Drought - inducible genes and differentially expressed sequence tags associated with components of drought tolerance in durum wheat
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Date
2008
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Volume Title
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Article
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Scientific Research and Essay
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Scientific Research and Essay;Vol. 3 (1), pp. 009-026, January 2008
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Abstract
Drought stress is one of the most important environmental factors reducing cereal yields. The genetic
and physiological bases of drought tolerance in durum wheat was investigated by QTL mapping and by
mapping candidate genes derived from differentially expressed genes and previous investigations. A
recombinant inbred population derived from a cross between two durum (Triticum turgidum L. var
durum) parents Jennah Khetifa and Cham1 that exhibit contrasting traits for drought tolerance was
employed. Twelve known genes and 103 differentially expressed sequence tags (dESTs) were surveyed
and 55 detected polymorphism between the two parental lines. In total, 162 loci including 6 known
genes, 37 dESTs, and an additional 119 markers that were unlinked in the previous map have been
merged with 306 previously mapped markers to produce a new map with 468 loci. Single point analysis
and composite interval mapping were used to identify the genomic regions controlling traits related to
drought stress. Significant QTL were identified for canopy temperature, photosynthesis-related parameters and water status index. One hundred and seventy eight markers, including 6 candidate genes
and 19 differentially expressed sequences were associated with QTL for drought tolerance traits. The
results indicate that there is considerable potential for improving drought tolerance of durum wheat by
using marker-assisted selection
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Keywords
Durum wheat, drought tolerance, QTL analysis, genetic linkage mapping, ESTs, RFLP
Citation
Acevedo E (1993). Potential for carbon isotope discrimination as a selection criterion in barley breeding. In: Ehleringer JR, Hall AE, Farquhar GD (eds) stable isotope and plant carbon-water realtions. Academic Press, New York. pp 399-417. Allen RD (1997). Use of transgenic plants to study antioxidant defenses. Free Radic. Biol. Med. 23: 473-479. Anderberg RJ, Walker-Simmons MK (1992). Isolation of a wheat cDNA clone for an abscisic acid-inducible transcript with homology to protein kinases Proc. Natl. Acad. Sci. U.S.A. 89 (21), 10183-10187. Aon MA, Cortassa S, Gomez Casati DF, Iglesias AA (1999). Effects of stress on cellular infrastructure and metabolic organization in plant cells. Int Rev Cytol. 194:239–273 Araus JL, Amaro T, Zuhair Y, Nachit MM (1997). Effect of leaf structure and water status on carbon isotope discrimination in fieldgrown durum wheat. Plant Cell Environ. 20:1484-1494. Araus JL, Reynolds MP, Acevedo E (1993). Leaf posture, grain yield, growth, leaf structure and carbon isotope discrimination in wheat. Crop Sci. 33: 1273-1279. Barrs HD, Weatherley PE (1968). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust. J. Biol. Sci. 15: 413-428. Belkhodja R, Morales-Fermin, Abadia-Anunciacion, Gomez-Aparisi J, Abadia-Javier (1994). hlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiol. 104: 667-673. Bell E, Mullet JE (1991). Lipoxygenase gene expression is modulated in plants by water deficit, wonding, and methyl jasmonate. Mol. Gen. Genet. 