Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2014 | 36 | 07 |

Tytuł artykułu

Changes in soluble carbohydrates in polar Caryophyllaceae and Poaceae plants in response to chilling

Warianty tytułu

Języki publikacji



Four species of flowering plants comprising Arctic populations of Cerastium alpinum and Poa arctica var. vivipara and indigenous Antarctic species Colobanthus quitensis and Deschampsia antarctica were investigated. Plants derived from natural origins were grown in an experimental greenhouse in Poland (53°47'N and 20°30'E latitude). Plants for experiment were collected during spring of 2010. Soluble carbohydrates in the intact shoots of C. alpinum and C. quitensis, polar plants of the family Caryophyllaceae, and D. antarctica and P. arctica var. vivipara, representatives of the family Poaceae, were analyzed by gas chromatography, and their involvement in the plants’ response to chilling stress was examined. Plant tissues of the examined families growing in a greenhouse conditions (18–20°C, short day 10/14 h light/darkness) differed in the content and composition of soluble carbohydrates. In addition to common monosaccharides, myo-inositol and sucrose, Caryophyllaceae plants contained raffinose family oligosaccharides (RFOs), ᴅ-pinitol and mono-galactosyl pinitols. RFOs and ᴅ-pinitol were not detected in plants of the family Poaceae which contain 1-kestose, a specific tri-saccharide. The accumulation of significant quantities of sucrose in all investigated plants, RFOs in Caryophyllaceae plants and 1-kestose in Poaceae plants in response to chilling stress (4°C for 48 h with a long day photoperiod, 20/4 h) indicates that those compounds participate in the stress response. The common sugar accumulating in cold stress response and probably most important for chilling tolerance of four investigated plants species seems to be sucrose. On the other hand, the accumulation of above-mentioned carbohydrates during chilling stress can be a return to sugars metabolism, occurring in natural environmental conditions. No changes in ᴅ-pinitol concentrations were observed in the tissues of C. alpinum and C. quitensis plants subjected to both low and elevated temperatures, which probably rules out the protective effects of ᴅ-pinitol in response to cold stress.

Słowa kluczowe








Opis fizyczny



  • Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1 A, 10-719 Olsztyn, Poland
  • Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1 A, 10-719 Olsztyn, Poland
  • Department of Antarctic Biology and Polish Antarctic Station "H. Arctowski", Institute of Biochemistry and Biophysics PAS, Ustrzycka 10/12, 02-141 Warsaw, Poland
  • Department of Plant Physiology, Genetics and Biotechnology, University of Warmia and Mazury in Olsztyn, Oczapowskiego 1 A, 10-719 Olsztyn, Poland


