Skip to main content
SpringerLink
Log in

Rubisco and some chaperone protein responses to water stress and rewatering at early seedling growth of drought sensitive and tolerant wheat varieties

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

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

    Article  PubMed  CAS  Google Scholar 

  • Bray E (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54. doi:10.1016/S1360-1385(97)82562-9

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hemmingsen SM (1990) The plastid chaperonin. Semin Cell Biol 1:47–54

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Nunes MES, Smith GR (2003) Electrolyte leakage assay capable of quantifying freezing resistance in rose clover. Crop Sci 43:1349–1357

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Portis AR Jr (2003) Rubisco activase—Rubisco’s catalytic chaperone. Photosynth Res 75:11–27. doi:10.1023/A:1022458108678

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sakamoto W (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57:599–621. doi:10.1146/annurev.arplant.57.032905.105401

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Institute of Plant Physiology, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bdg. 21, Sofia, 1113, Bulgaria

    Klimentina Demirevska, Lyudmila Simova-Stoilova & Valya Vassileva

  2. Institute of Plant Sciences, University of Bern, 3013, Bern, Switzerland

    Urs Feller

Authors
  1. Klimentina Demirevska
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lyudmila Simova-Stoilova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valya Vassileva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Urs Feller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klimentina Demirevska.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-008-9288-1

Keywords

Search

Navigation