Abstract
Accumulation of compatible osmolytes, such as soluble sugars, in plants is an important osmoprotective mechanism. Sugars play a role in osmotic adjustment and are associated with stabilization of proteins and cell structures, reactive oxygen species scavenging, signaling functions or induction of adaptive pathways. Galactinol is the galactosyl donor for the synthesis of raffinose family oligosaccharides (RFOs) and its synthesis by galactinol synthase (GolS) is the first committed step of the RFOs biosynthetic pathway. GolS genes are induced by a variety of stresses in both stress-sensitive and tolerant-plant species; however, the mechanism of transcriptional regulation is not fully established. In this paper, we characterized a GolS gene (BhGolS1) that was dehydration and ABA-inducible in the resurrection plant Boea hygrometrica and conferred dehydration tolerance in a transgenic tobacco system. Four W-box cis-elements were identified in the BhGolS1 promoter and shown to be bound by an early dehydration and ABA-inducible WRKY gene (BhWRKY1). These data suggest a mechanism where BhWRKY1 is likely to function in an ABA-dependent signal pathway to regulate BhGolS1 expression, which leads to the accumulation of RFOs in desiccation-tolerant B. hygrometrica leaves.
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Abbreviations
- GolS:
-
Galactinol synthase
- Gol:
-
Galactinol
- Raf:
-
Raffinose
- RFO:
-
Raffinose family oligosaccharide
References
Albini FM, Murelli C, Finzi PV, Ferrarotti M, Cantoni B, Puliga S, Vazzana C (1999) Galactinol in the leaves of the resurrection plant Boea hygroscopica. Phytochemistry 51:499–505
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) Map kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983
Ayre BG, Keller F, Turgeon R (2003) Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol 131:1518–1528
Bachmann M, Matile P, Keller F (1994) Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. (cold acclimation, translocation, and sink to source transition: discovery of chain elongation enzyme). Plant Physiol 105:1335–1345
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Brenac P, Horbowicz M, Downer SM, Dickerman AM, Smith ME, Obendorf RL (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. J Plant Physiol 150:481–488
Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucl Acids Res 31:3497–3500
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation acid guanidinuim thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159
Collett H, Shen A, Gardner M, Farrant JM, Denby KJ, Illing N (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiol Plant 122:39–53
Dellagi A, Birch PRJ, Heilbronn J, Avrova AO, Montesano M, Palva ET, Lyon GD (2000) A potato gene, erg-1, is rapidly induced by Erwinia carotovora ssp, atroseptica, Phytophthora infestans, ethylene and salicylic acid. J Plant Physiol 157:201–205
Deng X, Hu ZA, Wang HX, Wen XG, Kuang TY (2003) A comparison of photosynthetic apparatus of the detached leaves of the resurrection plant Boea hygrometrica with its non-tolerant relative Chirita heterotrichia in response to dehydration and rehydration. Plant Sci 165:851–861
Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37
Doyle J, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Du L, Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J 24:837–847
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:200–206
Farrant JM (2007) Mechanisms of desiccation tolerance in angiosperm resurrection plants. CAB International, Wallingford, UK
Farrant JM, Lehne A, Cooper K, Wiswedel S (2009) Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. Plant J 57:65–79
Frisch DA, Harris-Haller LW, Yokubaitis NT, Thomas TL, Hardin SH, Hall TC (1995) Complete sequence of the binary vector Bin 19. Plant Mol Biol 27:405–409
Goff SA, Ricke D, Lan TH et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100
Handley LW, Pharr DM, Mcfeeters RF (1983) Relationship between galactinol synthase activity and sugar composition of leaves and seeds of several crop species. J Am Soc Hortic Sci 108:600–605
Hara K, Yagi M, Kusano T, Sano H (2000) Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol Gen Genet 263:30–37
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl Acids Res 27:297–300
Horbowicz M, Obendorf RL (1994) Seed desiccation tolerance and storability: dependence on flatulence-producing oligosaccharides and cyclitols—review and survey. Seed Sci Res 4:385–405
Horsch R, Fry JE, Hoffmann N, Eichholtz D, Rogers S, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231
Huang T, Duman JG (2002) Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara. Plant Mol Biol 48:339–350
Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405
Jiang GQ, Wang Z, Shang HH, Yang WL, Hu ZA, Phillips J, Deng X (2007) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225:1405–1420
Kapila J, Rycke RD, Montagu MV, Angenon G (1997) An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122:101–108
Keller F, Pharr DM (1996) Metabolism of carbohydrates in sinks and source: galactosyl-sucrose oligosaccharides. In: Zamski E, Schaffer AA (eds) Photoassimilate distribution in plants and crops: source–sink relationships. Marcel Dekker, New York, pp 157–183
