Heat tolerance and expression of protein synthesis elongation factors, EF-Tu and EF-1α, in spring wheat
Urška Bukovnik A C , Jianming Fu A , Miranda Bennett A , P. V. Vara Prasad A and Zoran Ristic B DA Department of Agronomy, Kansas State University, Manhattan, KS 66506, USA.
B United States Department of Agriculture – Agricultural Research Service, Plant Science and Entomology Research Unit, 4008 Throckmorton Hall, Kansas State University, Manhattan, KS 66506, USA.
C Current address: Department of Biochemistry, Kansas State University, Manhattan, KS 66506, USA.
D Corresponding author. Email: zoran.ristic@ars.usda.gov
Functional Plant Biology 36(3) 234-241 https://doi.org/10.1071/FP08266
Submitted: 17 October 2008 Accepted: 11 December 2008 Published: 2 March 2009
Abstract
Protein elongation factors, EF-Tu and EF-1α, have been implicated in cell response to heat stress. We investigated the expression (accumulation) of EF-Tu and EF-1α in mature plants of spring wheat cultivars Kukri and Excalibur, and tested the hypothesis that cultivars with contrasting tolerance to heat stress differ in the accumulation of these elongation factors under prolonged exposure to high temperature (16 days at 36/30°C). In addition, we investigated the expression of EF-Tu and EF-1α in young plants experiencing a 24-h heat shock (43°C). Excalibur showed better tolerance to heat stress than Kukri. Heat stress induced accumulation of EF-Tu and EF-1α in mature plants of both cultivars, but to a greater extent in Excalibur. Young plants did not show appreciable accumulation of EF-Tu in response to heat shock. However, these plants showed increased accumulation of EF-1α and the accumulation appeared greater in Excalibur than in Kukri. The results support the hypothesis that EF-Tu plays a role in heat tolerance in spring wheat. The results also suggest that EF-1α may be of importance to wheat response to heat stress.
Acknowledgements
The authors are grateful to Dr Juan Juttner, Australian Centre for Plant Functional Genomics, The University of Adelaide, Adelaide, Australia, for generously providing seeds of cultivars of spring wheat. The authors are also thankful to Dr Tom Cheesbrough, South Dakota State University, Brookings, SD, and Dr Benjamin P. DeRidder, Grinnell College, Grinnell, IA for critical reading of the manuscript. This publication is approved as Kansas Agriculture Experiment Station No: 09–093-J. Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the United States Department of Agriculture, and does not imply its approval to the exclusion of other products which may also be suitable.
Al-Khatib K, Paulsen GM
(1990) Photosynthesis and productivity during high-temperature stress of wheat genotypes from major world regions. Crop Science 30, 1127–1132.
Basha E,
Lee GJ,
Demeler B, Vierling E
(2004) Chaperone activity of cytosolic small heat shock proteins from wheat. European Journal of Biochemistry 271, 1426–1436.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Beck BD
(1979) Polymerization of the bacterial elongation factor for protein synthesis, EF-Tu. European Journal of Biochemistry 97, 495–502.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bhadula SK,
Elthon TE,
Habben JE,
Helentjaris TG,
Jiao S, Ristic Z
(2001) Heat-stress induced synthesis of chloroplast protein synthesis elongation factor (EF-Tu) in a heat-tolerant maize line. Planta 212, 359–366.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Blum A
(1986) The effect of heat stress on wheat leaf and ear photosynthesis. Journal of Experimental Botany 37, 111–118.
