STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis

Plant Cell

Volumn 24, Issue 2, 2012, Pages 507-518

  Sakuraba, Yasuhito ^a   Schelbert, Silvia ^b   Park, So Yon ^a,d   Han, Su Hyun ^a   Lee, Byoung Doo ^a   Andrès, Céline Besagni ^c   Kessler, Felix ^c   Hörtensteiner, Stefan ^b   Paek, Nam Chon ^a  

^a Seoul National University   (South Korea)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^d UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

EID: 84859067812     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.089474     Document Type: Article

References (54)

1. Aubry, S., Mani, J., and Hörtensteiner, S. (2008). 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: 243-256.
2. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S., and Ohad, N. (2004). Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40: 419-427.
3. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K.M., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
4. Endler, A., Meyer, S., Schelbert, S., Schneider, T., Weschke, W., Peters, S.W., Keller, F., Baginsky, S., Martinoia, E., and Schmidt, U.G. (2006). Identification of a vacuolar sucrose transporter in barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol. 141: 196-207.
5. Ginsburg, S., Schellenberg, M., and Matile, P. (1994). Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol. 105: 545-554.
6. Guiboileau, A., Sormani, R., Meyer, C., and Masclaux-Daubresse, C. (2010). Senescence and death of plant organs: nutrient recycling and developmental regulation. C. R. Biol. 333: 382-391.
7. Horie, Y., Ito, H., Kusaba, M., Tanaka, R., and Tanaka, A. (2009). Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J. Biol. Chem. 284: 17449-17456.
8. Hörtensteiner, S. (2004). The loss of green color during chlorophyll degradation-A prerequisite to prevent cell death? Planta 219: 191-194.
9. Hörtensteiner, S. (2006). Chlorophyll degradation during senescence. Annu. Rev. Plant Biol. 57: 55-77.
10. Hörtensteiner, S. (2009). Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci. 14: 155-162.
11. Hörtensteiner, S., and Feller, U. (2002). Nitrogen metabolism and remobilization during senescence. J. Exp. Bot. 53: 927-937.
12. Hörtensteiner, S., and Krä utler, B. (2011). Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 1807: 977-988.
13. 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.
14. Jiang, H., Li, M., Liang, N., Yan, H., Wei, Y., Xu, X., Liu, J., Xu, Z., Chen, F., and Wu, G. (2007). Molecular cloning and function analysis of the stay green gene in rice. Plant J. 52: 197-209.
15. Jørgensen, K., Rasmussen, A.V., Morant, M., Nielsen, A.H., Bjarnholt, N., Zagrobelny, M., Bak, S., and Møller, B.L. (2005). Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr. Opin. Plant Biol. 8: 280-291.
16. Joyard, J., Ferro, M., Masselon, C., Seigneurin-Berny, D., Salvi, D., Garin, J., and Rolland, N. (2009). Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol. Plant 2: 1154-1180.
17. Krä utler, B. (2008). Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit. Photochem. Photobiol. Sci. 7: 1114-1120.
18. Krä utler, 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.
19. Kreuz, K., Tommasini, R., and Martinoia, E. (1996). Old enzymes for a new job. Herbicide detoxification in plants. Plant Physiol. 111: 349-353.
20. Kusaba, M., Ito, H., Morita, R., Iida, S., Sato, Y., Fujimoto, M., Kawasaki, S., Tanaka, R., Hirochika, H., Nishimura, M., and Tanaka, A. (2007). Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19: 1362-1375.
21. Lim, P.O., Kim, H.J., and Nam, H.G. (2007). Leaf senescence. Annu. Rev. Plant Biol. 58: 115-136.
22. Mach, J.M., Castillo, A.R., Hoogstraten, R., and Greenberg, J.T. (2001). The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98: 771-776.
23. Matile, P., Hörtensteiner, S., and Thomas, H. (1999). Chlorophyll degradation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 67-95.
24. 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.
25. Matile, P., Schellenberg, M., and Peisker, C. (1992). Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187: 230-235.
26. Meguro, M., Ito, H., Takabayashi, A., Tanaka, R., and Tanaka, A. (2011). Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23: 3442-3453.
27. Meyer, A., Eskandari, S., Grallath, S., and Rentsch, D. (2006). AtGAT1, a high affinity transporter for gamma-aminobutyric acid in Arabidopsis thaliana. J. Biol. Chem. 281: 7197-7204.
28. Mochizuki, N., Tanaka, R., Grimm, B., Masuda, T., Moulin, M., Smith, A.G., Tanaka, A., and Terry, M.J. (2010). The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci. 15: 488-498.
