Advertisement

Acta Physiologiae Plantarum

, 31:1129 | Cite as

Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit

  • Klimentina DemirevskaEmail author
  • Diana Zasheva
  • Rumen Dimitrov
  • Lyudmila Simova-Stoilova
  • Maria Stamenova
  • Urs Feller
Original Paper

Abstract

The leaf protein pattern from drought-tolerant and drought-sensitive wheat varieties subjected to severe soil drought but with the possibility for recover from stress was studied by two-dimensional polyacrylamide gel electrophoresis (2D-PAGE). The spots representing Rubisco large subunit (RLS) were identified using polyclonal antibodies against Rubisco and immunoblotting. Some qualitative and quantitative differences in the 2D-PAGE protein map of wheat varieties were revealed under drought conditions. Three days recovery of wheat plants were not enough for restoring RLS quantity to the level of controls after 7 days drought, especially in the drought-sensitive variety Miziya. There are contradictory data in the literature concerning increased or diminished RLS level in drought stressed plants. A comparison of RLS after SDS-PAGE and 2D-PAGE was made. The revealed protein pattern depended on the presence or absence of protease inhibitors in the extraction buffer, on the procedure of extraction, and on the degree of stress.

Keywords

2D-PAGE Drought stress Triticum aestivum L. Rubisco LS SDS-PAGE 

Abbreviations

BSA

Bovine serum albumin

2D-PAGE

2-Dimensional polyacrylamide gel electrophoresis

DTT

1,4-Dithio-dl-threitol

DW

Dry weight

EDTA

Ethylenediaminetetraacetic acid

EL

Electrolyte leakage

FW

Fresh weight

IEF

Isoelectric focusing

2-ME

β-Mercapthoethanol

MM

Molecular mass

PMSF

Phenylmethanesulfonyl fluoride

Rubisco

Ribulose-1,5-bisphosphate carboxylase/oxygenase

RLS

Rubisco large subunit

RSS

Rubisco small subunit

SDS-PAGE

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

SL

Shoot length

TCA

Trichloracetic acid

TW

Turgor weight

WD

Water deficit

Notes

Acknowledgments

This study was supported by grants from Swiss National Science Foundation, SCOPES (project DILPA) and from Ministry of Education and Science of Republic Bulgaria (project CC 1503). The authors are grateful to Dr I. Stancheva for her advices in growing wheat plants in soil and to B. Juperlieva-Mateeva and A. Kostadinova for their excellent technical assistance.

