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Transgenic Plants Overexpressing Trehalose Biosynthetic Genes and Abiotic Stress Tolerance in Plants

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Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants
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Abstract

Trehalose, a non-reducing disaccharide consisting of two glucose molecules, has been proposed to play protective role under various abiotic stresses. This protective molecule, however, does not seem to accumulate in sufficient amounts in plants. Therefore, the plants thought to be genetically modified to over-accumulate trehalose, which in turn can provide abiotic stress tolerance to the targeted plant. Numerous such transgenic plants have been raised from various species and tested for cold, heat, salt, and drought tolerance. The first attempts of genetic modification of the trehalose biosynthesis pathway were carried out in tobacco and potato. The modifications involved the introduction of bacterial or yeast genes that encoded the enzymes trehalose-phosphate synthase for trehalose synthesis via trehalose-phosphate. These transgenic plants exhibited higher resistance to stress and an unexpectedly wide range of phenotypic abnormalities indicating the role of trehalose metabolism in the growth and development of plants. Since then, several approaches have been used to enhance drought resistance and to avoid the undesirable morphological effects associated with constitutive expression of the microbial genes. These approaches are summarised in this chapter.

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References

  • Antal F, Kondrák M, Kovács G, Bánfalvi Z (2013) Influence of the StubSNF1 kinase complex and the expression of the yeast TPS1 gene on growth and tuber yield in potato. Plant Growth Regul 69:51–61

    Article  CAS  Google Scholar 

  • Almeida AM, Santos M, Villalobos E, Araujo SS, van Dijck P, Leyman B, Cardoso LA, Santos D, Fevereiro PS, Torne JM (2007a) Immunogold localization of trehalose-6-phosphate synthase in leaf segments of wild-type and transgenic tobacco plants expressing the AtTPS1 gene from Arabidopsis thaliana. Protoplasma 230:41–49

    Article  CAS  PubMed  Google Scholar 

  • Almeida AM, Silva AB, Araujo SS, Cardoso LA, Santos DM, Torne JM, Silva JM, Paul MJ, Fevereiro PS (2007b) 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 

  • Almeida AM, Villalobos E, Araujo SS, Leyman B, Van Dijck P, Alfaro-Cardoso L, Fevereiro PS, Torne JM, Santos DM (2005) Transformation of tobacco with an Arabidopsis thaliana gene involved in trehalose biosynthesis increases tolerance to several abiotic stresses. Euphytica 146:165–176

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Bledsoe SW, Henry C, Griffiths CA, Paul MJ, Feil R, Lunn JE, Stitt M, Lagrimini LM (2017) The role of Tre6P and SnRK1 in maize early kernel development and events leading to stress induced kernel abortion. BMC Plant Biol 17:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95

    Article  CAS  PubMed  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abioticstress by metabolic engineering of betaines and other compatiblesolutes. Curr Opin Plant Biol 5:250–257

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Drennan PM, Smith MT, Goldsworth D, van Staden J (1993) The occurrence of trehalose in the leaves of the desiccation tolerant angiosperm Myrothamnus flabellifolia welw. J Plant Physiol 142:493–496

    Article  CAS  Google Scholar 

  • Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhães R (2015) Revisiting yeast trehalose metabolism. Curr Genet 61:263–274

    Article  CAS  PubMed  Google Scholar 

  • Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN (2015) Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation. Biol Rev Camb Philos Soc 90:1065–1099

    Article  PubMed  Google Scholar 

  • Gaff D (1996) Tobacco-plant desiccation tolerance. Nature 382:502

    Article  CAS  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX (2008) Overexpression of thetrehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228:191–201

    Article  CAS  PubMed  Google Scholar 

  • Giaever HM, Styrvold OB, Kaasen I, Strom AR (1988) Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol 170:2841–2849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han B, Fu L, Zhang D, He X, Chen Q, Peng M, Zhang J (2016) Interspecies and intraspecies analysis of trehalose contents and the biosynthesis pathway gene family reveals crucial roles of trehalose in osmotic-stress tolerance in cassava. Int J Mol Sci 17:E1077

    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 Pleurotussajor caju. Plant Cell Tissue Organ Cult 82:151–158