Kim CY, Lee SH, Park HC, Bae CG, Cheong YH, Choi YJ, Han C, Lee SY, Lim CO, Cho MJ (2000) Identification of rice blast fungal elicitor-responsive genes by differential display analysis. Mol Plant Microbe Interact 13:470–474
Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol 88:829–832
Liu JJ, Odegard W, de Lumen BO (1995) Galactinol synthase from kidney bean cotyledon and zucchini leaf. Plant Physiol 109:505–511
Liu JJ, Krenz DC, Galvez AF, de Lumen BO (1998) Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation. Plant Sci 134:11–20
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547
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
Ochman H, Gerber AS, Hartl DL (1988) Genetic application of an inverse polymerase chain reaction. Genetics 120:621–623
Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased thermotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383
Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151:85–100
Panikulangara TJ, Eggers-Schumacher G, Wunderlich M, Stransky H, Schöffl F (2004) Galactinol synthase1. A novel heat shock factor target gene responsible for heat-induced synthesis of raffinose family oligosaccharides in Arabidopsis. Plant Physiol 136:3148–3158
Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating α-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133:901–909
Peterbauer T, Richter A (2001) Analysis of the raffinose family oligosaccharide pathway in pea seeds with contrasting carbohydrate composition. Plant Physiol 127:1764–1772
Peterbauer T, Mucha J, Mach L, Richter A (2002) Chain elongation of raffinose in pea seeds-isolation, characterization, and molecular cloning of a multifunctional enzyme catalyzing the synthesis of stachyose and verbascose. J Biol Chem 277:194–200
Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J Exp Bot 58:1947–1956
Phillips JR, Oliver MJ, Bartels D (2002) Molecular genetics of desiccation tolerant systems. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, pp 319–341
Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319–330
Qiu Y, Jing S, Fu J, Li L, Yu D (2004) Cloning and analysis of expression profile of 13 WRKY genes in rice. Chin Sci Bull 49:2159–2168
Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151
Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736–11743
Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence-and defense-related processes. Plant J 28:123–133
Scott P (2000) Resurrection plants and the secrets of eternal leaf. Ann Bot 85:159–166
Seki M, Narusaka M, Ishida J et al (2002) Monitoring the expression profiles of 7, 000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Sprenger N, Keller F (2000) Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga repants: the role of two distinct galactinol synthases. Plant J 21:249–258
Sun CX, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092
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
Ueda T, Coseo MP, Harrell TJ, Obendorf RL (2005) A multifunctional galactinol synthase catalyzes the synthesis of fagopyritol A1 and fagopyritol B1 in buckwheat seed. Plant Sci 168:681–690
Vicre M, Farrant JM, Driouich A (2004) Insights into the mechanisms of desiccation tolerance among resurrection plants. Plant Cell Environ 27:1329–1340
Wang H, Tang WN, Zhu C, Perry SE (2002) A chromatin immunoprecipitation (ChIP) approach to isolate genes regulated by AGL15, a MADS domain protein that preferentially accumulates in embryos. Plant J 32:831–843
Wang LL, Shang HH, Liu YX, Zheng MZ, Wu RH, Phillips J, Bartels D, Deng X (2009) A role for a cell wall localized glycine-rich protein in dehydration and rehydration of the resurrection plant Boea hygrometrica. Plant Biol. doi:10.1111/j.1438-8677.2008.00187.x
Xie Z, Zhang ZL, Zou XL, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189
Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (1)-d-Cadinene Synthase-A. Plant Physiol 135:507–515
Yu DQ, Chen CH, Chen ZX (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1539
Zhang ZL, Xie Z, Zou XL, Casaretto J, David Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513
Zhao TY, Thacker R, Willis CJ, Snyder JC, Meeley RB, Obendorf RL, Downie B (2004) Expression of the maize galactinol synthase gene family: (I) expression of two different genes during seed development and germination. Physiol Plant 121:634–646
Zhou QY, Tian AG, Zou HF, Xie ZM, Gang L, Jian H, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Biotechnol J 6:486–503
Zuther E, Büchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett 576:169–173
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This project was supported by the National High Technology Research and Development Program of China (863 Program) (No. 2007AA021403) and the National Natural Science Foundation of China (No. 30400027).
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Wang, Z., Zhu, Y., Wang, L. et al. A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230, 1155–1166 (2009). https://doi.org/10.1007/s00425-009-1014-3
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DOI: https://doi.org/10.1007/s00425-009-1014-3