Rubiscolytics: Fate of Rubisco after its enzymatic function in a cell is terminated

Journal of Experimental Botany

Volumn 59, Issue 7, 2008, Pages 1615-1624

  Feller, Urs ^a   Anders, Iwona ^a   Mae, Tadahiko ^b  

^a UNIVERSITY OF BERN   (Switzerland)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Chloroplast; Endopeptidase; Nitrogen remobilization; Phloem transport; Proteolysis; Rubisco; Stress; Vacuole

Indexed keywords

RIBULOSEBISPHOSPHATE CARBOXYLASE;

CONFERENCE PAPER; CYTOLOGY; ENZYMOLOGY; METABOLISM; PLANT;

PLANTS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

GLYCINE MAX; TRITICUM AESTIVUM;

EID: 44649118756     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erm242     Document Type: Conference Paper

References (85)

1. Adam Z, Clarke AK. 2002. Cutting edge of chloroplast proteolysis. Trends in Plant Science 7, 451-465.
2. Bhalerao R, Keskitalo J, Sterky F, et al. 2003. Gene expression in autumn leaves. Plant Physiology 131, 1-13.
3. Buchanan-Wollaston V. 1997. The molecular biology of senescence. Journal of Experimental Botany 48, 181-199.
4. Buchanan-Wollaston V, Earl S, Harrison E, Maths E, Navabpour S, Page T, Pink D. 2003. The molecular analysis of leaf senescence - a genomics approach. Plant Biotechnology Journal 1, 3-22.
5. Bushnell TP, Bushnell D, Jagendorf AT. 1993. A purified zinc protease of pea chloroplasts, EP1, degrades the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 103, 585-591.
6. Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T. 2003. Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant and Cell Physiology 44, 914-921.
7. Crafts-Brandner SJ, Egli DB. 1987. Sink removal and leaf senescence in soybean. Cultivar effects. Plant Physiology 85, 662-666.
8. Crafts-Brandner SJ, Hölzer R, Feller U. 1998. Influence of nitrogen deficiency on senescence and the amounts of RNA and proteins in wheat leaves. Physiologia Plantarum 102, 192-200.
9. Crafts-Brandner SJ, Klein RR, Klein P, Hölzer R, Feller U. 1996. Coordination of protein and mRNA abundances of stromal enzymes and abundances of the Clp protease subunits during senescence of Phaseolus vulgaris (L.) leaves. Planta 200, 312-318.
10. 2 exchange and activities of ribulose bisphosphate carboxylase/ oxygenase and phosphoenolpyruvate carboxylase of maize hybrids and inbred lines. Plant Physiology 84, 261-265.
11. Crafts-Brandner SJ, Salvucci ME. 1994. The Rubisco complex protein - a protein-induced by fruit removal that forms a complex with ribulose-1,5-bisphosphate carboxylase/oxygenase. Planta 194, 110-116.
12. Debrunner N, Feller U. 1995. Solute leakage from detached plant parts of winter wheat: influence of maturation stage and incubation temperature. Journal of Plant Physiology 145, 257-260.
13. Debrunner N, von Lerber F, Feller U. 1999. Solute losses from various shoot parts of field-grown wheat by leakage in the rain. In: Anacx C, Martin-Prével P, eds. Improved crop quality by nutrient management. Dordrecht: Kluwer Academic Publishers, 131-134.
14. Demirevska-Kepova K, Feller U. 2004. Heat sensitivity of Rubisco, Rubisco activase and Rubisco binding protein in higher plants. Acta Physiologiae Plantarum 26, 103-114.
15. Demirevska-Kepova K, Hölzer R, Simova-Stoilova L, Feller U. 2005. Heat stress effects on Rubisco, Rubisco binding protein and Rubisco activase in wheat leaves. Biologia Plantarum 49, 521-525.
16. Desimone M, Henke A, Wagner E. 1996. Oxidative stress induces partial degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiology 111, 789-796.
17. Desimone M, Wagner E, Johanningmeier U. 1998. Degradation of active-oxygen modified ribulose-1,5-bisphosphate carboxylase/oxygenase by chloroplastic proteases requires ATP-hydrolysis. Planta 205, 459-466.
18. Ellis RJ. 1979. The most abundant protein in the world. Trends in Biochemical Sciences 4, 241-244.
19. Evans JR, Seemann JR. 1989. The allocation of protein nitrogen in the photosynthetic apparatus: cost, consequences and control. In: Briggs WR, ed. Photosynthesis. New York: Alan R. Liss Inc., 183-205.