    Article  CAS  Google Scholar 

  • Holmström KO, Mantyla E, Welin B, Mandal A, Palva ET, Tunnela OE, Londesborough J (1996) Drought tolerance in tobacco. Nature 379:683–684

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Islam MO, Kato H, Shima S, Tezuka D, Matsui H, Imai R (2019) Functional identification of a rice trehalase gene involved in salt stress tolerance. Gene 685:42–49

    Article  CAS  PubMed  Google Scholar 

  • Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, Kim YS, SeoHS CYD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase intransgenic rice plants increases trehalose accumulation andabiotic stress tolerance without stunting growth. Plant Physiol 131:516–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joo J, Choi HJ, Lee YH, Lee S, Lee CH, Kim CH, Cheong JJ, Do Choi Y, Song SI (2014) Over-expression of BvMTSH, a fusion gene for maltooligosyltrehalose synthase and maltooligosyltrehalosetrehalohydrolase, enhances drought tolerance in transgenic rice. BMB Rep 47:27–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jun SS, Yang JY, Choi HY, Kim NR, Park MC, Hong YN (2005) Altered physiology in trehalose-producing transgenic tobacco plants: enhanced tolerance to drought and salinity stresses. J Plant Biol 48:456–466

    Article  CAS  Google Scholar 

  • Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mäntylä E, Palva ET, 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  CAS  PubMed  Google Scholar 

  • 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 Biol 12:74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kondrák M, Marincs F, Kalapos B, Juhász Z, Bánfalvi Z (2011) Transcriptome analysis of potato leaves expressing the trehalose-6-phosphate synthase 1 gene of yeast. PLoS One 6:e23466

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kwon SJ, Hwang EW, Kwon HB (2004) Genetic engineering of drought resistant potato plants by co-introduction of genes encoding trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase of Zygosaccharomyces rouxii. Korean J Genetic 26:199–206

    CAS  Google Scholar 

  • Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun M-O, Daniell H (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11:1–13

    Article  CAS  Google Scholar 

  • Li HW, Zang BS, Deng XW, Wang XP (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018

    Article  CAS  PubMed  Google Scholar 

  • Liu YB, Han LZ, Qin LJ, Zhao DG (2015) Saccharomyces cerevisiae gene TPS1 improves drought tolerance in Zea mays L. by increasing the expression of SDD1 and reducing stomatal density. Plant Cell Tissue Organ Cult 120:779–789

    Article  CAS  Google Scholar 

  • Lyu JI, Min SR, Lee JH, Lim YH, Kim J-K, Bae C-H, Liu JR (2013) Overexpression of a trehalose-6-phosphate synthase/phosphatase fusion gene enhances tolerance and photosynthesis during drought and salt stress without growth aberrations in tomato. Plant Cell Tissue Organ Cult 112:257–262

    Article  CAS  Google Scholar 

  • Lyu JI, Park JH, Kim JK, Bae CH, Jeong WJ, Min SR, Liu JR (2018) Enhanced tolerance to heat stress in transgenic tomato seeds and seedlings overexpressing a trehalose-6-phosphate synthase/phosphatase fusion gene. Plant Biotechnol Rep 12:399–408

    Article  Google Scholar 

  • Martins LL, Mourato MP, Baptista S, Reis R, Carvalheiro F, Almeida AM, Fevereiro P, Cuypers A (2014) Response to oxidative stress induced by cadmium and copper in tobacco plants (Nicotiana tabacum) engineered with the trehalose-6-phosphate synthase gene (AtTPS1). Acta Physiol Plant 36:755–765

    Article  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  CAS  PubMed  Google Scholar 

  • Nuccio ML, Wu J, Mowers R, Zhou HP, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, Basu SS, Lagrimini LM (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nature Biotechnol 33:862–869

    Article  CAS  Google Scholar 

  • Oszvald M, Primavesi LF, Griffiths CA, Cohn J, Basu SS, Nucio ML, Paul MJ (2018) Trehalose 6-phosphate in maize reproductive tissue regulates assimilate partitioning and photosynthesis. Plant Physiol 176:2623–2638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park SH, Jun SS, An G, Hong YN, Park MC (2003) A comparative study on the protective role of trehalose and LEA proteins against abiotic stresses in transgenic Chinese cabbage (Brassica campestris) overexpressing CaLEA or OtsA. J Plant Biol 46:277–286