230: 456-462. Bieleski RL (1993). Fructan hydrolysis drives peta1 expansion in the ephemeral daylily flower. Plant Physiol. 103:213-219. Blanco A, Bellomo P, Cenci A, De Giovanni C, D’Ovidio R, Iacono E, Laddomada B, Pagnotta MA, Porceddu E, Sciancalepore A, Simeone R, Tanzarella OA (1998). A genetic linkage map of durum wheat. Theo Appl Genet 97:721-728. Blum A, Munns R, Passioura JB, Turner NC (1996). Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations. Plant. Physiol. 110: 1051-1053. Bond J S, Butler PE (1987). Intracellular proteases. Annu. Rev. Biochem. 56: 333-364. Bruxelles GL, Peacock WJ, Dennis ES, Dolferus R (1996). Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiol. 111: 381-391. Capell T, Escobar C, Liu H, Burtin D, Lepri O, Christou P (1998). Overexpression of the oat arginine decarboxylase cDNA in transgenic rice Oryza sati6a L.) affects normal development patterns in vitro and results in putrescine accumulation in transgenic plants. Theor. Appl. Genet. 97: 246-254. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D (1997). Actin depolymerizing factor ADF/cofilin enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol. 136: 1307-1323. Ceccarelli S, Grando S (1996). Drought as a challenge for the plant breeder. Plant growth regulation. 20: 149-155. Cejudo FJ, Murphy G, Chinoy C, Baulcombe DC (1992). A gibberellinregulated gene from wheat with sequence homology to cathepsin B of mammalian cells. Plant J. 2: 937-948. Chazen O, Neumann PM (1994). Hydraulic signals from the roots and rapid cell-wall hardening in growing maiz (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits. Plant physiol. 104: 1385-1392. Condon AG, Farquhar GD, Richards RA (1990). Genotypic variation incarbon isotope discrimination and transpiration efficiency in wheat. Leaf gas exchange and whole plant studies. Aust. J. Plant Physiol. 17: 9-22. Conley TR, Peng HP, Shih MC (1999). Mutations affecting induction of glycolytic and fermentative genes during germination and environmental stresses in Arabidopsis. Plant Physiol. 119: 599-608. Cornic G, Massacci A (1996). In Advances in Photosynthesis, V.5, Photosynthesis and the Environment (Neil R. Baker, ed), pp. 347- 366. Kluwer Academic Publishers, Dordrecht/Boston/London Datta SK (2002). Recent development in transgenic for abioltic stress tolerance in rice. JIRCAS working report. PP. 43-53. De Vetten NC, Lu G, Ferl RJ (1992). A maize protein associated with the G-box binding complex has homology to brain regulatory proteins. Plant Cell. 4: 1295-1307. De Vienne D, Leonardi A, Damerval C, Zivy M (1999). Genetics of proteome variation for QTL characterization: application to droughtstress responses in maize. J. Exp. Bot. 50: 303-309. Dolferus R, Ellis M, De Bruxelles GL, Frevaskis B, Hoeren F, Dennis ES, Peacock WJ (1997). Strategies of gene action in Arabidopsis during hypoxia. Ann. Bot. 97: 21-31. Drew MC (1997). Oxygen deficiency and root metabolism: Injury and acclimation under hyboxia and anoxia. Annu. Rev. Plant Physiol. Plant Biol. 48: 223-250. Dumas B, Sailland A, Cheviet JP, Freyssinet GP (1993). Identification of barley oxalate oxidase as a germin-like CR Acad Sci Paris. 316: 793– 798. Edelman J, Jefford TG (1968). The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol. 67:517-531. Ernez M, Lannoye R (1991). Quantification of physiological disorders in stressed plants. in Physiology-Breeding of Winter cereals for stressed Mediterranean environments. INRA ed., Paris. PP. 369-390. Espinosa-Ruiz A, Belles JM, Serrano R, Culianez-Macia FA (1999). Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth. Plant J. 20: 529-539. Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000). Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol. 122: 657-665. Ezaki T, Kawamura Y, Li N, Li ZY, Zhao L, Shu S (2001). Proposal of the genera Anaerococcus gen. nov., Peptoniphilus gen. nov. and Gallicola gen. nov. for members of the genus Peptostreptococcus. Int. J. Syst. Evol. Microbiol. 51:1521-1528. Falk S, Maxwell DP, Laudenbach DE, Huner NPA (1996). In Advances in Photosynthesis, V.5, Photosynthesis and the Environment (Neil R. Baker, ed), pp. 367-385. Kluwer Academic Publishers, Dordrecht/Boston/London. Farquhar GD, Ehleringer JR, Hubick KT (1989). Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 503–537. Farquhar GD, Richards RA (1984). Isotopic composition of plant carbon correlates with water-use-efficiency of wheat genotypes. Aust. J. Plant Physiol. 11: 539–552. Firn RD, Friend J (1972). Enzymatic production of the plant growth inhibito, Xanthoxin. Planta 103: 263-266. Fuks B, Schnell DJ (1997). Mechanism of protein transport across the chloroplast envelop. Plant Physiol. 114: 405-410. Gahrtz M, Stolz J, Sauer N (1994). A phloem-specific sucrose-H1 symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J. 6: 697–706. Giuliano G, Hoffman N, Ko K, Scolnik PA, Cashmore AR (1988). A lightentrained circadian clock controls transcription of several plant genes. EMBO J. 7: 3635–3642. Guerrero FD, Jones JT, Mullet JE (1990). Turgor-responsive gene transcription and RNA levels increase rapisly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol. Biol. 15:11-26. Haldane JBS (1919). The combination of linkage values, and the calculation of distance between linkage factors. J. Genet. 8: 299-309. Halliwell B, Gutteridge JMC (1984). Free Radicals in Biology and Medicine 2 nd edn. Clarendon Press, Oxford. Havaux M, Ernez M, Lannoye R (1988). Correlation between heat tolerance and drought tolerance in cerealsdemonstrated by rapid chlorophyll fluorescence tests. J. Plant Physiol. 133: 555-560. Heitz T, Bergey DR, Ryan CA (1997). A gene encoding a chloroplasttargeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiol. 114: 1085- 1093. Hendry GAF (1993). Evolutionary origins and natural functions of fructans: A climatological, biogeographic and mechanistic appraisal. New Phytol. 123: 3-14. Hirose T, Imaizumi N, Scofield GN, Furbank RT, Ohsugi R (1997). cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol. 38:1389- 1396. Hurkman, W.J., Lane, B.G. and Tanaka, C.K. 1994. Nucleotide sequence of a transcript encoding a germin-like protein that is present in salt-stressed barley (Hordeum vulgare L.) roots. Plant Physiol 104:803–804 Hurkman WJ, Tao HP, Tanaka CK (1991). Germin-like polypeptides increase in barley roots during salt stress. Plant Physiol. 97: 366– 374. Im YJ, Han O, Chung GC, Cho BH (2001). Antisense expression of an arabidopsis ω-3 fatty acid desaturase gene reduces salt/drought tolerance in transgenic tobacco plants. Molecules and cells. 13: 261- 271. Ingram J, Bartels D (1996). The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. 47: 377–403. Jarillo JA, Leyva A, Salinas J, Martinez-Zapater JM (1993). Low temperature induces the accumulation of alcohol dehydrogenase mRNA in Arabidopsis thaliana, a chilling-tolerant plant. Plant Physiol. 101: 833-837. Kampfenekel KM, Van Montagu M, Inzé D (1995). Effect of iron excess on Nicotiana plumbaginifolia plants. Implications to oxidative stress. Plant Physiol. 107, 725–735. Kato-Noguchi H (1999). Flooding induced increases in alcohol gehydrogenase activity in timothy and ryegrass seedlings. Biol. Plant. 42: 445-449. Kato-Noguchi H (2000). Osmotic stress increases alcohol dehydrogenase activity in maize seedlings. Biol. Plant. 