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Abiotic Stress Responses in Plants pp 253–265Cite as

Trehalose and Abiotic Stress Tolerance

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Abstract

Trehalose is a nonreducing disaccharide present in diverse organisms ranging from bacteria and fungi to invertebrates, in which it serves as an energy source as well as an osmolyte and/or protein/membrane protectant. Until recently, trehalose was not thought to be of any real significance in plants, although genetic studies have confirmed the existence of surprising abundance of genes for trehalose metabolism in plants, which have led to propose trehalose pathway as a central metabolic regulator. Multiple studies have linked trehalose to abiotic stress tolerance in plants and different research groups have attempted to create stress tolerant plants by introducing trehalose biosynthetic genes in important crops such as rice, tomato, and potato. Particular cases of the trehalose metabolism are plant symbiotic interactions such as the rhizobia–legume symbiosis, where trehalose has been described as a major carbohydrate in root nodules of some species. The discovery of trehalose metabolism in the recent years has pointed out the importance of trehalose biosynthesis in stress responses in plants.

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References

  • Addy HD, Schaffer GF, Miller MH, Peterson RL (1994) Survival of the extraradical mycelium of a VAM fungus in frozen soil over winter. Mycorrhiza 5:1–5

    Article  Google Scholar 

  • Almeida AM, Silva AB, Aráujo SS, Cardoso LA, Santos DM (2007) Responses to water withdrawal of tobacco plants genetically engineered with the AtTPS1 gene: a special reference to photosynthetic parameters. Euphytica 154:113–126

    Article  CAS  Google Scholar 

  • Anselmino O, Gilg E (1913) Ueber das Vorkommen von Trehalose in Selaginella lepidophylla. Ber Deut Pharm Ges 23:326–330

    CAS  Google Scholar 

  • Arguelles JC (2000) Physiological roles of trehalose in bacteria and yeasts: a comparative analysis. Arch Microbiol 174:217–224

    Article  PubMed  CAS  Google Scholar 

  • Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G (2004) The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659

    Article  PubMed  CAS  Google Scholar 

  • Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G (2006) Insights on the evolution of trehalose biosynthesis. BMC Evol Biol 6:109–113

    Article  PubMed  Google Scholar 

  • Becker A, Scholeder P, Wegener G (1996) The regulation metabolism in insects. Experientia 52:433–439

    Article  PubMed  CAS  Google Scholar 

  • Bianchi G, Gamba A, Limiroli R, Pozzi N, Elster R, Salamini F, Bartels D (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226

    Article  CAS  Google Scholar 

  • Blázquez MA, Santos E, Flores CL, Martínez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13: 685–689

    Article  PubMed  Google Scholar 

  • Cabib E, Lenoir LF (1958) The biosynthesis of trehalose phosphate. J Biol Chem 231:259–275

    PubMed  CAS  Google Scholar 

  • Cortina C, Culianez-Maciá FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75–82

    Article  CAS  Google Scholar 

  • Crowe JH (2007) Trehalose as a “chemical chaperone”: fact and fantasy. Adv Exp Med Biol 594:143–158

    Article  PubMed  Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703

    Article  PubMed  CAS  Google Scholar 

  • De Smet KA, Weston A, Brown IN, Young DB, Robertson BD (2000) Three pathways for trehalose biosynthesis in mycobacteria. Microbiology 146:199–208

    PubMed  Google Scholar 

  • Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29: 223–235

    Article  Google Scholar 

  • Elbein AD (1974) The metabolism of α,α-trehalose. Adv Carbohydr Chem Biochem 30:227–256

    Article  PubMed  CAS  Google Scholar 

  • Elbein AD, Mitchell M (1973) Levels of glycogen and trehalose in Mycobacterium smegmatis and the purification and properties of the glycogen synthetase. J Bacteriol 113(2):863–873

    PubMed  CAS  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifuntional molecule. Glycobiology 13:17–27

    Article  Google Scholar 

  • Farías-Rodriguez R, Mellor RB, Arias C, Peña-Cabriales JJ (1998) The accumulation of trehalose in nodules of several cultivars of common bean (Phaseolus vulgaris) and its correlation with resistance to draught stress. Physiol Plant 102:353–359

    Article  Google Scholar 

  • Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417

    Article  PubMed  CAS  Google Scholar 

  • Fougère F, Le Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.). Plant Physiol 96:1228–1236

    Article  PubMed  Google Scholar 

  • Frison M, Parrou JL, Guillaumot D, Masquelier D, François J, Chaumont F, Batoko H (2007) The Arabidopsis thaliana trehalase is a plasma membrane-bound enzyme with extracellular activity. FEBS Lett 581:4010–4016