  • Amiard V, Morvan-Bertrand A, Billard J-P, Huault C, Keller F, Prud’homme M-P (2003) Fructans, but not the sucrosyl-galactosides, raffinose and loliose, are affected by drought stress in perennial ryegrass. Plant Physiol 132:2218–2229
  • Bachmann M, Metile 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
  • Benina M, Obata T, Mehterov N, Ivanov I, Petrov V, Toneva V, Fernie AR, Gechev TS (2013) Comparative metabolic profiling of Haberlea rhodopensis, Thellungiella halophyla, and Arabidopsis thaliana exposed to low temperature. Front Plant Sci. doi:10.3389/fpls.2013.00499
  • Bravo LA, Griffith M (2005) Characterization of antifreeze activity in Antarctic plants. J Exp Bot 56:1189–1196
  • Bravo LA, Ulloa N, Zuñiga GE, Casanova A, Corcuera LJ, Alberdi M (2001) Cold resistance in Antarctic angiosperms. Physiol Plant 111:55–65
  • Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AG, Huner NPA, Corcuera LJ (2007) Effect of cold acclimation on the photosynthesis performance of two ecotypes of Colobanthus quitensis (Kunth.) Bartl. J Exp Bot 58:3581–3590
  • Cunningham SM, Nadeau P, Castonguay Y, Laberge S, Volence JJ (2003) Raffinose and stachyose accumulation, galactinol synthase expression, and winter injury of contrasting alfalfa germplasms. Crop Sci 43:562–570
  • Davey MP, Woodward FI, Quick WP (2009) Intraspecific variation in cold-temperature metabolic phenotypes of Arabidopsis lyrata ssp. petraea. Metabolomics 5:138–149
  • Del Viso F, Casabuono AC, Couto AS, Hopp HE, Puebla AP, Heinz RA (2011) Functional characterization of a sucrose:fructan 6-fructosyltransferase of the cold-resistant grass Bromus pictus by heterelogous expression in Pichia pastoris and Nicotiana tabacum and its involvement in freezing tolerance. J Plant Physiol 168:493–499
  • Downie B, Gurusinghe S, Dahal P, Thacker RR, Snyder JC, Nonogaki H, Yim K, Fukanaga K, Alvarado V, Bradford KJ (2003) Expression of a GALACTINOL SYNTHASE gene in tomato seeds is up-regulated before maturation desiccation and again after imbibition whenever radicle protrusion is prevented. Plant Physiol 131:1347–1359
  • ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16:1–8
  • Giełwanowska I (2003) Deschampsia antarctica responses to abiotic stress factors. Acta Physiol Plant 25:61–62
  • Giełwanowska I, Szczuka E (2005) New ultrastructural features of organelle in leaf cells of Deschampsia antarctica Desv. Polar Biol 28:951–955
  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235
  • Iftime D, Hannah MA, Peterbauer T, Heyer AG (2011) Stachyose in the cytosol does not influence freezing tolerance of transgenic Arabidopsis expressing stachyose synthase from adzuki bean. Plant Sci 180:24–30
  • John UP, Polotnianka RM, Sivakumaran KA, Chew O, Mackin L, Kuiper MJ, Talbot JP, Nugent GD, Mautord J, Schrauf GE, Spangenberg GC (2009) Ice recrystallization inhibition proteins (IRIPs) and freeze tolerance in the cryophilic Antarctic hair grass Deschampsia antarctica E Desv. Plant Cell Environ 32:336–348
  • 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 36:1242–1255
  • Klotke J, Kopka J, Gatzke N, Heyer AG (2004) Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation—evidence for a role of raffinose in cold acclimation. Plant Cell Environ 27:1395–1404
  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350
  • Lackey KH, Pope PM, Johnson MD (2003) Expression of 1L-myoinositol-1-phosphate synthase in organelles. Plant Physiol 132:2240–2247
  • 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
  • Lundmark M, Cavaco AM, Trevanion S, Hurry V (2006) Carbon partitioning and export in transgenic Arabidopsis thaliana with altered capacity for sucrose synthesis grown at low temperature: a role for metabolite transporters. Plant Cell Environ 29:1703–1714
  • Monson RK, Rosenstiel TN, Forbis TA, Lipson DA, Jaeger CH (2006) Nitrogen and carbon storage in alpine plants. Integr Comp Biol 46(1):35–48
  • Montiel PO, Cowan DA (1993) The possible role of soluble carbohydrates and polyols as cryoprotectans in Antarctic plants. In: Heywood RB (ed). University Research in Antarctica. 1989–1992. British Antarctic Survey. Cambridge, pp. 119–125
  • Obendorf RL, Górecki RJ (2012) Soluble carbohydrates in legume seeds. Seed Sci Res 22:219–242
