning and function analysis of the stay green gene in rice. Plant J. 52 (2007) 197-209
40. Sato Y., Morita R., Nishimura M., Yamaguchi H., and Kusaba M. Mendel's green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 14169-14174
41. Roca M., James C., Pruzinska A., Hortensteiner S., Thomas H., and Ougham H. Analysis of the chlorophyll catabolism pathway in leaves of an introgression senescence mutant of Lolium temulentum. Phytochemistry 65 (2004) 1231-1238
42. Ougham H., Hortensteiner S., Armstead I., Donnison I., King I., Thomas H., and Mur L. The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. Plant Biol. 10 (2008) 4-14
43. Zelisko A., Garcia-Lorenzo M., Jackowski G., Jansson S., and Funk C. AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 13699-13704
44. Hruz T., Laule O., Szabo G., Wessendorp F., Bleuler S., Oertle L., Widmayer P., Gruissem W., and Zimmermann P. Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics (2008) 10.1155/2008/420747
45. Sebaihia M., Peck M.W., Minton N.P., Thomson N.R., Holden M.T.G., Mitchell W.J., Carter A.T., Bentley S.D., Mason D.R., Crossman L., Paul C.J., Ivens A., Wells-Bennik M.H.J., Davis I.J., Cerdeno-Tarraga A.M., Churcher C., Quail M.A., Chillingworth T., Feltwell T., Fraser A., Goodhead I., Hance Z., Jagels K., Larke N., Maddison M., Moule S., Mungall K., Norbertczak H., Rabbinowitsch E., Sanders M., Simmonds M., White B., Whithead S., and Parkhill J. Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res. 17 (2007) 1082-1092
46. Zverlov V.V., and Schwarz W.H. Bacterial cellulose hydrolysis in anaerobic environmental subsystems-Clostridium thermocellum and Clostridium stercorarium thermophilic plant-fiber degraders. In: Wiegel J., Maier R.J., and Adams M.W.W. (Eds). Incredible Anaerobes: From Physiology to Genomics to Fuels (2008), Blackwell Publishing 298-307
47. Heap J.T., Pennington O.J., Cartman S.T., Carter G.P., and Minton N.P. The ClosTron: a universal gene knock-out system for the genus Clostridium. J. Microbiol. Methods 70 (2007) 452-464
48. O'Connor J.R., Lyras D., Farrow K.A., Adams V., Powell D.R., Hinds J., Cheung J.K., and Rood J.I. Construction and analysis of chromosomal Clostridium difficile mutants. Mol. Microbiol. 61 (2006) 1335-1351
49. Kusaba M., Ito H., Morita R., Iida S., Sato Y., Fujimoto M., Kawasaki S., Tanaka R., Hirochika H., Nishimura M., and Tanaka A. Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19 (2007) 1362-1375
50. Espineda C.E., Linford A.S., Devine D., and Brusslan J.A. The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 10507-10511
51. Oster U., Tanaka R., Tanaka A., and Rudiger W. Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J. 21 (2000) 305-310
52. Tanaka A., Ito H., Tanaka R., Tanaka N.K., Yoshida K., and Okada K. Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12719-12723
53. Sato Y., Morita R., Katsuma S., Nishimura M., Tanaka A., and Kusaba M. Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J. 57 (2009) 120-131
54. Goldschmidt E.E., Huberman M., and Goren R. Probing the role of endogenous ethylene in the degreening of citrus fruit with ethylene antagonists. Plant Growth Regul. 12 (1993) 325-329
55. Purvis A.C., and Barmore C.R. Involvement of ethylene in chlorophyll degradation in peel of citrus fruits. Plant Physiol. 68 (1981) 854-856
56. Paran I., and van der Knaap E. Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J. Exp. Bot. 58 (2007) 3841-3852
57. Kerr E.A. Green flesh, gf Rpt. Tomato Genet. Coop. 6 (1956) 17
