Abstract
Drought is one of the major factors that limits crop production and reduces yield. To understand the early response of plants under nearly natural conditions, pepper plants (Capsicum annuum L.) were grown in a greenhouse and stressed by withholding water for 1 week. Plants adapted to the decreasing water content of the soil by adjustment of their osmotic potential in root tissue. As a consequence of drought, strong accumulation of raffinose, glucose, galactinol and proline was detected in the roots. In contrast, in leaves the levels of fructose, sucrose and also galactinol increased. Due to the water deficit cadaverine, putrescine, spermidine and spermine accumulated in leaves, whereas the concentration of polyamines was reduced in roots. To study the molecular basis of these responses, a combined approach of suppression subtractive hybridisation and microarray technique was performed on the same material. A total of 109 unique ESTs were detected as responsive to drought, while additional 286 ESTs were selected from the bulk of rare transcripts on the array. The metabolic profiles of stressed pepper plants are discussed with respect to the transcriptomic changes detected, while attention is given to the differences between defence strategies of roots and leaves.
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Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Bi 16:1–18
Boeuf S, Klingenspor M, Van Hal NL, Schneider T, Keijer J, Klaus S (2001) Differential gene expression in white and brown preadipocytes. Phys Genom 7:15–25
Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264
Cushman C (2001) Osmoregulation in plants: implications for agriculture. Am Zool 41:758–769
De Ronde JA, Cress WA, Kruger GHJ, Strasser RJ, van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5VR gene, during heat and drought stress. J Plant Physiol 166:1211–1224
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223
Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskayqa N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030
El-Bashiti T, Hamamci H, Öktem HA, Yücel M (2005) Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions. Plant Sci 169:47–54
Fluch S, Olmo CC, Tauber S, Stierschneider M, Kopecky D, Reichenauer TG, Matusikova I (2008) Transcriptomic changes in wind-exposed poplar leaves are dependent on developmental stage. Planta 228:757–764
Girousse C, Bournoville R, Bonnemain JL (1996) Water deficit induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111:109–113
Golan-Goldhirsh A, Hankamer B, Lips SH (1990) Hydroxyproline and proline content of cell walls of sunflower, peanut and cotton grown under salt stress. Plant Sci 69:27–32
González-Dugo V, Orgaz F, Fereres E (2007) Responses of pepper to deficit irrigation for paprika production. Sci Hortic 114:77–82
Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero AC Jr (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95:11140–11145
Hanson AD, Rathinasabapathi B, Rivoal J, Burnet M, Dillon MO, Gage DA (1994) Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci USA 91:306–310
Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434
Hida K, Wada J, Zhang H, Hiragushi K, Tsuchiyama Y, Shikata K, Makino H (2000) Identification of genes specifically expressed in the accumulated visceral adipose tissue of OLETF rats. J Lipid Res 41:1615–1622
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992
Kacperska A (2004) Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plantarum 122:159–168
Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi RN, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Ist implication in plant growth and abiotic stress tolerance. Curr Sci 88:424–438
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487
Kuznetsov V, Shorina M, Aronova E, Stetsenko L, Rakitin V, Shevyakova N (2007) NaCl- and ethylene-dependent cadaverine accumulation and Ist possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci 172:363–370
Laher FR, Aziz A, Gibon Y, Trotel-Aziz P, Sulpice R, Bouchereau A (2003) An assessment of the physiological properties of the so-called compatible solutes using in vitro experiments with leaf discs. Plant Physiol Biochem 41:657–666
Liu K, Fu H, Bie Q, Luan S (2000a) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326
Liu Q, Zhang Y, Shouyi C (2000b) Plant protein kinase genes induced by drought, high salt and cold stresses. Chinese Sci Bull 45:1153–1157
Liu F, Jensen CR, Andersen MN (2003) Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crop Res 86:1–13
Liu HP, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci 166:1261–1267