    Article  PubMed  CAS  Google Scholar 

  • García B, de Almeida EJ, Iyer S, Gerats T, Van Montagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169

    PubMed  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  PubMed  CAS  Google Scholar 

  • Gibon Y, Bessieres MA, Larher F (1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant Cell Environ 20:329–340

    Article  Google Scholar 

  • Gomez LD, Baud S, Gilday A, Li Y, Graham I (2006) Delayed embryo development in the Arabidopsis trehalose 6-phosphate synthase 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46:69–84

    Article  PubMed  CAS  Google Scholar 

  • Gooddijn OJM, Verwoerd TC, Voogd E, Krutwagen PWHH, de Graaf PTHM, Poels J, Van Dun K, Ponstein AS, Damm B, Pen J (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiol 113:181–190

    Article  Google Scholar 

  • Grennan AK (2007) The role of trehalose biosynthesis in plants. Plant Physiol 144:3–5

    Article  PubMed  CAS  Google Scholar 

  • Han SE, Park SR, Kwon HB, Yi BY, Lee GB, Byun MO (2005) Genetic engineering of drought-resistant tobacco plants by introducing the trehalose phosphorylase (TP) gene from Pleurotus sajor-caju. Plant Cell Tissue Organ Cult 82:151–158

    Article  CAS  Google Scholar 

  • Higashiyama T (2002) Novel functions and applications of trehalose. Pure Appl Chem 74:1263–1269

    Article  CAS  Google Scholar 

  • Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50: 1223–1229

    Article  PubMed  CAS  Google Scholar 

  • Jasper DA, Abbott LK, Robson AD (1993) The survival of infective hyphae of vesicular arbuscular mycorrhizal fungi in soil: an interaction with sporulation. New Phytol 124:73–479

    Article  Google Scholar 

  • Kaasen I, McDougall J, Strom AR (1994) Analysis of the otsBA operon for osmoregulatory trehalose synthesis in Escherichia coli. Gene 145:9–15

    Article  PubMed  CAS  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller K, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature–stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    Article  PubMed  CAS  Google Scholar 

  • Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mäntylä E, Tapio Palva E, Van Dijck P, Holmström KO (2007) Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol 64:371–386

    Article  PubMed  CAS  Google Scholar 

  • Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via post-translational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102:11118–11123

    Article  PubMed  CAS  Google Scholar 

  • Leyman B, Van Dijck P, Thevelein JM (2001) An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends Plant Sci 6:510–513

    Article  PubMed  CAS  Google Scholar 

  • Liu MS, Chien CT, Lin TP (2008) Constitutive components and induced gene expression are involved in the desiccation tolerance of Selaginella tamariscina. Plant Cell Physiol 49:653–663

    Article  PubMed  CAS  Google Scholar 

  • López M, Herrera-Cervera JA, Lluch C, Tejera NA (2006) Trehalose metabolism in root nodules of the model legume Lotus japonicus in response to salt stress. Physiol Plant 128(4):701–709

    Article  Google Scholar 

  • López M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C (2008a) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: Nodule carbon metabolism. J Plant Physiol 165:641–650

    Article  PubMed  Google Scholar 

  • López M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA (2008b) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant 134:575–582

    Article  PubMed  Google Scholar 

  • López M, Tejera NA, Lluch C (2009) Validamycin A improves the response to salt stress of Medicago truncatula by inducing trehalose accumulation in the root nodules. J Plant Physiol 166:1218–1222

    Article  PubMed  Google Scholar 

  • Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34:550–563

    Article  CAS  Google Scholar 

  • Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R (2006) Sugar induced increases in trehalose 6-phosphate are correlated with redox activation of ADP-glucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397:139–148

    Article  PubMed  CAS  Google Scholar 

  • Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J Exp Zool 193:335–342

    Article  CAS  Google Scholar 

  • Martin MC, Diaz LA, Manzanal MB, Hardisson C (1986) Role of trehalose in the spores of Streptomyces. FEMS Microbiol Lett 35:49–54

    Article  Google Scholar 

  • Maruta K, Hattori K, Nakada T, Kubota M, Sugimoto T, Kurimoto M (1996) Cloning and sequencing of trehalose biosynthesis genes from Rhizobium sp. Biosci Biotechnol Biochem 60:717–720

    Article  PubMed  CAS  Google Scholar 

  • Miranda JA, Avonce N, Suarez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421

