Osmotic stress induces genes, enzymes and accumulation of galactinol, raffinose and stachyose in seedlings of pea (Pisum sativum L.)

• Autorzy: Pluskota W.E. , Szablinska J. , Obendorf R.L. , Gorecki R. , Lahuta L.B.
• Języki publikacji: EN

Abstrakty

EN

The objective of the present study was to recognize the molecular background of the accumulation of raffinose family oligosaccharides (RFOs) in pea (Pisum sativum L.) seedlings under osmotic stress conditions. The exposure of 5-day-old pea seedlings to osmotic stress for 48 h created by immersing roots in PEG8000 solution (-1.5 MPa) induced synthesis of galactinol and RFOs (raffinose and stachyose) in the epicotyl and root tissues, but not in cotyledons. After 24 h of recovery, galactinol completely disappeared, raffinose decreased fourfold and stachyose decreased twofold in roots, but increased in epicotyls. The temporary accumulation of RFOs resulted from a dramatic increase in the enzymatic activity and changes in expression of galactinol synthase (PsGolS), raffinose synthase (PsRS) and stachyose synthase (PsSTS) genes. PsGolS was induced by osmotic stress in both epicotyls as well as in roots. PsRS and PsSTS were induced only in epicotyls, but repressed or remained unaffected in roots, respectively. During recovery, the expression and activity of PsGolS, PsRS and PsSTS dramatically decreased. The expression of PsGolS gene, that level of mRNA transcript significantly decreased during recovery and whose promoter region was identified to contain some stress-related regulating elements, seems to play a crucial role in the biosynthesis of RFOs under osmotic stress. Possible signals that may trigger the induction of expression of PsGolS, PsRS and PsSTS genes and accumulation of RFOs in pea seedlings are discussed.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 08
• Opis fizyczny: fig.,ref.

Twórcy

autor

Pluskota W.E.

• Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, ul.Oczapowskiego 1A/103, 10-718 Olsztyn, Poland

autor

Szablinska J.

• Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, ul.Oczapowskiego 1A/103, 10-718 Olsztyn, Poland

autor

Obendorf R.L.

• Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, ul.Oczapowskiego 1A/103, 10-718 Olsztyn, Poland

autor

Gorecki R.

• Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, ul.Oczapowskiego 1A/103, 10-718 Olsztyn, Poland

autor

Lahuta L.B.

• Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, ul.Oczapowskiego 1A/103, 10-718 Olsztyn, Poland