29. Morita, R., Sato, Y., Masuda, Y., Nishimura, M., and Kusaba, M. (2009). Defect in non-yellow coloring 3, an alpha/beta hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J. 59: 940-952.
30. Oberhuber, M., Berghold, J., Breuker, K., Hörtensteiner, S., and Krä utler, B. (2003). Breakdown of chlorophyll: a nonenzymatic reaction accounts for the formation of the colorless "nonfluorescent" chlorophyll catabolites. Proc. Natl. Acad. Sci. USA 100: 6910-6915.
31. Park, S.-Y., et al. (2007). The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19: 1649-1664.
32. Porra, R.J., Thompson, W.A., and Kriedemann, P.E. (1989). Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and chlorophyll b extracted with 4 different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975: 384-394.
33. Pružinská, A., Anders, I., Aubry, S., Schenk, N., Tapernoux-Lüthi, E., Müller, T., Krä utler, B., and Hörtensteiner, S. (2007). In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19: 369-387.
34. Pružinská, A., Tanner, G., Anders, I., Roca, M., and Hörtensteiner, S. (2003). 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 100: 15259-15264.
35. Pružinská, A., Tanner, G., Aubry, S., Anders, I., Moser, S., Müller, T., Ongania, K.-H., Krä utler, B., Youn, J.-Y., Liljegren, S.J., and Hörtensteiner, S. (2005). Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol. 139: 52-63.
36. Ren, G., An, K., Liao, Y., Zhou, X., Cao, Y., Zhao, H., Ge, X., and Kuai, B. (2007). Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 144: 1429-1441.
37. Ren, G.D., Zhou, Q., Wu, S.X., Zhang, Y.F., Zhang, L.G., Huang, J.R., Sun, Z.F., and Kuai, B.K. (2010). Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J. Integr. Plant Biol. 52: 496-504.
38. Rodoni, S., Mühlecker, W., Anderl, M., Kräutler, B., Moser, D., Thomas, H., Matile, P., and Hörtensteiner, S. (1997). Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps. Plant Physiol. 115: 669-676.
39. Sakuraba, Y., Yokono, M., Akimoto, S., Tanaka, R., and Tanaka, A. (2010). Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in Arabidopsis thaliana. Plant Cell Physiol. 51: 1055-1065.
40. Sato, Y., Morita, R., Katsuma, S., Nishimura, M., Tanaka, A., and Kusaba, M. (2009). 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: 120-131.
41. Sato, Y., Morita, R., Nishimura, M., Yamaguchi, H., and Kusaba, M. (2007). Mendel's green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc. Natl. Acad. Sci. USA 104: 14169-14174.
42. Scheibe, R., Wedel, N., Vetter, S., Emmerlich, V., and Sauermann, S.M. (2002). Co-existence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269: 5617-5624.
43. Schelbert, S., Aubry, S., Burla, B., Agne, B., Kessler, F., Krupinska, K., and Hörtensteiner, S. (2009). Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21: 767-785.
44. Schenk, N., Schelbert, S., Kanwischer, M., Goldschmidt, E.E., Dörmann, P., and Hörtensteiner, S. (2007). The chlorophyllases AtCLH1 and AtCLH2 are not essential for senescence-related chlorophyll breakdown in Arabidopsis thaliana. FEBS Lett. 581: 5517-5525.
45. Shlyk, A.A. (1971). Biosynthesis of chlorophyll b. Annu. Rev. Plant Physiol. 22: 169-184.
46. Takamiya, K.I., Tsuchiya, T., and Ohta, H. (2000). Degradation pathway(s) of chlorophyll: What has gene cloning revealed? Trends Plant Sci. 5: 426-431.
47. Tanaka, R., Hirashima, M., Satoh, S., and Tanaka, A. (2003). The Arabidopsis-accelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: Inhibition of the pheophorbide a oxygenase activity does not lead to the "stay-green" phenotype in Arabidopsis. Plant Cell Physiol. 44: 1266-1274.
48. Tanaka, R., and Tanaka, A. (2007). Tetrapyrrole biosynthesis in higher plants. Annu. Rev. Plant Biol. 58: 321-346.
49. Thomas, H., and Howarth, C.J. (2000). Five ways to stay green. J. Exp. Bot. 51(Spec No): 329-337.
50. Thomas, H., Ougham, H.J., Wagstaff, C., and Stead, A.D. (2003). Defining senescence and death. J. Exp. Bot. 54: 1127-1132.
51. Vidi, P.A., Kanwischer, M., Baginsky, S., Austin, J.R., Csucs, G., Dörmann, P., Kessler, F., and Bréhélin, C. (2006). Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J. Biol. Chem. 281: 11225-11234.
52. Zavaleta-Mancera, H.A., Franklin, K.A., Ougham, H.J., Thomas, H., and Scott, I.M. (1999a). Regreening of senescent Nicotiana leaves I. Reappearance of NADPH-protochlorophyllide oxidoreductase and light-harvesting chlorophyll a/b-binding protein. J. Exp. Bot. 50: 1677-1682.
53. Zavaleta-Mancera, H.A., Thomas, B.J., Thomas, H., and Scott, I.M. (1999b). Regreening of senescent Nicotiana leaves II. Redifferentiation of plastids. J. Exp. Bot. 50: 1683-1689.
54. Zhang, X.R., Henriques, R., Lin, S.S., Niu, Q.W., and Chua, N.H. (2006). Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1: 641-646.