20. Feller U. 1978. Changes in nitrogen contents and in proteolytic activities in different parts of field-grown wheat ears (Triticum aestivum L.) during maturation. Plant and Cell Physiology 19, 1489-1495.
21. Feller U. 1990. Nitrogen remobilization and protein degradation during senescence. In: Abrol YP, ed. Nitrogen in higher plants. Somerset: Research Studies Press Ltd, 195-222.
22. Feller U. 2004. Proteolysis. In: Noodén LD, ed. Plant cell death processes. San Diego: Academic Press, 107-123.
23. Feller U, Crafts-Brandner SJ, Salvucci ME. 1998. Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiology 116, 539-546.
24. Feller U, Erismann KH. 1978. Changes in gas exchange and in the activities of proteolytic enzymes during senescence of wheat leaves (Triticum aestivum L.). Zeitschrift für Pflanzenphysiologie 90, 235-244.
25. Feller U, Fischer A. 1994. Nitrogen metabolism in senescing leaves. Critical Reviews in Plant Sciences 13, 241-273.
26. Feller UK, Soong T-ST, Hageman RH. 1977. Leaf proteolytic activities and senescence during grain development of fieldgrown corn (Zea mays L.). Plant Physiology 59, 290-294.
27. Fischer A, Feller U. 1994. Senescence and protein degradation in leaf segments of young winter wheat: influence of leaf age. Journal of Experimental Botany 45, 103-109.
28. Franceschi VR, Giaquinta RT. 1983. Specialized cellular arrangements in legume leaves in relation to assimilate transport and compartmentation - comparison of the paraveinal mesophyll. Planta 159, 415-422.
29. Franceschi VR, Wittenbach VA, Giaquinta RT. 1983. Paraveinal mesophyll of soybean leaves in relation to assimilate transfer and compartmentation. III. Immunohistochemical localization of specific glycopeptides in the vacuole after depodding. Plant Physiology 72, 586-589.
30. Fröhlich V, Feller U. 1992. Effect of phloem interruption on endopeptidase and aminopeptidase activities in flag leaves of field-grown wheat. Biochemie und Physiologie der Pflanzen 188, 13-21.
31. 2 in the wheat ear. Australian Journal of Plant Physiology 28, 1047-1053.
32. Gietl C, Schmid M. 2001. Ricinosomes: an organelle for developmentally regulated cell death in senescing plant tissues. Naturwissenschaften 88, 49-58.
33. Guiamét JJ, Pichersky E, Noodén LD. 1999. Mass exodus from senescing soybean chloroplasts. Plant and Cell Physiology 40, 986-992.
34. Gutteridge S, Millard BN, Parry MAJ. 1986. Inactivation of ribulose-bisphosphate carboxylase by limited proteolysis. FEBS Letters 196, 263-268.
35. 2, light and temperature influence senescence and protein degradation in wheat leaf segments. Physiologia Plantarum 103, 320-326.
36. Hildbrand M, Fischer A, Feller U. 1994. Protein catabolism in bean leaf discs: accumulation of a soluble fragment of ribulose-1,5-bisphosphate carboxylase/oxygenase under oxygen deficiency. Journal of Experimental Botany 45, 1197-1204.
37. Hörtensteiner S. 2006. Chlorophyll degradation during senescence. Annual Review of Plant Biology 57, 55-77.
38. Hörtensteiner S, Feller U. 2002. Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53, 927-937.
39. Houtz RL, Mulligan RM. 1991. Protection of tryptic-sensitive sites in the large subunit of ribulosebisphosphate carboxylase/oxygenase by catalysis. Plant Physiology 96, 335-339.
40. Ishida H, Makino A, Mae T. 1999. Fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase by reactive oxygen species occurs near Gly-329. Journal of Biological Chemistry 274, 5222-5226.
41. Ishida H, Nishimori Y, Sugisawa M, Makino A, Mae T. 1997. The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented into 37-kDa and 16-kDa polypeptides by active oxygen species in the lysates of chloroplasts from primary leaves of wheat. Plant and Cell Physiology 38, 471-479.
42. Ishida H, Shimizu S, Makino A, Mae T. 1998. Light-dependent fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts isolated from wheat. Planta 204, 305-309.
43. Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F. 2004. The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220, 97-104.