Bibliografia

• Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
• Bogdan J, Zagdańska B (2006) Changes in the pool of soluble sugars induced by dehydration at the heterotrophic phase of growth of wheat seedlings. Plant Physiol Biochem 44:787–794
• Brenac P, Horbowicz M, Smith ME, Obendorf RL (2013) Raffinose and stachyose accumulate in hypocotyls during drying of common buckwheat seedlings. Crop Sci 53:1615–1625
• Chakravarthy S, Tuori RP, DAscenzo MD, Fobert PR, Despres C, Martin GB (2003) The tomato transcription factor Pti4 regulates defence-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15:3033–3050
• Chandrasekharan MB, Bishop KJ, Hall TC (2003) Module-specific regulation of the beta-phaseolin promoter during embryogenesis. Plant J 33:853–866
• ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16:1–8
• Farrant JM, Bailly C, Leymarie J, Hamman B, Côme D, Corbineau F (2004) Wheat seedlings as a model to understand desiccation tolerance and sensitivity. Physiol Plant 120:563–574
• Górecki RJ, Piotrowicz-Cieślak AI, Lahuta LB, Obendorf RL (1997) Soluble carbohydrates in desiccation tolerance of yellow lupin seeds during maturation and germination. Seed Sci Res 7:107–115
• Górecki RJ, Lahuta LB, Hedley C, Jones A (2000) Soluble sugars in maturing pea seeds of different lines in relation to desiccation tolerance. In: Black M, Bradford KJ, Vasquez-Ramos J (eds) Seed biology: advances and applications, proceedings of the sixth international workshop on seeds, Merida, Mexico, CAB International, Wallingford, UK, pp 67–74
• Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235
• Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
• Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 7:1242–1255
• Kim SY, Chung HJ, Thomas TL (1997) Isolation of a novel class of bZIP transcription factors that interact with ABA-responsive and embryo-specification elements in the Dc3 promoter using a modified yeast one-hybrid system. Plant J 11:1237–1251
• Kim JH, Hossain AM, Kim N, Lee DH, Lee H (2011) Identification of functional characterization of the galactinol synthase (MoGolS1) gene in Melissa officinalis plants. J Appl Biol Chem 54:244–251
• Komatsu S, Hossain Z (2013) Organ-specific proteome analysis for identification of abiotic stress response mechanism in crop. Front Plant Sci 4:71. doi:10.3389/fpls.2013.00071
• Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol 88:829–832
• Kranner I, Roach T, Beckett RP, Whitaker C, Minibayeva FV (2010) Extracellular production of reactive oxygen species during seed germination and early seedling growth in Pisum sativum. J Plant Physiol 167:805–811
• Lahuta LB (2006) Biosynthesis of raffinose family oligosaccharides and galactosyl pinitols in developing and maturing seeds of winter vetch (Vicia villosa Roth.). Acta Soc Bot Pol 75:219–227
• Lahuta LB, Górecki RJ (2011) Raffinose in seedlings of winter vetch (Vicia villosa Roth) under osmotic stress and followed by recovery. Acta Physiol Plant 33:725–733
• Lahuta LB, Górecki RJ, Gojło E, Horbowicz M (2005) Differences in accumulation of soluble a-galactosides during seed maturation of several Vicia species. Acta Physiol Plant 27:163–171
• Lahuta LB, Pluskota WE, Stelmaszewska J, Szablińska J (2014) Dehydration induces expression of GALACTINOL SYNTHASE and RAFFINOSE SYNTHASE in seedlings of pea (Pisum sativum L.). J Plant Physiol 171:1306–1314
• Maia J, Dekkers BJW, Dolle MJ, Ligterink W, Hilhorst HWM (2014) Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytol 203:81–93
• Michel BE (1983) Evaluation of the water potentials of solutions of polyethylene glycol 8000. Plant Physiol 72:66–70
• Montgomery J, Goldman S, Deikman J, Margossian L, Fischer RL (1993) Identification of an ethylene-responsive region in the promoter of a fruit ripening gene. Proc Natl Acad Sci USA 90:5939–5943
• Morsy MR, Jouve L, Hausman JF, Hoffmann L, Stewart JMD (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167
• Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3- and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60:51–68
• 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
• Nishizawa-Yokoi A, Yabuta Y, Shigeoka S (2008) The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage. Plant Sign Behav 3:1016–1018
• Obendorf RL (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Sci Res 7:63–74
• Obendorf RL, Górecki RJ (2012) Soluble carbohydrates in legume seeds. Seed Sci Res 22:219–242
• Obendorf RL, Zimmerman AD, Zhang Q, Castillo A, Kosina SM, Bryant EG, Sensenig EM, Wu J, Schnebly SR (2009) Accumulation of soluble carbohydrates during seed development and maturation of low-raffinose, low-stachyose soybean. Crop Sci 49:329–341
• Okorska SB, Michalczyk DJ, Okorski A, Piotrowicz-Cieślak A, Głowacka K, Pupel P, Jagielska T, Go´recki RJ (2014) Variability of PSPAL1 (phenylalanine ammonia-lyase gene-1) proximal promoter sequence and expression in pea challenged with Mycosphaerella pinodes. Czech J Genet Plant Breed 50:163–170
• Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, Kim MC, Park CY, Jeong JC, Moon BC, Lee JH, Yoon HW, Lee SH, Chung WS, Lim CO, Lee SY, Hong JC, Cho MJ (2004) Pathogen- and NaClinduced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol 135:2150–2161
• Pastorczyk M, Giełwanowska I, Lahuta LB (2014) Changes in soluble carbohydrates in polar Caryophyllaceae and Poaceae plants in response to chilling. Acta Physiol Plant 36:1771–1780
• Peterbauer T, Richter A (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Sci Res 11:185–197
• Peterbauer T, Lahuta LB, Blöchl A, Mucha J, Jones DA, Hedley CL, Górecki RJ, Richter A (2001) Analysis of the raffinose family oligosaccharide pathway in pea seeds with contrasting carbohydrate composition. Plant Physiol 127:1764–1772
• Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. CABIOS 7:203–206
• Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582
• Roach T, Kranner I (2011) Extracellular superoxide production associated with secondary root growth following desiccation of Pisum sativum seedlings. J Plant Physiol 168:1870–1873
• Rogers SO, Bendich AJ (1994) Extraction of total cellular DNA from plants, algae and fungi. In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual, 2nd edn. Kluwer Academic Publishers, Dordrecht, pp 183–190
• Rosenwasser S, Fluhr R, Joshi JR, Leviatan N, Sela N, Hetzroni A, Friedman H (2013) ROSMETER: a bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiol 163:1071–1083
• Singh AK, Rana MK, Singh S, Kumar S, Kumar R, Singh R (2014) CAAT box-derived polymorphism (CBDP): a novel promotertargeted molecular marker for plants. J Plant Biochem Biotechnol 23:175–183
• Sun WQ, Leopold AC (1997) Cytoplasmic vitrification and survival of anhydrobiotic organisms. Compar Biochem Physiol A 117A:327–333
• Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89
• 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
• Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organization, expression and DNA-binding characteristics. Plant Mol Biol 50:43–57
• Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539
• Valluru R, Van den Ende W (2011) myo-Inositol and beyond—emerging networks under stress. Plant Sci 181:387–400
• Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18
• Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X (2009) A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of galactinol synthase (BhGolS1) promoter. Planta 230:1155–1166
• Wang D, Yao W, Song Y, Liu W, Wang Z (2012a) Molecular characterization and expression of three galactinol synthase genes that confer stress tolerance in Salvia miltiorrhiza. J Plant Physiol 169:1838–1848
• Wang G, Wang G, Zhang X, Wang F, Song R (2012b) Isolation of high quality RNA from cereal seeds containing high levels of starch. Phytochem Anal 23:159–163
• Wu X, Kishitani S, Ito Y, Toriyama K (2009) Accumulation of raffinose in rice seedlings overexpressing OsWRKY11 in relation to desiccation tolerance. Plant Biotech 26:431–434
• Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, ThompsonD, ShenQJ (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
• Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cryoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830
• Yu SM, Lee YC, Chan MT, Hwa SF, Liu LF (1996) Sugars act as signal molecules and osmotica to regulate the expression of alpha-amylase genes and metabolic activities in germinating cereal grains. Plant Mol Biol 30:1277–1289
• Zhou ML, Zhang Q, Zhou M, Sun ZM, Zhu XM, Shao JR, Tang YX, Wu YM (2012) Genome-wide identification of genes involved in raffinose metabolism in maize. Glycobiology 22:1775–1785
• Zhou J, Yang Y, Yu J, Wang L, Yu X, Ohtani M, Kusano M, Saito K, Demura T, Zhuge Q (2014) Responses of Populus trichocarpa galactinol synthase genes to abiotic stresses. J Plant Res 127:347–358

Identyfikatory

DOI

10.1007/s11738-015-1905-9