58. Efrati A., Eyal Y., and Paran I. Molecular mapping of the chlorophyll retainer (cl) mutation in pepper (Capsicum spp.) and screening for candidate genes using tomato ESTs homologous to structural genes of the chlorophyll catabolism pathway. Genome 48 (2005) 347-351
59. Roca M., and Minguez-Mosquera M.I. Chlorophyll catabolism pathway in fruits of Capsicum annuum (L.): stay-green versus red fruits. J. Agric. Food Chem. 54 (2006) 4035-4040
60. Akhtar M.S., Goldschmidt E.E., John I., Rodoni S., Matile P., and Grierson D. Altered patterns of senescence and ripening in gf, a stay-green mutant of tomato (Lycopersicon esculentum Mill). J. Exp. Bot. 50 (1999) 1115-1122
61. Cheung A.-Y., McNellis T., and Piekos B. Maintenance of chloroplast components during chromoplast differentiation in the tomato mutant green flesh. Plant Physiol. 101 (1993) 1223-1229
62. Tanksley S.D., Ganal M.W., Prince J.P., De-Vicente M.C., Bonierbale M.W., Broun P., Fulton T.M., Giovannoni J.J., and Grandillo S. High density molecular linkage maps of the tomato and potato genomes. Genetics 132 (1992) 1141-1160
63. Livingstone K.D., Lackney V.K., Blauth J.R., van Wijk R., and Jahn M.K. Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152 (1999) 1183-1202
64. Alos E., Roca M., Iglesias D.J., Minguez-Mosquera M.I., Damasceno C.M.B., Thannhauser T.W., Rose J.K.C., Talon M., and Cercos M. An evaluation of the basis and consequences of a stay-green mutation in the navel negra citrus mutant using transcriptomic and proteomic profiling and metabolite analysis. Plant Physiol. 147 (2008) 1300-1315
65. Ramirez D.A., and Tomes M.L. Relationship between chlorophyll and carotenoid biosynthesis in dirty-red (green-flesh) mutant in tomato. Bot. Gaz. 125 (1964) 221-226
66. Roca M., Hornero-Mendez D., Gandul-Rojas B., and Minguez-Mosquera M.I. Stay-green phenotype slows the carotenogenic process in Capsicum annuum (L.) fruits. J. Agric. Food Chem. 54 (2006) 8782-8787
67. Goff S.A., and Klee H.J. Plant volatile compounds: sensory cues for health and nutritional value?. Science 311 (2006) 815-819
68. Moser S., Müller T., Ebert M.-O., Jockusch S., Turro N., and Kräutler B. Blue luminescence of ripening bananas. Angew. Chem. Int. Ed. 47 (2008) 8954-8957
69. Muller T., Ulrich M., Ongania K.H., and Krautler B. Colorless tetrapyrrolic chlorophyll catabolites found in ripening fruit are effective antioxidants. Angew. Chem. Int. Ed. 46 (2007) 8699-8702
70. Gapper N.E., Coupe S.A., McKenzie M.J., Scott R.W., Christey M.C., Lill R.E., McManus M.T., and Jameson P.E. Senescence-associated down-regulation of 1-aminocyclopropane-1-carboxylate (ACC) oxidase delays harvest-induced senescence in broccoli. Funct. Plant Biol. 32 (2005) 891-901
71. Chen L.F.O., Huang J.Y., Wang Y.H., Chen Y.T., and Shaw J.F. Ethylene insensitive and post-harvest yellowing retardation in mutant ethylene response sensor (BoERS) gene transformed broccoli (Brassica olercea var. italica). Mol. Breeding 14 (2004) 199-213
72. Gan S.S., and Amasino R.M. Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270 (1995) 1986-1988
73. McCabe M.S., Garratt L.C., Schepers F., Jordi W., Stoopen G.M., Davelaar E., van Rhijn J.H.A., Power J.B., and Davey M.R. Effects of P-SAG12-IPT gene expression on development and senescence in transgenic lettuce. Plant Physiol. 127 (2001) 505-516
74. Chen L.F.O., Hwang J.Y., Charng Y.Y., Sun C.W., and Yang S.F. Transformation of broccoli (Brassica oleracea var. italica) with isopentenyltransferase gene via Agrobacterium tumefaciens for post-harvest yellowing retardation. Mol. Breeding 7 (2001) 243-257
75. Thomas H. Chlorophyll: a symptom and a regulator of plastid development. New Phytol. 136 (1997) 163-181