    Article  PubMed  CAS  Google Scholar 

  • Müller J, Boller T, Wiemken A (1995a) Effects of validamycin A, a potent trehalase inhibitor, and phytohormones on trehalose metabolism in roots and root nodules of soybean and cowpea. Planta 197:362–368

    Google Scholar 

  • Müller J, Boller T, Wiemken A (1995b) Trehalose and trehalase in plants: recent developments. Plant Sci 112: 1–9

    Article  Google Scholar 

  • Müller J, Boller T, Wiemken A (1996) Pools of non-structural carbohydrates in soybean root nodules during water stress. Physiol Plant 98:723–730

    Article  Google Scholar 

  • Müller J, Boller T, Wiemken A (1997) Trehalose affects sucrose synthase and invertase activities in soybean (Glycine max (L.) Merr.) roots. J Plant Physiol 153: 255–257

    Google Scholar 

  • Müller J, Aeschbacher RA, Wingler A, Boller T, Wiemken A (2001) Trehalose and trehalase in Arabidopsis. Plant Physiol 125:1086–1093

    Article  PubMed  Google Scholar 

  • Paiva CLA, Panek AD (1996) Biotechnological applications of the disaccharide trehalose. Biotechnol Annu Rev 2:293–314

    Article  PubMed  CAS  Google Scholar 

  • Paul M (2007) Trehalose 6-phosphate. Curr Opin Plant Biol 10:303–309

    Article  PubMed  CAS  Google Scholar 

  • Paul MJ, Pellny TK, Goddijn O (2001) Enhancing photosynthesis with sugar signals. Trends Plant Sci 6:197–200

    Article  PubMed  CAS  Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  PubMed  CAS  Google Scholar 

  • Pellny TK, Ghannoum O, Conroy JP, Schluepmann H, Smeekens S (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2:71–82

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–592

    Article  PubMed  CAS  Google Scholar 

  • Phillips DV, Wilson DO, Dougherty DE (1984) Soluble carbohydrates in legumes and nodulated nonlegumes. J Agric Food Chem 32:1289–1291

    Article  CAS  Google Scholar 

  • Pilon-Smits EAH, Terry N, Seors T, Kim H, Zayed A, Seongbin H, Van Dun K, Voogd E, Verwoerd TC, Krutwagen RW, Goddijn OJM (1998) Trehalose-producing transgenic tobacco plants show improved growth and performance under drought stress. J Plant Physiol 152:525–532

    CAS  Google Scholar 

  • Pramanik MHR, Imai R (2005) Functional identification of a trehalose-6-phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58:751–762

    Article  PubMed  CAS  Google Scholar 

  • Purvis JE, Yomano LP, Ingram LPO (2005) Enhanced trehalose production improves growth of Escherichia coli under osmotic stress. Appl Environ Microbiol 71:3761–3769

    Article  PubMed  CAS  Google Scholar 

  • Qu Q, Lee SJ, Boss W (2004) TreT, a novel trehalose glycosyltransferring synthase of the hyperthermophilic archeon Thermococcus litoralis. J Biol Chem 279: 47890–47897

    Article  PubMed  CAS  Google Scholar 

  • Ramon M, Rolland F (2007) Plant development: introducing trehalose metabolism. Trends Plant Sci 12:185–188

    Article  PubMed  CAS  Google Scholar 

  • Romero C, Bellés JM, Vayá JL, Serrano R, Culiáñez-Macià A (1997) Expresion of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293–297

    Article  PubMed  CAS  Google Scholar 

  • Ryu SI, Park CS, Cha J, Woo EJ, Lee SB (2005) A novel trehalose-synthesizing glycosyltransferase from Pyro­coccus horikoshii: molecular cloning and characterization. Biochem Biophys Res Commun 329:429–436

    Article  PubMed  CAS  Google Scholar 

  • Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441: 227–230

    Article  PubMed  CAS  Google Scholar 

  • Schellenbaum L, Müller J, Boller T, Wiemken A, Schüepp H (1998) Effects of drought on non-mycorrhizal and mycorrhizal maize: changes in the pools of non-structural carbohydrates, in the activities of invertase and trehalase, and in the pools of amino acids and imino acids. New Phytol 138:59–66

    Article  CAS  Google Scholar 

  • Schiraldi C, Di Lernia I, De Rosa M (2002) Trehalose production: exploiting novel approaches. Trends Biotechnol 20:420–425

    Article  PubMed  CAS  Google Scholar 

  • Schluepmann H, Pellny T, Van Dijken A, Smeekens S, Paul MJ (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilisation and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6849–6854

