Senescence in wheat leaves: is a cysteine endopeptidase involved in the degradation of the large subunit of Rubisco?

• Autorzy: Thoenen M. , Herrmann B. , Feller U.
• Języki publikacji: EN

Abstrakty

EN

In wheat (Triticum aestivum L.), leaf senescence can be initiated by different factors. Depending on the plant system (intact plants or detached leaves) or the environmental conditions (light, nutrient availability), the symptoms of senescence differ. The aim of this work was to elucidate the catabolism of ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco, EC. 4.1.1.39) under various senescence-inducing conditions. Leaf senescence was initiated in intact plants by darkness or by N-deprivation and in leaf segments by exposure to light or darkness. Depending on the treatment, a 50 kDa fragment of Rubisco was observed. The formation of this fragment was enhanced by leaf detachment and low light. In segments exposed to high light and in intact plants induced to senesce by N-deprivation, the fragment was essentially absent. Since an antibody against the N-terminus of a large subunit of Rubisco (LSU) did not cross-react with the fragment, it appears likely that a smaller fragment was removed from the N-terminus of LSU. Inhibitor studies suggest that a cysteine endopeptidase was involved in the formation of the 50 kDa fragment. Non-denaturing-PAGE followed by SDS-PAGE revealed that the fragment was produced while LSU was integrated in the holoenzyme complex, and that it remained there after being produced. It remains open how the putative endopeptidase reaches the stromal protein Rubisco. The results indicate that depending on the senescence-inducing conditions, different proteolytic enzymes may be involved. The involvement of vacuolar proteases must be considered as occurring during LSU degradation, which takes place in darkness, low light or under carbon limitation.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2007
• Tom: 29
• Numer: 4
• Opis fizyczny: p.339-350,fig.,ref.

Twórcy

autor

Thoenen M.

• Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland

autor

Herrmann B.

• Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland

autor

Feller U.

• Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland

Bibliografia

• Aubert S, Gout E, Bligny R, Marty-Mazars D, Barrieu F, Alabouvette J, Marty F, Douce R (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133:1251–1263
• Becker W, Apel K (1993) Differences in gene expression between natural and artificially induced leaf senescence. Planta 189:74–79
• Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Björkbacka H, Birve SJ, Karlsson J, Gardeström P, Gustafsson P, Lundeberg J, Jansson S (2003) Gene expression in autumn leaves. Plant Physiol 131:430–442
• Bhalla PL, Dalling MJ (1986) Endopeptidase and carboxypeptidase enzymes of vacuoles prepared from mesophyll protoplasts of the primary leaf of wheat seedlings. J Plant Physiol 122:289–302
• Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein dye binding. Anal Biochem 72:248–254
• Brouquisse R, Masclaux C, Feller U, Raymond P (2001) Protein hydrolysis and nitrogen remobilisation in plant life and senescence. In: Lea PJ, Morot-Gaudry J-F (eds) Plant nitrogen. Springer, Berlin, pp 275–293
• 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 Physiol 103:585–591
• Cuello J, Quiles MJ, Sabater B (1984) Role of protein synthesis and light in the regulation of senescence in detached barley leaves. Physiol Plant 60:133–138
• Demirevska-Kepova K, Feller U (2004) Heat sensitivity of Rubisco, Rubisco activase and Rubisco binding protein in higher plants. Acta Physiol Plant 26:103–114
• Demirevska-Kepova K, Hölzer R, Simova-Stoilova L, Feller U (2005) Heat stress effecects on Rubisco, Rubisco binding protein and Rubisco activase in wheat leaves. Biol Plant 49:521–525
• Desimone M, Henke A, Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111:789–796
• Feller U (1983) Senescence and proteolytic activities in detached leaves and detached shoots of wheat. Physiol Veg 21:93–102
• Feller U (2004) Proteolysis. In: Noodén LD (ed) Plant cell death processes. Elsevier/Academic, Amsterdam, pp 107–123
• Feller U, Fischer A (1994) Nitrogen metabolism in senescing leaves. Crit Rev Plant Sci 13:241–273
• 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 Physiol 116:539–546
• Fischer A, Brouquisse R, Raymond P (1998) Influence of senescence and of carbohydrate levels on the pattern of leaf proteases in purple nutsedge (Cyperus rotundus). Physiol Plant 102:385–395
• Gietl C, Schmid M (2001) Ricinosomes: an organelle for developmentally regulated cell death in senescing plant tissues. Naturwissenschaften 88:49–58
• Guiamet JJ, Pichersky E, Noodén LD (1999) Mass exodus from senescing soybean chloroplasts. Plant Cell Physiol 40:986–992
• Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci USA 102:2238–2243
• Gutteridge S, Millard BN, Parry MAJ (1986) Inactivation of ribulose-bisphosphate carboxylase by limited proteolysis. FEBS Lett 196:263–268
• Hensel LL, Grbic V, Baumgarten DA, Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell 5:553–564
• Herrmann B, Feller U (1998) CO₂, light and temperature influence senescence and protein degradation in wheat leaf segments. Physiol Plant 103:320–326
• 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. J Exp Bot 45:1197–1204
• Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937
• Houtz RL, Mulligan RM (1991) Protection of tryptic-sensitive sites in the large subunit of ribulosebisphosphate carboxylase/oxygenase by catalysis. Plant Physiol 96:335–339
• Houtz RL, Stults JT, Mulligan RM, Tolbert NE (1989) Post-translational modifications in the large subunit of ribulose bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 86:1855–1859
• Huffaker RC (1990) Proteolytic activity during senescence of plants. New Phytol 116:199–231
• 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 in the lysates of chloroplasts from primary leaves of wheat. Plant Cell Physiol 38:471–479
• 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
• Ishida H, Makino A, Mae T (1999) Fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase by reactive oxygen species occurs near Gly-329. J Biol Chem 274:5222–5226
• Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
• Lin W, Wittenbach VA (1981) Subcellular localization of proteases in wheat and corn mesophyll protoplasts. Plant Physiol 67:969–972
• Lohmann KN, Gan S, John MC, Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92:322–328
• Makino A, Osmond B (1991) Effects of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 96:355–362
• 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 Environ 29:898–908
• Marquez AJ, Avila C, Forde BG, Wallsgrove RM (1988) Ferredoxin-glutamate synthase from barley leaves: rapid purification and partial characterization. Plant Physiol Biochem 26:645–651
• Mitsuhashi W, Feller U (1992) Effects of light and external solutes on the catabolism of nuclear-encoded stromal proteins in intact chloroplasts isolated from pea leaves. Plant Physiol 100:2100–2105
• Mitsuhashi W, Crafts-Brandner SJ, Feller U (1992) Ribulose-1,5-bis-phosphate carboxylase/oxygenase degradation in isolated pea chloroplasts incubated in the light or in the dark. J Plant Physiol 139:653–658
• 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 Physiol 92:1215–1219
• 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. Proc Natl Acad Sci USA 85:1513–1517
• 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 Cell Physiol 47:270–276
• Navarre DA, Wolpert TJ (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11:237–249
• Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753
• Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Andrew Staehelin L, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844
• Park H, Eggink LL, Roberson RW, Hoober JK (1999) Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (chlorophyta): a pathway for degradation. J Phycol 35:528–538
• Park JH, Oh SA, Kim YH, Woo HR, Nam HG (1998) Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis. Plant Mol Biol 37:445–454
• 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
• Pauncz Y, Gepstein S, Horwitz BA (1992) Photocontrol of the accumulation of plastid polypeptides during greening of tomato cotyledons. Plant Physiol 100:1934–1939
• Roulin S, Feller U (1998a) Light-independent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: requirement for divalent cations. Planta 205:297–304
• 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 Physiol Biochem 36:849–856
• Roulin S, Feller U (2001) Reversible accumulation of (1 → 3,1 → 4)-β-glucan endohydrolase in wheat leaves under sugar depletion. J Exp Bot 52:2323–2332
• Schmid M, Simpson DJ, Sarioglu H, Lottspeich F, Gietl C (2001) The ricinosomes of senescing plant tissue bud from the endoplasmatic reticulum. Proc Natl Acad Sci USA 98:5353–5358
• Smart CM, Hosken SE, Thomas H, Greaves JA, Blair BG, Schuch W (1995) The timing of maize leaf senescence and characterisation of senescence-related cDNAs. Physiol Plant 93:673–682
• Stieger PA, Feller U (1994) Senescence and protein remobilisation in leaves of maturing wheat plants grown on waterlogged soil. Plant Soil 166:173–179
• Strain HH, Cope BT, Svec WA (1971) Analytical procedures for the isolation, identification, estimation and investigation of the chlorophylls. In: San Pietro A (ed) Methods in enzymology, Academic, New York: 452–476
• 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 im maize seedlings. Plant Physiol 75:665–669
• Thayer SS, Huffaker RC (1984) Vacuolar localization of endoproteinases EP1 and EP2 in barley mesophyll cells. Plant Physiol 75:70–73
• Wälti M, Roulin S, Feller U (2002) Effects of pH, light and temperature on (1 → 3,1 → 4)-β-glucanase stability in wheat leaves. Plant Physiol Biochem 40:363–371
• Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469
• 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. Eur J Biochem 238:317–324
• Zhang LF, Rui Q, Xu LL (2006) Degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in wheat leaves. J Integr Plant Biol 47:60–66