  • Parnikoza I, Kozeretska I, Kunakh V (2011) Vascular plants of the maritime Antarctic: orgin and adaptation. Am J Plant Sci 2:381–395
  • Peterbauer T, Richter A (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Sci Res 11:185–197
  • Peters S, Keller F (2009) Frost tolerance in excised leaves of the common bugle (Ajuga reptans L.) correlates positively with the concentrations of raffinose family oligosaccharides (RFOs). Plant Cell Environ 32:1099–1107
  • Piotrowicz-Cieślak AI, Giełwanowska I, Bochenek A, Loro P, Górecki R (2005) Occurrence of carbohydrates in Colobanthus quitensis and Deschampsia antarctica. Acta Soc Bot Pol 74:209–217
  • Pontis HG (1989) Fructans and cold stress. J Plant Physiol 134:148–150
  • Purdy SJ, Maddison AL, Jones LE, Webster RJ, Andralojc J, Donnison I, Clifton-Brown J (2013) Characterization of chillingshock responses in four genotypes of Miscanthus reveals the superior tolerance of M. × giganteus compared with M. sinensis and M. sacchariflorus. Ann Bot 111:999–1013
  • Romero M, Casanova A, Iturra G, Reyes A, Montenegro G, Alberdi M (1999) Leaf anatomy of Deschampsia antarctica (Poaceae) from the maritime Antarctic and its plastic response to changes in the growth conditions. Revista Chilena de Historia Natural 72:411–425
  • Sandve SR, Kosmala A, Rudi H, Fjellheim S, Rapacz M, Yamada T, Rognli OA (2011) Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates. Plant Sci 180:69–77
  • Schneider T, Keller F (2009) Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant Cell Physiol 50:2174–2182
  • Shimojima M, Ohta H (2011) Critical regulation of galactolipid synthesis controls membrane differentiation and remodeling in distinct plant organs and following environmental changes. Prog Lipid Res 50:258–266
  • Somerville CR, Browse J (1996) Dissecting desaturation: plants prove advantageous. Trends Cell Biol 6:148–153
  • Strand A, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux trough the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ 26:523–535
  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important role of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426
  • Turner S, Senaratna T, Touchell D, Bunn E, Dixon K, Tan B (2001) Stereochemical arrangement of hydroxyl groups in sugar and polyalcohol molecules as an important factor in effective cryopreservation. Plant Sci 160:489–497
  • Usadel B, Bläsing OE, Gibon Y, Poree F, Höhne M, Günther M, Trethewey R, Kamlage B, Poorter H, Stitt M (2008) Multilevel genomic analysis of the response of transcripts enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ 31:518–547
  • Valluru R, Van den Ende W (2008) Plant fructans in stress environment: emerging concepts and future prospects. J Exp Bot 59:2905–2916
  • Van den Bogaart G, Hermans N, Krasnikov V, de Vries AH, Poolman B (2007) On the decrease in lateral mobility of phospholipids by sugars. Biophys J 92:1598–1605
  • Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4:247. doi:10.3389/fpls.2013.00247
  • Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18
  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cryoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830
  • Zúñiga GE, Alberdi M, Fernández J, Montiel P, Corcuera LJ (1994) Lipid content in leaves of Deschampsia antarctica from the Maritime Antarctic. Phytochemistry 37:669–672
  • Zúñiga GE, Alberdi M, Corcuera LJ (1996) Non-structural carbohydrates in Deschampsia antarctica Desv. from South Shetland Islands, maritime Antarctic. Environ Exp Bot 36:393–398
  • Zúñiga-Feest A, Inostroza P, Vega M, Bravo LA, Corcuera LJ (2003) Sugars and enzyme activity in the grass Deschampsia antarctica. Antarct Sci 15:483–491
  • Zúñiga-Feest A, Ort DR, Gutierrez A, Gidekel M, Bravo LA, Corcuera LJ (2005) Light regulation of sucrose-phosphate synthase activity in the freezing-tolerant grass Deschampsia antarctica. Photosynt Res 83:75–86
  • Zúñiga-Feest A, Bascuñán-Godoy L, Reyes-Diaz M, Bravo LA, Corcuera LJ (2009) Is survival after ice encasement related with sugar distribution in organs of the Antarctic plants Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae)? Polar Biol 32:583–591
  • 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

Typ dokumentu



Identyfikator YADDA

JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.