    Article  CAS  Google Scholar 

  • Paul MJ, Gonzalez-Uriarte A, Griffiths CA, Hassani-Pak K (2018) The role of trehalose 6-phosphate in crop yield and resilience. Plant Physiol 177:12–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petitjean M, Teste M-A, François JM, Parrou J-L (2015) Yeast trehalose-6P tolerance to various stresses relies on the synthase (Tps1) protein, not on trehalose. J Biol Chem 290:16177–16190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petitjean M, Teste MA, Leger-Silvestre FJM, Parrou JL (2016) Anew function for the yeast trehalose-6P synthase (Tps1) protein as key pro-survival factor during growth, chronological ageing and apoptotic stress. Mech Ageing Dev 161:234–246

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Romero C, Belles JM, Vaya JL, Serrano R, Culianez-Macia FA (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293–297

    Article  CAS  PubMed  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 227:299–308

    Article  CAS  PubMed  Google Scholar 

  • Suprasanna P, Nikalje G, Rai AN (2016) Osmolyte accumulation and implications in plant abiotic stress tolerance. In: Iqbal N, Khan NA, Nazar R (eds) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, New Delhi, pp 1–12

    Google Scholar 

  • Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M et al (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60:796–804

    Article  CAS  PubMed  Google Scholar 

  • Yeo ET, Kwon HB, Han SE, Lee JT, Ryu JC, Byun MO (2000) Genetic engineering of drought resistant potato plants by introduction of the trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells 10:263–268

    CAS  PubMed  Google Scholar 

  • Van Houtte H, Vandesteene L, Lopez-Galvis L, Lemmens L, Kissel E, Carpentier SC, Feil R, Avonce N, Beeckman T, Lunn JE, Van Dijck P (2013) Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in ABA-induced stomatal closure. Plant Physiol 161:1158–1171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vishal B, Krishnamurthy P, Ramamoorthy R, Kumar PP (2019) OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition. New Phytol 221:1369–1386

    Article  CAS  PubMed  Google Scholar 

  • Wang CL, Zhang SC, Qi SD, Zheng CC, Wu CA (2016) Delayed germination of Arabidopsis seeds under chilling stress by overexpressing an abiotic stress inducible GhTPS11. Gene 575:206–212

    Article  CAS  PubMed  Google Scholar 

  • Williams B, Njaci I, MoghaddamL LH, Dickman MB, Zhang X, Mundree S (2015) Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet 11:e1005705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wurzinger B, Nukarinen E, Nägele T, Weckwerth W, Teige M (2018) The SnRK1 kinase as central mediator of energy signaling between different organelles. Plant Physiol 176:1085–1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of Snf1-related protein kinase (SnRK1) activity and regulation of metabolic pathways by trehalose 6-phosphate. Plant Physiol 149:1860–1871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SZ, Yang BP, Feng CL, Tang HL (2005) Genetic transformation of tobacco with the trehalose synthase gene from Grifola frondosa Fr. enhances the resistance to drought and salt in tobacco. J Integr Plant Biol 47:579–587

    Article  CAS  Google Scholar 

  • Zhao HW, Chen YJ, Hu YL, Gao Y, Lin ZP (2000) Construction of a trehalose-6-phosphate synthase gene driven by drought-responsive promoter and expression of drought-resistance in transgenic tobacco. Acta Bot Sin 42:616–619

    CAS  Google Scholar 

  • Zhao F, Li QY, Weng ML, Wang XL, Guo BT, Wang L, Wang W, Duan DL, Wang B (2013) Cloning of TPS gene from eelgrass species Zostera marina and its functional identification by genetic transformation in rice. Gene 531:205–211

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Zsófia Bánfalvi .

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Bánfalvi, Z. (2019). Transgenic Plants Overexpressing Trehalose Biosynthetic Genes and Abiotic Stress Tolerance in Plants. In: Hossain, M., Kumar, V., Burritt, D., Fujita, M., Mäkelä, P. (eds) Osmoprotectant-Mediated Abiotic Stress Tolerance in Plants. Springer, Cham. https://doi.org/10.1007/978-3-030-27423-8_10

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