References

  1. Anderson B, Aro E-M (1997) Proteolytic activities and proteases of plant chloroplasts. Physiol Plant 100:780–793. doi: 10.1111/j.1399-3054.1997.tb00005.x CrossRefGoogle Scholar
  2. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24(1):23–58. doi: 10.1080/07352680590910410 CrossRefGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osorio ML, Carvalho I, Faria T, Pineiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot (Lond) 89:907–916. doi: 10.1093/aob/mcf105 CrossRefGoogle Scholar
  5. 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 Cell Physiol 44:914–921. doi: 10.1093/pcp/pcg118 CrossRefPubMedGoogle Scholar
  6. Cohen I, Knopf JA, Irihimaitch V, Shapira M (2005) A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and subunit expression. Plant Physiol 137:738–746. doi: 10.1104/pp.104.056341 CrossRefPubMedGoogle Scholar
  7. Cohen I, Sapir Y, Shapira M (2006) A conserved mechanism controls translation of Rubisco large subunit in different photosynthetic organisms. Plant Physiol 141:1089–1097. doi: 10.1104/pp.106.079046 CrossRefPubMedGoogle Scholar
  8. Damerval C, De Vienne D, Zivy M, Thiellement H (2005) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7(1):52–54. doi: 10.1002/elps.1150070108 CrossRefGoogle Scholar
  9. Demirevska K, Simova L, Vassileva V, Feller U (2008) 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. doi: 10.1007/s10725-008-9288-1 CrossRefGoogle Scholar
  10. Demirevska-Kepova K, Simova L (1989) Isolation and purification of ribulose-1,5-bisphosphate carboxylase/oxygenase from barley leaves. Bulg J Plant Physiol 15:3–10Google Scholar
  11. 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(3–4):31–44Google Scholar
  12. Desimone M, Henke A, Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111:789–796PubMedGoogle Scholar
  13. Ellis RJ (1979) The most abundant protein in the world. Trends Biochem Sci 4:241–244. doi: 10.1016/0968-0004(79)90212-3 CrossRefGoogle Scholar
  14. Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624. doi: 10.1093/jxb/erm242 CrossRefPubMedGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. Granier F (1988) Extraction of plant proteins for two-dimensional electrophoresis. Electrophoresis 9:712–718. doi: 10.1002/elps.1150091106 CrossRefPubMedGoogle Scholar
  17. 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. doi: 10.1016/S0003-9861(03)00122-X PubMedGoogle Scholar
  18. Inmaculada J, Navarro RM, Lenz C, Ariza D, Jorrin J (2006) Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress. Proteomics 6:S207–S214. doi: 10.1002/pmic.200500364 CrossRefGoogle Scholar
  19. 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(4):471–479PubMedGoogle Scholar
  20. Islam N, Lonsdale M, Upadhyaya NM, Higgins TJ, Hirano H, Akhurst R (2004) Protein extraction from mature rice leaves for two-dimensional gel electrophoresis and its application in proteome analysis. Proteomics 4:1903–1908. doi: 10.1002/pmic.200300816 CrossRefPubMedGoogle Scholar
  21. Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11(1):100–105Google Scholar
  22. 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 CrossRefGoogle Scholar
  23. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the heat of bacteriophage T4. Nature 227:680–685. doi: 10.1038/227680a0 CrossRefPubMedGoogle Scholar
  24. 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. doi: 10.1104/pp.100.4.2100 CrossRefPubMedGoogle Scholar
  25. Pääkkönen E, Vahala J, Pohjolai M, Holopainen T, Kärenlampi L (1998) Physiological, stomatal 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 CrossRefGoogle Scholar
  26. Pell EJ, Eckardt NA, Glick RE (1993) Biochemical and molecular basis for impairment of photosynthetic potential. Photosynth Res 39:453–462. doi: 10.1007/BF00014598 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Benett J (2002a) Proteomic analysis of rice leaves during drought stress and recovery. Proteomics 2:1131–1145. doi: 10.1002/1615-9861(200209)2:9<1131::AID-PROT1131>3.0.CO;2-1 CrossRefPubMedGoogle Scholar
  31. Salekdeh Gh H, Siopongco J, Wade LJ, Ghareyazie B, Benett J (2002b) 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 CrossRefGoogle Scholar
  32. 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 9:1–101Google Scholar
  33. Thiellement H, Bahrman N, Damerval C, Plomion C, Rossignol M, Santoni V, de Vienne D, Zivy M (1999) Proteomics for genetic and physiological studies in plants. Electrophoresis 20:2013–2026. doi: 10.1002/(SICI)1522-2683(19990701)20:10<2013::AID-ELPS2013>3.0.CO;2-# CrossRefPubMedGoogle Scholar
  34. Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresti M (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24:2369–2375. doi: 10.1002/elps.200305500 CrossRefPubMedGoogle Scholar
  35. Wostrikoff K, Stern D (2007) Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts. Proc Natl Acad Sci USA 104:6466–6471. doi: 10.1073/pnas.0610586104 CrossRefPubMedGoogle Scholar
  36. Yoshida T, Minamikawa T (1996) Successive amino-terminal proteolysis of large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase by vacuolar enzymes from French leaves. Eur J Biochem 238:317–324. doi: 10.1111/j.1432-1033.1996.0317z.x CrossRefPubMedGoogle Scholar
  37. 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 CrossRefPubMedGoogle Scholar
  38. Zhao C, Wang J, Cao M, Zhao K, Shao J, Lei T, Yin J, Hill GG, Xu N, Liu S (2005) Proteomic changes in rice leaves during development of field-growth rice plants. Proteomics 5:961–972. doi: 10.1002/pmic.200401131 CrossRefPubMedGoogle Scholar
  39. Zorb C, Schmitt S, Neeb A, Karl S, Linder M, Schubert S (2004) The biochemical reaction of maize (Zea mays L.) to salt stress is characterized by a mitigation of symptoms and not by a specific adaptation. Plant Sci 167(1):91–100. doi: 10.1016/j.plantsci.2004.03.004 CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2009

Authors and Affiliations

  • Klimentina Demirevska
    • 1
    Email author
  • Diana Zasheva
    • 2
  • Rumen Dimitrov
    • 2
  • Lyudmila Simova-Stoilova
    • 1
  • Maria Stamenova
    • 2
  • Urs Feller
    • 3
  1. 1.Institute of Plant PhysiologyBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Institute of Biology and Immunology of ReproductionBulgarian Academy of SciencesSofiaBulgaria
  3. 3.Institute of Plant SciencesUniversity of Bern3013Switzerland

Personalised recommendations