Abstract
Four wheat varieties differing in their drought tolerance were subjected to severe but recoverable water stress at seedling stage. Growth parameters, leaf water deficit (WD) and electrolyte leakage (EL) were used to evaluate the stress intensity and the extent of recovery. The physiological response of the varieties was quite similar under severe drought. Leaf protein patterns and levels of some individual proteins relevant to ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) maintenance were studied in control, stressed and recovering plants by electrophoresis and immunoblotting. The bands representing Rubisco large subunit (RLS), N- and C-terminus of RLS, Rubisco activase (RA) and Rubisco binding protein (RBP, cpn 60), as well as the chaperone and proteolytic subunits of the Clp protease complex were identified using polyclonal antibodies. Under drought conditions RLS, Clp proteases and especially RBP were enhanced, whereas the RA band was only slightly affected. The drought tolerant varieties had higher RBP content in the controls and drought treated plants. Its concentration could be a potential marker for drought tolerance.
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Abbreviations
- Clp:
-
ATP dependent calpain protease
- Cpn:
-
Chaperone
- EL:
-
Electrolyte leakage
- FW:
-
Fresh weight
- MW:
-
Molecular weight
- Rubisco:
-
Ribulose-1,5-bisphosphate carboxylase/oxygenase
- RA:
-
Rubisco activase
- RBP:
-
Rubisco binding protein
- RLS:
-
Rubisco large subunit
- RLS-C:
-
C-terminus of RLS
- RLS-N:
-
N-terminus of RLS
- RSS:
-
Rubisco small subunit
- RT:
-
Room temperature
- RuBP:
-
Ribulose-1,5-bisphosphate
- SDS-PAGE:
-
SDS polyacrylamide gel electrophoresis
- WD:
-
Water deficit
References
Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Bray E (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54. doi:10.1016/S1360-1385(97)82562-9
Demirevska-Kepova K, Juperlieva-Mateeva B (1990) Purification of Rubisco large subunit binding protein from barley and preparation of polyclonal antisera against it. Compt Rend Acad Sci Bulg 43:101–104
Demirevska-Kepova K, Simova L (1989) Isolation and purification of ribulose-1, 5-bisphosphate carboxylase/oxygenase from barley leaves. Bulg J Plant Physiol 15:3–10
Demirevska-Kepova K, Simova L, Kjurkchiev S (1999) Barley leaf Rubisco, Rubisco binding protein and Rubisco activase and their protein/protein interactions. Bulg J Plant Physiol 25:31–44
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. Biol Plant 49(4):521–525. doi:10.1007/s10535-005-0045-2
Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot Advance Access Nov 1:1–10
Fisher RA, Maurer R (1978) Drought tolerance in spring wheat cultivars I. Grain yield response. Aust J Agric Res 29:897–912. doi:10.1071/AR9780897
Haupt-Herting S, Klug K, Fock HP (2001) A new approach to measure gross CO2 fluxes in leaves. Gross CO2 assimilation, photorespiration, and mitochondrial respiration in the light in tomato under drought stress. Plant Physiol 126:388–396. doi:10.1104/pp.126.1.388
Hemmingsen SM (1990) The plastid chaperonin. Semin Cell Biol 1:47–54
Holland N, Belking A, Holland D, Pick U, Edelman M (1998) Stress-responsive accumulation of plastid chaperonin 60 during seedling development. Plant J 13:311–316. doi:10.1046/j.1365-313X.1998.00028.x
Houtz RL, Portis AR Jr (2003) The life of ribulose 1,5-bisphosphate carboxylase/oxygenase—Posttranslational facts and mysteries. Arch Biochem Biophys 414:150–158
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 lisates of chloroplasts from primary leaves of wheat. Plant Cell Physiol 38(4):471–479
Jagtap V, Bhargava S, Streb P, Feieraben J (1998) Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) Moench. J Exp Bot 49:1715–1721. doi:10.1093/jexbot/49.327.1715
Kalapos T, van den Boogaard R, Lambers H (1996) Effect of soil drying on growth, biomass allocation and leaf gas exchange of two annual grass species. Plant Soil 185:137–149. doi:10.1007/BF02257570
Law RD, Crafts-Brandner ST (2001) High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/oxygenase activase protein. Arch Biochem Biophys 386:261–267. doi:10.1006/abbi.2000.2225
Lawlor DW (2002) Limitation to photosynthesis in water stressed leaves: stomata vs. metabolism and role of ATP. Ann Bot (Lond) 89:871–885. doi:10.1093/aob/mcf110
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294. doi:10.1046/j.0016-8025.2001.00814.x
Majumdar S, Ghosh S, Glick BR, Dumbroff EB (1991) Activities of chlorophyllase, phosphoenolpiruvate carboxylase and ribulose 1,5-bisphosphate carboxylase in the primary leaves of soybean during senescence and drought. Physiol Plant 81:473–480. doi:10.1111/j.1399-3054.1991.tb05087.x
Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-1,5-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant Cell Physiol 25:429–437
Martinez DE, Bartoli CG, Grbic V, Guiamet JJ (2007) Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. J Exp Bot 58:1099–1107. doi:10.1093/jxb/erl270
Medrano H, Parry MAJ, Socias X, Lawlor DW (1997) Long term water deficit inactivates Rubisco in subtertanean clover. Ann Appl Biol 131:491–501. doi:10.1111/j.1744-7348.1997.tb05176.x
