About the role of trehalose in plants

Tjaša GORJANC, Dominik VODNIK

Abstract


Trehalose is an important disaccharide which takes a major role of a stress protector in many organisms, including green algae and lower plants. It has long been thought that trehalose functions in higher plants are marginal and that they have been overtaken by sucrose. In the last years it has been discovered that trehalose takes on a lot of important physiological roles in vascular plants metabolism. It is an important signal metabolite of sucrose availability and maintains sucrose concentrations within an appropriate range. It also contributes to starch synthesis and degradation and to synthesis of organic acids. Trehalose-sucrose nexus was found to be very important in plant interactions with pathogenic organisms and herbivorous insects. Furthermore, trehalose is involved in response of plant to abiotic stressors such as drought, cold, salinity and hypoxia. It contributes in regulation of stomatal conductivity where it interacts with abscisic acid. All this makes trehalose an important primary metabolite which significantly influences plant growth and development such as induction of flowering and stimulation of photosynthesis.

Keywords


trehalose; sugar metabolism; sucrose; starch; stress

References


Aeschbacher R.A., Müller J., Boller T., Wiemken A. (1999). Purification of the trehalase GMTRE 1 from soybean nodules and cloning of its cDNA: GMTRE 1 is expressed at a low level in multiple tissues. Plant Physiology, 119, 489–496. doi:10.1104/pp.119.2.489

Anselmino O., Gilg E. (2013). Űber das Vorkommen von Trehalose in Selaginella lepidophylla. Berichte der Deutschen Chemischen Gesellschaft, 23, 309-320.

Blázquez M.A., Santos E., Flores C., Martinez-Zapater J.M., Salinas J., Gancedo C. (1998). Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant Journal, 13, 685-689. doi:10.1046/j.1365-313X.1998.00063.x

Brodmann D., Schuller A., Ludwig-Műller J., Aeschbacher R., Wiemken A., Boller T., Wingler A. (2002). Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicae. The American Phytopathological Society, 15, 693-700.

Chen Y., Hoehenwarter W. (2015). Changes in the phosphoproteome and metabolome link early signaling events to rearrangement of photosynthesis and central metabolism in salinity and oxidative stress response in Arabidopsis. Plant Physiology, 169, 3021-3033. doi:10.1104/pp.15.01486

Couee I., Sulmon C., Gouesbet G., El-Amrani A. (2006). Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany, 57, 449-459. doi:10.1093/jxb/erj027

Dangl J.L., Jones J.D.G. (2001). Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833. doi:10.1038/35081161

De Smet K., Weston A., Brown I., Young D., Robertson D. (2000). Three pathways for trehalose byosinthesis in mycobacteria. Microbiology, 146, 199-208. doi:10.1099/00221287-146-1-199

El-bashiti T., Hamamci H., Oktem H.A., Yucel M. (2005). Biochemical analysis of trehalose and its metabolizing anzymes in wheat under abiotic stress conditions. Plant Science, 169, 47-54. doi:10.1016/j.plantsci.2005.02.024

Elbein A.D., Pan Y.T., Pastuszak I., Carroll D. (2003). New insights on trehalose: a multifunctional molecule. Glycobiology, 13, 17R-27R. doi:10.1093/glycob/cwg047

Farooq M., Hussain M., Nawaz A., Lee D.J., Alghamdi S.S., Siddique K.H.M. (2017). Seed priming improves chilling tolerance in chickpea by modulating germination metabolism, trehalose accumulation and carbon assimilation. Plant Physiology and Biochemistry, 111, 274-283. doi:10.1016/j.plaphy.2016.12.012

Farrant J.M., Cooper K., Hilgart A., Abdalla K.O., Bentley J., Thomson J.A., Dace H.J., Penton N., Mundree S.G., Rafudeen M.S. (2015). A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta, 242, 407-426. doi:10.1007/s00425-015-2320-6

Fernandez J., Wilson R.A. (2012). Why no feeding frenzy? Mechanisms of nutrient acquisition and utilization during infection by the rice blast fungus Magnoporthe oryzae. Molecular Plant-microbe Interactions, 25, 1286-1293. doi:10.1094/MPMI-12-11-0326