43: 621-624. Kennedy RA, Rumpho ME, Fox TC (1992). Anaerobic metabolism in plants. Plant Physiol. 100:1-6. Koizumi M, Yamaguchi-Shinozaki K, Tsuii H, Shinozaki K (1993). Structure and expression of two genes that encode distinct droughtinducible cysteine proteinases in Arabidopsis thaliana. Gene. 129:175-182. Koroleva OA, Tomos AD, Farrar JF, Gallagher J, Pollock CJ (2001). Carbon allocation and sugar status in individual cells of barley leaves affects expression of sucrose-fructan 6-fructosyltransferase gene. Ann. Appl. Biol. 138:27–32. Koroleva OA, Tomos AD, Farrar JF, Roberts P, Pollock CJ (2000). Tissue distribution of primary metabolism between epidermal, mesophyll and parenchymatous bundle cells in barley leaves. Aust. J. Plant Physiol. 27: 747–755. Kuhn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997). Macromolecular trafficking indicated by localization and turnover of sucrose transporters in enucleate sieve elements. Science 275: 1298–1300. Lane BG (1994). Oxalate, germin, and the extracellular matrix of higher plants. FASEB J. 8: 294–301. Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993). Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol. Chem. 268:12239–12242. Lappalainen P, Fedorov EV, Fedorov AA, Almo SC, Drubin DG (1997). Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J. 16: 5520–5530. Lappaleinen P, Kessels MM, Cope MJTV, Drubin D (1998). The ADF homology (ADF-H) domain: a highly exploited actin-binding module. Mol. Biol. Cell. 9:1951–1959. Leopold AC (1990). Coping with desiccation. In: Alscher RG and Cumming JR. Stress responses in plants: Adaptation and Acclimation Mechanisms. Wily-Liss, New York. pp. 37-56. Leung H (2001). Genetic resources conservation, evaluation, and gene discovery. IRRI, project summary and highlights, pp. 13-16.Lewis DH (1993). Nomenclature and diagrammatic representation of oligomeric fructans. New Phytologist. 124: 583-593. Lidgett AJ, Moran M, Wong KAL, Furze J, Rhodes MJC, Hamill JD (1995). Isolation and expression pattern of a cDNA encoding a cathepsin B-like protease from Nicotiana rustica. Plant Mol. Biol. 29: 379-384. Lu C, Koroleva OA, Farrar JF, Gallagher J, Pollock CJ, Deri TA (2002). Rubisco Small Subunit, Chlorophyll a/b-Binding Protein and Sucrose: Fructan-6-Fructosyl Transferase Gene Expression and Sugar Status in Single Barley Leaf Cells in Situ. Cell Type Specificity and Induction by Light. Plant Physiol. 130:1335–1348. Ludlow MM, Chun ACP, Clements RT, Kerslake RG (1983). Adaptation of speccies of Centrosema to water stress. Aust. J. Plant Physiol. 10:119-130. Manly KF, Cudmore Jr RH (1997). Map Manager QT, Software for mapping quantitative trait loci. Abstracts of the 11th International Mouse Genome Conference, St. Petersburg, FL. Matsukura C, Saitoh T, Hirose T, Perata ROP, Yamaguchi J (2000). Sugar Uptake and Transport in Rice Embryo. Expression of Companion Cell-Specific Sucrose Transporter (OsSUT1) Induced by Sugar and Light. Plant Physiol. 124: 85-93. McGough A, Chiu W (1999). ADF/cofilin weakens lateral contacts in the actin filament. J. Mol. Biol. 291: 513–519. Merah O, Monneveux P, Dele´ens E (2001). Relationships between flag leaf carbon isotope discrimination and several morpho-physiological traits in durum wheat genotypes under Mediterranean conditions. Environ. Exp. Bot. 45: 63–71. Nachit MM (1983). Use of planting dates to select stress tolerance and yield stable genotypes for the rainfed Mediterranean environment. Rachis. 3:15-17. Nachit MM, Elouafi I, Pagnotta MA, El saleh A, Iacono E, Labhilili M, Asbati A, Azrak M, Hazzam H, Benscher D, Khairalla M, Ribaut JM, Tanzarella OA, Porceddu E, Sorrells ME (2001). Molecular linkage map for an interspecific recombinant inbred population of durum wheat (Triticum turgidum L. Var. Durum). Theo Appl. Genet. 