Lu P, Chen N, An R, Su Z, Qi B, Ren F, Chen J, Wang X (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305
Mercke P, Kappers IF, Verstappen FWA, Vorst O, Dicke M, Bouwmeester HJ (2004) Combined Transcript and Metabolite Analysis Reveals Genes Involved in Spider Mite Induced Volatile Formation in Cucumber Plants. Plant Physiol 135:2012–2024
Molinari HBC, Marur CJ, Bespalhok Filho JC, Kobyashi AK, Pilleggi M, Leite RP Jr, Pereira LFP, Vieira LGE (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb × Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167:1375–1381
Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263
Oufir M, Legay S, Nicot N, Van Moer K, Hoffmann L, Renaut J, Hausman JF, Evers D (2008) Gene expression in potato during cold exposure: changes in carbohydrate and polyamine metabolisms. Plant Sci 175:839–852
Oufir M, Schulz N, Sha Vallikhan PS, Wilhelm E, Burg K, Hausman JF, Hoffmann L, Guignard C (2009) Simultaneous measurement of proline and related compounds in oak leaves by high-performance ligand-exchange chromatography and electrospray ionization mass spectrometry for environmental stress studies. J Chromatogr A 1216:1094–1099
Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z (2007) Identification of early salt stress responses genes in tomato root by suppression subtractive hybridisation and microarray analysis. J Exp Bot 58:507–520
Petalidis L, Bhattacharyya S, Morris GA, Collins VP, Freeman TC, Lyons PA (2003) Global amplification of mRNA by template-switching PCR: linearity and application to microarray analysis. Nucl Acids Res 31:e142
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucl Acids Res 30:36
Pinheiro C, Chaves MM, Ricardo CP (2001) Alterations in carbon and nitrogen metabolism induced by water deficit in the stems and leaves of Lupinus albus L. J Exp Bot 52:1063–1070
Prewein C, Vagner M, Wilhelm E (2004) Changes in water status and proline and abscisic acid concentrations in developing somatic embryos of pedunculate oak (Quercus robur) during maturation and germination. Tree Physiol 24:1251–1257
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202
Rondeau G, McClelland M, Nguyen T, Risques R, Wang Y, Judex M, Cho AH, Welsh J (2005) Enhanced microarray performance using low complexity representations of the transcriptome. Nucl Acids Res 33:e100
Rylski I, Spigelman M (1982) Effects of different diurnal temperature combinations on fruit set of sweet pepper. Sci Hortic 17:101–106
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 14:1675–1690
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Su J, Wu R (2004) Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci 166:941–948
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426
Theiss C, Bohley P, Voigt J (2002) Regulation by Polyamines of Ornithine Decarboxylase Activity and Cell Division in the Unicellular Green Alga Chlamydomonas reinhardtii. Plant Physiol 128:1470–1479
Trouverie J, Thévenot C, Rocher JP, Sotta B, Prioul JL (2003) The role of abscisic acid in the response of a specific vacuolar invertase to water stress in the adult maize leaf. J Exp Bot 54:2177–2186
Ueda A, Yamamoto-Yamane Y, Takabe T (2007) Salt stress enhances proline utilization in the apical region of barley roots. Biochem Biophys Res Co 355:61–66
Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kumar D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson LT, van Zyl L, Egertdotter U, Sederoff RR, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133:1702–1716
Way H, Chapman S, McIntyre L, Casu R, Xue GP, Manners J, Shorter R (2005) Identification of differentially expressed genes in wheat undergoing gradual water deficit stress using a subtractive hybridisation approach. Plant Sci 168:661–670
Yalovsky S, Paulsen H, Michaeli D, Chirnis PR, Nechushtai R (1992) Involvement of a chloroplast HSP70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane. Proc Natl Acad Sci USA 89:5616–5619
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Acknowledgments
The authors gratefully acknowledge E. Boland, B. De Vos and L. Solinhac for their valuable technical assistance and Dr. Bodo Trognitz (AIT Austrian Institute of Technology GmbH, Department of Health and Environment/Bioresources, PICME) for his valuable comments on the manuscript. The work of IM was supported by the project COST FA 0605.
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Sziderics, A.H., Oufir, M., Trognitz, F. et al. Organ-specific defence strategies of pepper (Capsicum annuum L.) during early phase of water deficit. Plant Cell Rep 29, 295–305 (2010). https://doi.org/10.1007/s00299-010-0822-z
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DOI: https://doi.org/10.1007/s00299-010-0822-z