Figueroa C.M., Feil R., Ishihara H., Wanatabe M., Kolling K., Krause U., Hohne M., Encke B., Plaxton W.C., Zeeman S.C., Li Z., Schulze W.X., Hoefgen R., Stitt M., Lunn J.E. (2016). Trehalose 6-phosphate coordinates organic and amino acid metabolism with carbon availability. Plant Journal, 85, 410-423. doi:10.1111/tpj.13114

Figueroa C.M., Lunn J.E. (2016). A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiology, 172, 7-27. doi:10.1104/pp.16.00417

Garg R., Shankar R., Thakkar B., Kudapa H., Krishnamurthy L., Varshney R.K., Bhatia S., Jain M. (2016). Transcritome analyses reveal genotype- and developmental stage-specific molecular responses to drought and salinity stress in chickpea. Scientific Reports, 6: 19228. doi:10.1038/srep19228

Golem S., Culver J.N. (2003). Tobacco mosaic virus induces alterations in the gene expression profile of Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 16, 681-688. doi:10.1094/MPMI.2003.16.8.681

Goméz L.D., Gildaz A., Fell R., Lunn, J.E., Graham I.A. (2010). AtTPS mediated trehalose-6-phosphate synthesis is essential for embryogenic and vegetative growth and responsiveness to ABA in germinating seeds and stomatal guard cells. Plant Journal, 64, 1-13.

Grant J.J., Loake G.J. (2000). Role of reactive oxygen intermediates and cognate redox signalling in disease resistance. Plant Physiology, 124, 21-29. doi:10.1104/pp.124.1.21

Griffiths C.A., Paul M.J., Foyer C.H. (2016). Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochimica et Biophysica Acta, 1857, 1715-1725. doi:10.1016/j.bbabio.2016.07.007

Iordachescu M., Imai R. (2008). Trehalose biosynthesis in response to abiotic stresses. Journal of Integrative Plant Biology, 50, 1223-1229. doi:10.1111/j.1744-7909.2008.00736.x

Iturriaga G., Cushman M.A.F., Cushman J.C. (2006). An EST catalogue from the resurrection plant Selaginella lepidophylla reveals abiotic stress-adaptive genes. Plant Science, 170, 1173-1184. doi:10.1016/j.plantsci.2006.02.004

Kolbe A., Tiessen A., Schluepmann H., Paul M., Ulrich S., Geigenberger P. (2005). Trehalose-6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proceedings of the National Academy of Sciences, 102, 1118-11123. doi:10.1073/pnas.0503410102

Kondrák M., Marincs F., Antal F., Juhász Z., Bánfalvi Z. (2012). Effects of yeast trehalose-6-phosphate synthase 1 on gene expression and carbohydrate contents of potato leaves under drought stress conditions. BMC Plant Biology, 12: e74, doi: 10.1186/1471-2229-12-74: 12 str.

Krasensky J., Broyart C., Rabanal F.A., Jonak C. (2014). The redox-sensitive chloroplast trehalose-6-phosphate phosphatase AtTPPD regulates salt stress tolerance. Antioxid Redox Signal, 21, 1289-1304. doi:10.1089/ars.2013.5693

Kretzschmar T., Pelayo M.A.F., Trijatmiko K.R., Gabunada L.F.M., Alam R., Jimenez R., Mendorio M.S., Slamet-Loedin I.H., Sreenivaslu N., Bailey-Serres J., Ismail A.M., Mackill D.J., Septiningsih E.M. (2015). A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants, 1, 15124. doi:10.1038/nplants.2015.124

Leyman B., van Dijck P., Thevelein J.M. (2001). An unexpected plethora of trehalose biosynthesis genes in Arabidopsis thaliana. Trends in Plant Science, 6, 510-513. doi:10.1016/S1360-1385(01)02125-2

Lunn J.E., Delorge I., Figueroa M.C., van Dijck P., Stitt M. (2014). Trehalose metabolism in plants. The Plant Journal, 79, 544-567. doi:10.1111/tpj.12509

Luo Y., Li W.M., Wang W. (2008). Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environmental and Experimental Botany, 63, 378-384. doi:10.1016/j.envexpbot.2007.11.016

Martins M.C.M, Hejazi M., Fettke J. (2013). Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose-6-phosphate. Plant Physiology, 163, 1142-1163. doi:10.1104/pp.113.226787

Mostofa M.G., Hossain M.A., Fujita M. (2015). Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma, 252, 461-475. doi:10.1007/s00709-014-0691-3