102:177- 186. Nachit MM, Ketata H (1986). Breeding strategy for improving durum wheat in Mediterranean rainfed areas. International Wheat Conference, Rabat, Morocco, May. pp. 2-5. Nachit MM, Ketata H (1991). Selection of morpho-physiological traits for multiple abiotic stresses resistance in durum wheat (Triticum turgidum L. var. Durum). In: Physiology-Breeding of Winter Cereals for Stressed Mediterranean Environments, (E. Acevedo, A.P. Conesa, Ph. Monneveux, J.P. Srivastava, Eds.). pp 391-400. Les Colloques 55, INRA, Paris. Nachit MM, Monneveux P, Araus JL, Sorrells, ME (2000). Relationship of dryland productivity and drought tolerance with some molecular markers for possible MAS in durum wheat (Triticum turgidum L. var. durum). Durum whaet improvement in the Mediterranean region: New challenges. pp. 203-206. Nagai J, Bloch K (1968). Enzymatic desaturation of stearyl acyl carrier protein. J. Biol. Chem. 243: 4626–4633. O’Tool JC (1989). Breeding for drought resistance in cereals: emerging new technologies. In: Baker FWG, ed. Drought resistance in cerials. Wallingford, UK: CAB international. pp. 81-94. Ouellet FO, Carpentier E, Cope MJTV, Monroy AF Sarhan F (2001). Regulation of a Wheat Actin-Depolymerizing Factor during Cold Acclimation. Plant Physiol. 125: 360–368. Ozturk NZ, Talame V, Michalowski CB, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002). Monitoring large-scale changed in transcript abundance in drought- and saly-stressed barley. Plant molecular biology (In press). Pilon-Smits EAH, Ebskamp MJM, Paul MJ, Jeuken JW, Weisbeek PJ, Smeekens SCM (1995). Improved performance of transgenic fructanaccumulating tobacco under drought stress. Plant Physiol. 107: 125– 130. Pollock CJ (1986). Fructans and the metabolism of sucrose in vascular plants. New Phytol. 104:1-24. Pollock CJ, Cairns AJ 1991). Fructan metabolism in grasses and cereals. Annu. Rev. Plant Physiol. 42:77-101. Pontis HG, Del CE (1985). Fructans, In: Dey PM, Dixon RA eds. Biochemistry of storage carbohydrates in green plants. Academic Diab et al. 025 Press, New York, NY. pp. 205-227. Rekika D, Nachit MM, Araus JL, Monneveux P (1998). Effects of water deficit on photosynthetic capacity and osmotic adjustment in tetraploid wheats. Photosynthetica. 129-138. Reynolds MP, Balota M, Delgado MIB, Amani I, Fischer RA (1994). Physiological and morphological traits associated with spring wheat yield under hot, irrigated conditions. Aust. J. Plant Physiol. 21, 717– 730. Ricard B, Couee I, Raymond P, Saglio PH, Saint-Ges V, Pradet A (1994). Plant metabolism under hypoxia and anoxia. Plant Physiol. Biochem. 32:1-10. Richards RA, Condon AG (1993). Challenges ahead in using carbon isotope discrimination in plant breeding programs. In ‘Stable isotopes and plant carbon/water relations’. (Eds JR Ehleringer, AE Hall, GD Farquhar) pp. 451–462. (Academic Press: New York). Roxas VP, Smith RK, Allen ER, Allen RD (2000). Overexpression of glutathione-S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotechnol. 