44. Khan S, Andralojc PJ, Lea PJ, Parry MAJ. 1999. 2′-Carboxy-D-arabinitol 1-phosphate protects ribulose 1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown. European Journal of Biochemistry 266, 840-847.
45. Klauer SF, Franceschi VR, Ku MSB, Zhang DZ. 1996. Identification and localization of vegetative storage proteins in legume leaves. American Journal of Botany 83, 1-10.
46. Kokubun N, Ishida H, Makino A, Mae T. 2002. The degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase into the 44-kDa fragment in the lysates of chloroplasts incubated in darkness. Plant and Cell Physiology 43, 1390-1395.
47. Kumar PA, Parry MAJ, Mitchell RAC, Ahmad A, Abrol YP. 2002. Photosynthesis and nitrogen use-efficiency. In: Foyer CH, Noctor G, eds. Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Dordrecht: Kluwer Academic Publishers, 23-34.
48. 2+-catalyzed site-specific cleavage of the large subunit of ribulose 1,5-bisphosphate carboxylase close to the active site. Journal of Biological Chemistry 277, 12383-12387.
49. Mae T. 2004. Leaf senescence and nitrogen metabolism. In: Noodén LD, ed. Plant cell death processes. San Diego: Academic Press, 157-168.
50. Makino A. 2003. Rubisco and nitrogen relationships in rice. Leaf photosynthesis and plant growth. Soil Science and Plant Nutrition 49, 319-327.
51. Makino A, Sakuma H, Sudo E, Mae T. 2003. Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant and Cell Physiology 44, 952-956.
52. Marín-Navarro J, Moreno J. 2006. Cysteines 449 and 459 modulate the reduction-oxidation conformational changes of ribulose 1,5-bisphosphate carboxylase/oxygenase and the translocation of the enzyme to membranes during stress. Plant, Cell and Environment 29, 898-908.
53. Martinez DE, Luguez VM, Bartoli CG, Guiamet JJ. 2003. Persistence of photosynthetic components and photochemical efficiency in ears of water-stressed wheat (Triticum aestivum). Physiologia Plantarum 119, 519-525.
54. Minamikawa T, Toyooka K, Okamoto T, Hara-Nishimura I, Nishimura M. 2001. Degradation of ribulose-bisphosphate carboxylase by vacuolar enzymes of senescing French bean leaves: immunocytochemical and ultrastructural observations. Protoplasma 218, 144-153.
55. Mitsuhashi W, Crafts-Brandner SJ, Feller U. 1992. Ribulose-1,5-bisphosphate carboxylase/oxygenase degradation in isolated pea chloroplasts incubated in the light or in the dark. Journal of Plant Physiology 139, 653-658.
56. Miyadai K, Mae T, Makino A, Ojima K. 1990. Characteristics of ribulose-1,5-bisphosphate carboxylase/oxygenase degradation by lysates of mechanically isolated chloroplasts from wheat leaves. Plant Physiology 92, 1215-1219.
57. Mulligan RM, Houtz RL, Tolbert NE. 1988. Reaction-intermediate analogue binding by ribulose bisphosphate carboxylase/ oxygenase causes specific changes in proteolytic sensitivity: the amino terminal residue of the large subunit is acetylated proline. Proceedings of the National Academy of Sciences, USA 85, 1513-1517.
58. Nakano R, Ishida H, Makino A, Mae T. 2006. In vivo fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species in an intact leaf of cucumber under chilling-light conditions. Plant and Cell Physiology 47, 270-276.
59. Nakano H, Makino A, Mae T. 1995. Effects of panicle removal on the photosynthetic characteristics of the flag leaf of rice plants during the ripening stage. Plant and Cell Physiology 36, 653-659.
60. Nakano H, Muramatsu S, Makino A, Mae T. 2000. Relationship between the suppression of photosynthesis and starch accumulation in the pod-removed bean. Australian Journal of Plant Physiology 27, 167-173.
61. Navarre DA, Wolpert TJ. 1999. Victorin induction of an apoptotic/senescence-like response in oats. The Plant Cell 11, 237-249.
62. Nooden LD, Guiamet JJ, John I. 1997. Senescence mechanisms. Physiologia Plantarum 101, 746-753.
63. Parrott D, Yang L, Shama L, Fischer AM. 2005. Senescence is accelerated, and several proteases are induced by carbon 'feast' conditions in barley (Hordeum vulgare L.) leaves. Planta 222, 989-1000.