Müller J., Aeschbacher R.A., Wingler A., Boller T., Wiemken A. (2001). Trehalose and trehalase in Arabidopsis. Plant Physiology, 125, 1086–1093. doi:10.1104/pp.125.2.1086

Pramanik M.H.R. in Imai R. (2005). Functional identification of a trehalose-6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Molecular Biology, 58,751-762. doi:10.1007/s11103-005-7404-4

Shahbaz M., Abid A., Masood A., Waraich E.A. (2017). Foliar-applied trehalose modulates growth, mineral nutrition, photosynthetic ability, and oxidative defense system of rice (Oryza sativa L.) under saline stress. Journal of Plant Nutrition, 40, 584-599. doi:10.1080/01904167.2016.1263319

Singh V., Louis J., Ayre B.G., Reese J.C., Shah J. (2011). Trehalose phosphate synthase11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae. Plant Journal, 67, 94-104. doi:10.1111/j.1365-313X.2011.04583.x

Suzuki N., Bajad S., Shuman J., Shulaev V., Mitter R. (2008). The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. The Journal of Biological Chemistry, 283, 9269-9275. doi:10.1074/jbc.M709187200

Svanström A., van Leeuwen M.R., Dijksterhuis J., Melin P. (2014). Trehalose synthesis in Aspergillus niger: characterization of six homologous genes, all with conserved orthologs in related species. BMC Mikrobiology, 14, 90-106. doi:10.1186/1471-2180-14-90

Tapia H., Young L., Fox D., Bertozzi C.R., Koshland D. (2015). Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, 112, 6122-6127. doi:10.1073/pnas.1506415112

Tayeh C., Randoux B., Vincent D., Bourdon N., Reignault P., (2014). Exogenous trehalose induces defenses in wheat before and during a biotic stress caused by powdery mildew. Phytopathology, 104, 293-305. doi:10.1094/PHYTO-07-13-0191-R

Thiel J., Rolletschek H., Friedel S., Lunn J.E., Nguyen T.H., Feil R., Tschiersch H., Műller M., Borisjuk L. (2011). Seed-specific elevation of non-symbiotic hemoglobin AtHb1: beneficial effects and underlying molecular networks in Arabidopsis thaliana. BMC plant biology, 15, 11, 48. doi:10.1186/1471-2229-11-48

Van Houtte H., Vandesteene L., López-Galvis L. (2013). Overespression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiology, 161, 1158-1171. doi:10.1104/pp.112.211391

Vodnik D. 2012. Osnove fiziologije rastlin. Oddelek za agronomijo, Biotehniška fakulteta, Univerza v Ljubljani: 141 str.

Vogel G., Aeschbacher R.A., Műller J., Boller T., Wiemken A. (1998). Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of the yeast tps2 mutant. Plant Journal, 13, 673-683. doi:10.1046/j.1365-313X.1998.00064.x

Yadav P.U., Ivakov A., Feil R., Duan G., Walter D., Giavalisco P., Piques M., Carillo P., Hubberton M., Stitt M., Lunn J.E. (2014). The sucrose-trehalose-6-fosfat (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. Journal of Experimental Botany, 65, 1051-1068. doi:10.1093/jxb/ert457

Zhang H.,Hong Y., Huang L., Liu S., Tian L.,Dai Y.,Cao Z.,Huang L.,Li D., Song F.(2016). Virus-induced gene silencing-based functional analyses revealed the involvement of several putative trehalose-6-phosphate synthase/phosphatase genes in disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 in tomato. Frontiers in Plant Science, 7, 1176. doi:10.3389/fpls.2016.01176

Zhang W., Lunn J.E., Feil R., Wang Y.F., Zhao J.J., Tao H.X., Guo Y.P., Zhao Z.Y. (2017). Trehalose 6-phosphate signal is closely related to sorbitol in apple (Malus domestica Borkh. cv. Gala). Biology Open, 6, 260-268. doi:10.1242/bio.022301

Zhou B., Fang Y., Fan Y., Wang Y., Qi J., Tang C. (2017). Expressional characterization of two class I trehalose-6-phosphate synthase genes in Hevea brasiliensis (para rubber tree) suggests a role in rubber production. New Forests, 48, 513-526. doi:10.1007/s11056-017-9578-4




DOI: http://dx.doi.org/10.14720/aas.2018.111.1.21

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