    Article  PubMed  CAS  Google Scholar 

  • Schluepmann H, Van Dijken A, Aghdasi M, Wobbes B, Paul M, Smeekens S (2004) Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose 6-phosphate accumulation. Plant Physiol 135:879–890

    Article  PubMed  CAS  Google Scholar 

  • Shima S, Matsui H, Tahara S, Imai R (2007) Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. FEBS J 274:1192–1201

    Article  PubMed  CAS  Google Scholar 

  • Shimakata T, Minatagawa Y (2000) Essential role of trehalose in the synthesis and subsequent metabolism of corynomycolic acid in Corynebacterium matruchotii. Arch Biochem Biophys 380:331–338

    Article  PubMed  CAS  Google Scholar 

  • Stiller I, Dulai S, Kondrák M, Tarnai R, Szabó L, Toldi O, Bánfalvi Z (2008) Effects of drought on water content and photosynthetic parameters in potato plants expressing the trehalose-6-phosphate synthase gene of Saccharomyces cerevisiae. Planta 227(2):299–308

    Article  PubMed  CAS  Google Scholar 

  • Streeter JG (1980) Carbohydrates in soybean nodules. Distribution of compounds in seedling during the onset of nitrogen fixation. Plant Physiol 66:471–476

    Article  PubMed  CAS  Google Scholar 

  • Streeter JG (1985) Accumulation of α,α-trehalose by Rhizobium bacteria and bacteroids. J Bacteriol 164:78–84

    PubMed  CAS  Google Scholar 

  • Streeter JG, Bhagwat A (1999) Biosynthesis of trehalose from maltooligosaccharides in Rhizobia. Can J Microbiol 45:716–721

    Article  PubMed  CAS  Google Scholar 

  • Streeter JG, Gómez ML (2006) Three enzymes for trehalose synthesis in Bradyrhizobium cultured bacteria and bacteroids from soybean nodules. Appl Environ Microbiol 72:4250–4255

    Article  PubMed  CAS  Google Scholar 

  • Suárez R, Wong A, Ramírez M, Barraza A, Orozco C, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966

    Article  PubMed  Google Scholar 

  • Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The transcriptional co-activator mbf1c is a key regulator of thermotolerance in Arabidopsis thaliana. J Biol Chem 283:9269–9275

    Article  PubMed  CAS  Google Scholar 

  • Van Dijken AJH, Schluepmann H, Smeekens SCM (2004) Arabidopsis trehalose 6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiol 135:969–977

    Article  PubMed  Google Scholar 

  • Vogel G, Aeschbacher RA, Müller J, Boller T, Wiemken A (1998) Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant J 13:673–683

    Article  PubMed  CAS  Google Scholar 

  • Vogel G, Fiehn O, Jean-Richard L, Boller T, Wiemken A (2001) Trehalose metabolism of Arabidopsis: occurrence of trehalose and molecular cloning and characterisation of trehalose 6-phosphate synthase homologues. J Exp Bot 52:1817–1826

    Article  PubMed  CAS  Google Scholar 

  • Wannet WJB, Op den Camp HJM, Wisselink HW, Van der Drift C, Van Griensven LJLD, Vogels GD (1998) Purification and characterization of trehalose phosphorylase from the commercial mushroom Agaricus bisporus. Biochim Biophys Acta 1425: 177–188

    Article  PubMed  CAS  Google Scholar 

  • Wingler A, Fritzius T, Wiemken A, Boller T, Aeschbacher A (2000) Trehalose induces the ADP-glucose pyrophosphorylase gene and starch synthesis in Arabidopsis. Plant Physiol 124:105–114

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Departamento de Fisiología Vegetal, Facultad de Ciencias, Universidad de Granada, Campus de Fuentenueva s/n, Granada, 18071, Spain

    Miguel López-Gómez & Carmen Lluch

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  1. Miguel López-Gómez
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  2. Carmen Lluch
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Correspondence to Miguel López-Gómez .

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Editors and Affiliations

  1. , Botany, University of Kashmir, Srinagar, 190008, India

    Parvaiz Ahmad

  2. , Department of Plant Sciences, University of Hyderabad, Andhra Pradesh, Hyderabad, 500046, India

    M.N.V. Prasad

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López-Gómez, M., Lluch, C. (2012). Trehalose and Abiotic Stress Tolerance. In: Ahmad, P., Prasad, M. (eds) Abiotic Stress Responses in Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0634-1_14

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