64. Roulin S, Feller U. 1997. Light-induced proteolysis of stromal proteins in pea (Pisum sativum L.) chloroplasts: requirement for intact organelles. Plant Science 128, 31-41.
65. Roulin S, Feller U. 1998a. Light-dependent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: requirement for divalent cations. Planta 205, 297-304.
66. Roulin S, Feller U. 1998b. Dithiothreitol triggers photooxidative stress and fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in intact pea chloroplasts. Plant Physiology and Biochemistry 36, 849-856.
67. Sage RF, Pearcy RW, Seemann JR. 1987. The nitrogen use efficiency of C3 and C4 plants. III. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 85, 355-359.
68. Salvucci ME, Crafts-Brandner SJ. 1995. Purification and properties of a unique nucleotide pyrophosphatase/phosphodiesterase I that accumulates in soybean leaves in response to fruit removal. Plant Physiology 108, 1269-1276.
69. Schaller A, Ryan CA. 1995. Cloning of a tomato cDNA (Gen bank L38581) encoding the proteolytic subunit of a Clp-like energy dependent protease. Plant Physiology 108, 1341.
70. Shanklin J, DeWitt ND, Flanagan JM. 1995. The stroma of higher-plant plastids contain ClpP and ClpC, functional homologs of Escherichia-coli ClpP and ClpA - an archetypal 2-component ATP-dependent protease. The Plant Cell 7, 1713-1722.
71. Spreitzer RJ, Salvucci ME. 2002. Rubisco: structure, regulatory interactions and possibilities for a better enzyme. Annual Review of Plant Biology 53, 449-475.
72. Stieger PA, Feller U. 1997. Requirements for the light-stimulated degradation of stromal proteins in isolated pea (Pisum sativum L.) chloroplasts. Journal of Experimental Botany 48, 1639-1645.
73. Sugiyama T, Mizuno M, Hayashi M. 1984. Partitioning of nitrogen among ribulose-1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and pyruvate orthophosphate dikinase as related to biomass productivity in maize seedlings. Plant Physiology 75, 665-669.
74. Tambussi EA, Bort J, Guiamet JJ, Nogues S, Araus JL. 2007. The photosynthetic role of ears in C-3 cereals: metabolism, water use efficiency and contribution to grain yield. Critical Reviews in Plant Scences 26, 1-16.
75. Tambussi EA, Nogues S, Araus JL. 2005. Ear of durum wheat under water stress: water relations and photosynthetic metabolism. Planta 221, 446-458.
76. Thoenen M, Herrmann B, Feller U. 2007. Senescence in wheat leaves: is a cysteine endopeptidase involved in the degradation of the large subunit of Rubisco? Acta Physiologiae Plantarum 29, 339-350.
77. Thomas H, Ougham H, Canter P, Donnison I. 2002. What staygreen mutants tell us about nitrogen remobilization in leaf senescence. Journal of Experimental Botany 53, 801-808.
78. Tranbarger TJ, Franceschi VR, Hildebrand DF, Grimes HD. 1991. The soybean 94-kilodalton vegetative storage protein is a lipoxygenase that is localized in paraveinal mesophyll cell vacuoles. The Plant Cell 3, 973-987.
79. 2 retrieval in immature barley caryopses. Journal of Experimental Botany 42, 1013-1019.
80. 2 fixation in various photosynthetic organs of wheat and oat. Zeitschrift für Pflanzenphysiologie 82, 78-87.
81. Wittenbach VA. 1982. Effect of pod removal on leaf senescence in soybeans. Plant Physiology 70, 1544-1548.
82. Yoshida T, Minamikawa T. 1996. Successive amino terminal proteolysis of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase by vacuolar enzymes from French bean leaves. European Journal of Biochemistry 238, 317-324.
83. Zhang LF, Rui Q, Zhang P, Wang XY, Xu LL. 2007. A novel 51-kDa fragment of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase formed in the stroma of chloroplasts in dark-induced senescing wheat leaves. Physiologia Plantarum 131, 64-71.
84. Zhang LF, Rui Q, Xu LL. 2006. Degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in wheat leaves. Journal of Integrative Plant Biology 47, 60-66.
85. Zhong P-Y, Tanaka T, Yamauchi D, Minamikawa T. 1997. A 28-kilodalton pod storage protein of French bean plants. Plant Physiology 113, 479-485.