| Crossref | GoogleScholarGoogle Scholar |
Blumenthal T,
Landers TA, Weber K
(1972) Bacteriophage Qβ replicase contains the protein biosynthesis elongation factors EF-Tu and EF-Ts. Proceedings of the National Academy of Sciences of the United States of America 69, 1313–1317.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Boyer JS
(1982) Plant productivity and the environment. Science 218, 443–448.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Buckley BA,
Gracey AY, Somero GN
(2006) The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. Journal of Experimental Biology 209, 2660–2677.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bunai F,
Ando K,
Ueno H, Numata O
(2006)
Tetrahymena eukaryotic translation elongation factor 1A (eEF1A) bundles filamentous actin through dimmer formation. Journal of Biochemistry 140, 393–399.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Caldas TD,
Yaagoubi AE, Richarme G
(1998) Chaperone properties of bacterial elongation factor. Journal of Biological Chemistry 273, 11478–11482.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Caldas TD,
Laalami S, Richarme G
(2000) Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. Journal of Biological Chemistry 275, 855–860.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Feder ME, Hofmann GE
(1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243–282.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fu J,
Momčilović I,
Clemente TE,
Nersesian N,
Trick HN, Ristic Z
(2008) Heterologous expression of a plastid EF-Tu reduces protein thermal aggregation and enhances CO2 fixation in wheat (Triticum aestivum) following heat stress. Plant Molecular Biology 68, 277–288.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gallardo K,
Job C,
Groot SPS,
Puype M,
Demol H,
Vandekerckhove J, Job D
(2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiology 126, 835–848.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gallie DR,
Le H,
Caldwell C,
Tanguay RL,
Hoang NX, Browning KS
(1997) The phosphorylation state of translation initiation factors is regulated developmentally and following heat shock in wheat. Journal of Biological Chemistry 272, 1046–1053.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gallie DR,
Le H,
Caldwell C, Browning KS
(1998) Analysis of translation elongation factors from wheat during development and following heat shock. Biochemical and Biophysical Research Communications 245, 295–300.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hendrick JP, Hartl FU
(1993) Molecular chaperone functions of heat shock proteins. Annual Review of Biochemistry 62, 349–384.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hotokezaka Y,
Többen U,
Hotokezaka H,
van Leyen K,
Beatrix B,
Smith DH,
Nakamura T, Wiedmann M
(2002) Interaction of the eukaryotic elongation factor 1A with newly synthesized polypeptides. Journal of Biological Chemistry 277, 18545–18551.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Izanloo A,
Condon AG,
Langridge P,
Tester M, Schnurbusch T
(2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. Journal of Experimental Botany 59, 3327–3346.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kobza J, Edwards GE
(1987) Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiology 83, 69–74.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Krause GH, Weis E
(1984) Chlorophyll fluorescence as a tool in plant physiology: II. interpretation of fluorescence signals. Photosynthesis Research 5, 139–157.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Large EC
(1954) Growth stages in cereals. Plant Pathology 3, 128–129.
| Crossref | GoogleScholarGoogle Scholar |
Lee GJ, Vierling E
(2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiology 122, 189–197.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li ZY, Chen SY
(1999) Inducible expression of translation elongation factor 1A gene in rice seedlings in response to environmental stresses. Acta Botanica Sinica 41, 800–806.
|
CAS |
Lobell DB, Asner GP
(2003) Climate and management contributions to recent trends in U.S. agricultural yields. Science 299, 1032.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Malki A,
Caldas TD,
Parmeggiani A,
Kohiyama M, Richarme G
(2002) Specificity of elongation factor EF-Tu for hydrophobic peptides. Biochemical and Biophysical Research Communications 296, 749–754.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Momcilovic I, Ristic Z
(2004) Localization and abundance of chloroplast protein synthesis elongation factor (EF-Tu) and heat stability of chloroplast stromal proteins in maize. Plant Science 166, 81–88.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Momcilovic I, Ristic Z
(2007) Expression of chloroplast protein synthesis elongation factor, EF-Tu, in two lines of maize with contrasting tolerance to heat stress during early stages of plant development. Journal of Plant Physiology 164, 90–99.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nissen P,
Kjeldgaard M,
Thirup S,
Polekhina G,
Reshetnikova L,
Clark BFC, Nyborg J
(1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270, 1464–1472.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Prasad PVV,
Pisipati SR,
Ristic Z,
Bukovnik U, Fritz AK
(2008) Impact of nighttime temperature on physiology and growth of spring wheat. Crop Science 48, 2372–2380.