15: 988-991. Royo C, Villegas D, García del Mora LF, Elhani S, Aparicio N, Rharrabti Y, Araus JL (2002). Comparative performance of carbon isotope discrimination and canopy temperature depression as predictors of genotype differences in durum wheat yield in Spain. Aust. J. Agric. Res. 53:561–569. Royo C, Garcia Del Moral LF, Aparicio N, Villegas D, Casadesus J, Araus JL (2000). Tools for improving the efficiency of durum wheat selection under Mediterranean conditions. Durum wheat improvement in the Mediterranean region: New challenges. pp. 63- 70. Reynolds, M.P., Singh, R.P., Ibrahim, A., Ageeb, O.A., LarquéSaavedra, A., and Quick J.S., 1998. Evaluating physiological traits to complement empirical selection for wheat in warm environments. Euphytica 100:85-94. Sauer N, Stolz J (1994). SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana. Expression and characterization in baker’s yeast and identification of the histidine-tagged protein. Plant J. 6: 67– 77. Sindhu R, Walton DC (1987). The conversion of xanthoxin to abscisic acid by cell-free preparations from bean leaves. Plant Phsiol. 85: 916-921. Sprenger N, Bortlik K, Brandt A, Boller T, Wiemken A (1995). Purification, cloning, and functional expression of sucrose:fructa- 6- fructosyltransferase, a key enzyme of fructan synthesis in barley. Proc. Natl. Acad. Sci. U.S.A. 92: 11652-11656. Staiger CJ, Gibbon BC, Kovar DR, Zonia LE (1997). Profilin and actindepolymerizing factor: modulators of actin organization in plants. Trends Plant Sci. 2: 275–281. Tambussi EA, Casadesus J, Munné-Bosch S, Araus JL (2002). Photoprotection in water-stressed plants of durum wheat (Triticum turgidum var. durum): changes in chlorophyll fluorescence, spectral signature and photosynthetic pigments. Funct. Plant Biol. 29:35–44. Tetlow IJ, Farrar, JF (1993). Apoplastic sugar concentration and pH in barley leaves infected with Brown rust. J. Exp. Bot, 4: 929-936. Van Deynze AE, Nelson JC, Harrington SE, Yglesias ES, Braga D, McCouch SR, Sorrells ME (1995b). Comparative mapping in grasses: wheat relationships. Mol. Gen. Genet. 248: 744-754. Vick BA, Zimmerman DC (1987). oxidative systems for modification of fatty acids: the lipoxygenase pathway. In: Stumpf PK (ed) The biochemistry of plants: A comprehensive treatise, Vol 9. Academic Press, New York. pp. 53-90. Villegas D, Aparicio N, Nachit MM, Araus JL, Royo C (2000). Photosynthetic and developmental traits associated with genotypic differences in durum wheat yield across the Mediterranean basin. Aust. J. Agric. Res. 51:891–901. Vincent JL, Dahiya P, Brewin NJ (2000). Localized expression of cathepsin B-like sequences from root nodule of Pea (Pisum sativum). American Phtopathology Society. 13: 778-780. Walker-Simmons MK (1997). The wheat protein kinase gene, TaPK3, of the PKABA1 subfamily is differentially regulated in greening wheat seedlings. Plant Mol. Biol. 33: 935-941. Ward W, Alvarado L, Rawlings ND, Engel JC, Franklin C, McKerrow JH (1997). A primitive enzyme for a primitive cell: The protease requiredfor excystation of Giardia. Cell 89: 437-444. Wei Y, Zhang Z, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, Thordal-Christensen H (1998). An epidermis/papilla-specific oxalate oxidase-like protein in the defence response of barley attacked by the powdery mildew fungus. Plant Mol. Biol. 36: 101–112. Williams ML, Farrar JF, Pollock CJ (1989). Cell specialisation within the parenchymatous bundle sheath of barley. Plant Cell Environ. 12: 909–918. Wilson JR, Fisher MJ, Schulze ED, Dolby GR, Ludlow MM (1997). Comparison between pressure-volume and lew point-hygrometry techniques for determining water relation characteristics of grass and legume leaves Oecologia. 41: 77-88. Yang KY, Im YJ, Chung GC, Cho BH (2002). Activity of the Arabidopsis blue copper-binding protein gene promoter in transgenic tobacco plants upon wounding. Plant Cell Rep. 20: 987–991. Zhou F, Zhang Z, Gregersen PL, Mikkelsen JD, de Neergaard E, Collinge DB, Thordal-Christensen H (1998) Molecular Characterization of the Oxalate Oxidase Involved in the Response of Barley to the Powdery Mildew Fungus. Plant Physiol. 117: 33-41.