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
Musgrove JE, Jonson RA, Ellis RJ (1987) Dissociation of the ribulose bisphosphate carboxylase large subunit binding protein into dissimilar subunits. Eur J Biochem 163:529–534. doi:10.1111/j.1432-1033.1987.tb10900.x
Nakashima K, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1997) A nuclear gene, erdl, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J 12:851–861. doi:10.1046/j.1365-313X.1997.12040851.x
Neuwald AF, Aravind L, Spouge JL, Koonin EV (2006) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43
Nunes MES, Smith GR (2003) Electrolyte leakage assay capable of quantifying freezing resistance in rose clover. Crop Sci 43:1349–1357
Pääkkönen E, Vahala J, Pohjolai M, Holopainen T, Kärenlampi L (1998) Physiological, stomatatal and ultrastructural ozone responses in birch (Betula pendula Roth.) are modified by water stress. Plant Cell Environ 21:671–684. doi:10.1046/j.1365-3040.1998.00303.x
Pancović D, Sakač Z, Kevrešan S, Plesničar M (1999) Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism. J Exp Bot 50:127–138. doi:10.1093/jexbot/50.330.127
Parrott DL, McInnerney K, Feller U, Fischer AM (2007) Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. New Phytol 176:56–69. doi:10.1111/j.1469-8137.2007.02158.x
Parry MAJ, Andralojc PJ, Khan V, Lea PJ, Keys AJ (2002) Rubisco activity: effect of drought stress. Ann Bot (Lond) 89:833–839. doi:10.1093/aob/mcf103
Pelloux J, Jolivet Y, Fontaine V, Banvoy J, Dizengremel P (2001) Changes in Rubisco and Rubisco activase gene expression and polypeptide content in Pinus halepensis M subjected to ozone and drought. Plant Cell Environ 24:123–131. doi:10.1046/j.1365-3040.2001.00665.x
Portis AR Jr (2003) Rubisco activase—Rubisco’s catalytic chaperone. Photosynth Res 75:11–27. doi:10.1023/A:1022458108678
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202. doi:10.1016/j.jplph.2004.01.013
Riccardi F, Gazeau P, Jacquemot M-P, Vincent D, Zivy M (2004) Deciphering genetic variation of proteome responses to water deficit in maize leaves. Plant Physiol Biochem 42:1003–1011. doi:10.1016/j.plaphy.2004.09.009
Rokka A, Zhang L, Aro EM (2001) Rubisco activase: an enzyme with a temperature-dependent dual function? Plant J 25:463–471. doi:10.1046/j.1365-313x.2001.00981.x
Roy-Macauley H, Zuily-Fodil Y, Kidric M, Pham Thi AT, Viera da Silva J (1992) Effect of drought stress on proteolytic activities in Phaseolus and Vigna leaves from sensitive and resistant plants. Physiol Plant 85:90–96. doi:10.1111/j.1399-3054.1992.tb05268.x
Sakamoto W (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57:599–621. doi:10.1146/annurev.arplant.57.032905.105401
Salekdeh GH, Siopongco J, Wade LJ, Chareyazie B, Bennett J (2002) A proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crops Res 76:199–219. doi:10.1016/S0378-4290(02)00040-0
Salvucci ME, Osteryoung KW, Crafts-Brander SJ, Vierling E (2001) Exceptional sensitivity of rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiol 127:1053–1064. doi:10.1104/pp.127.3.1053
Salvucci ME, Portis AR, Ogren WL (1985) A soluble chloroplast protein catalyses ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res 7:193–201. doi:10.1007/BF00037012
Sanchez de Jimenes E, Medrano L, Martines-Barajas E (1995) Rubisco activase, a possible new number of the molecular chaperone family. Biochemistry 34:2826–2831. doi:10.1021/bi00009a012
Simova-Stoilova L, Vassileva V, Petrova T, Tsenov N, Demirevska K, Feller U (2006) Proteolytic activity in wheat leaves during drought stress and recovery. Gen Appl Plant Physiol Spec Issue 32(1–2):91–100
Zagdanska B, Wishnewski K (1998) ATP-dependent proteolysis contributes to the acclimation-induced drought resistance in spring wheat. Acta Physiol Plant 20:41–48. doi:10.1007/s11738-998-0041-1
Zang X, Komatsu S (2007) A proteomic approach for identifying osmotic-stress-related proteins in rice. Phytochemistry 68:426–437. doi:10.1016/j.phytochem.2006.11.005
Zheng B, Halperin T, Hruskova-Heidingsfeldova O, Adam Z, Clarke AK (2002) Characterization of chloroplast Clp proteins in Arabidopsis: localization, tissue specificity and stress responses. Physiol Plant 114:92–101. doi:10.1034/j.1399-3054.2002.1140113.x
Acknowledgments
This study was supported by grants from the Swiss National Science Foundation, SCOPES (project DILPA) and from the Ministry of Education and Science of Republic Bulgaria (projects CC 1503 and PISA). The authors are grateful to Dr. I. Stancheva for her advices on growing wheat plants in soil conditions and to B. Juperlieva-Mateeva and A. Kostadinova for their excellent technical assistance.
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Demirevska, K., Simova-Stoilova, L., Vassileva, V. et al. Rubisco and some chaperone protein responses to water stress and rewatering at early seedling growth of drought sensitive and tolerant wheat varieties. Plant Growth Regul 56, 97–106 (2008). https://doi.org/10.1007/s10725-008-9288-1
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DOI: https://doi.org/10.1007/s10725-008-9288-1