| Crossref |
Rao D,
Momcilovic I,
Kobayashi S,
Callegari E, Ristic Z
(2004) Chaperone activity of recombinant maize chloroplast protein synthesis elongation factor, EF-Tu. European Journal of Biochemistry 271, 3684–3692.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Reddy P,
Miller D, Peterkofsky A
(1986) Simulation of Escherichia coli adenylate cyclase activity by elongation factor Tu, a GTP-binding protein essential for protein synthesis. Journal of Biological Chemistry 261, 11448–11451.
|
CAS |
PubMed |
Reynolds MP,
Singh RP,
Ibrahim A,
Ageeb OAA,
Larque-Saavedra A, Quick JS
(1998) Evaluating physiological traits to complement empirical selection for wheat in warm environments. Euphytica 100, 85–94.
| Crossref | GoogleScholarGoogle Scholar |
Richarme G
(1998) Protein-disulfide isomerase activity of elongation factor EF-Tu. Biochemical and Biophysical Research Communications 252, 156–161.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Riis B,
Rattan SIS,
Clark BFC, Merrick WC
(1990) Eukaryotic protein elongation factors. Trends in Biochemical Sciences 15, 420–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ristic Z,
Wilson K,
Nelsen C,
Momcilovic I,
Kobayashi S,
Meeley R,
Muszynski M, Habben J
(2004) A maize mutant with decreased capacity to accumulate chloroplast protein synthesis elongation factor (EF-Tu) displays reduced tolerance to heat stress. Plant Science 167, 1367–1374.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ristic Z,
Momčilović I,
Fu J,
Callegari E, DeRidder BP
(2007a) Chloroplast protein synthesis elongation factor, EF-Tu, reduces thermal aggregation of rubisco activase. Journal of Plant Physiology 164, 1564–1571.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ristic Z,
Bukovnik U, Prasad PVV
(2007b) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Science 47, 2067–2073.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ristic Z,
Bukovnik U,
Momčilović I,
Fu J, Prasad PVV
(2008a) Heat-induced accumulation of chloroplast protein synthesis elongation factor, EF-Tu, in winter wheat. Journal of Plant Physiology 165, 192–202.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ristic Z,
Bukovnik U,
Prasad PVV, West M
(2008b) A model for prediction of heat stability of photosynthetic membranes. Crop Science 48, 1513–1522.
| Crossref | GoogleScholarGoogle Scholar |
Santarius KA
(1974) Seasonal changes in plant membrane stability as evidenced by the heat sensitivity of chloroplast membrane reactions. Zeitschrift fuer Pflanzenphysiologie 73, 448–451.
Schreiber U, Berry JA
(1977) Heat-induced changes of chloroplast fluorescence in intact leaves correlated with damage to photosynthetic apparatus. Planta 136, 233–238.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Shamovsky I,
Ivannikov M,
Kandel ES,
Gershon D, Nudler E
(2006) RNA-mediated response to heat shock in mammalian cells. Nature 440, 556–560.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Stone PJ, Nicolas ME
(1995) A survey of the effects of high temperature during grain filling on yield and quality of 75 wheat cultivars. Australian Journal of Agricultural Research 46, 475–492.
| Crossref | GoogleScholarGoogle Scholar |
Sutton F, Kenefick DG
(1994) Nucleotide sequence of a cDNA encoding an elongation factor (EF-1α) from barley primary leaf. Plant Physiology 104, 807.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Suzuki H,
Ueda T,
Taguchi H, Takeuchi N
(2007) Chaperone properties of mammalian mitochondrial translation elongation factor Tu. Journal of Biological Chemistry 282, 4076–4084.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Vierling E
(1991) The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 42, 579–620.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Wahid A,
Gelani S,
Ashraf M, Foolad MR
(2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
| Crossref | GoogleScholarGoogle Scholar |
Wardlaw IF,
Sofield I, Cartwright PM
(1980) Factors limiting the rate of dry matter accumulation in the grain of wheat grown at high temperature. Australian Journal of Plant Physiology 7, 387–400.
| Crossref | GoogleScholarGoogle Scholar |
Young CC, Bernlohr RW
(1991) Elongation factor Tu is methylated in response to nutrient deprivation in Escherichia coli. Journal of Bacteriology 173, 3096–3100.
|
CAS |
PubMed |