Abstract
Trehalose, a non-reducing disaccharide, can effectively protect the biological structures of plants from damage under stress conditions (i.e., high or low temperature, drought, and dehydration) by forming a special protective membrane on the plant-cell surface. Transformation of maize with stably expressed trehalose-6-phosphate synthase (TPS), the key enzyme of trehalose biosynthesis, to improve drought-resistance has important theoretical and economic values. In this study, we constructed the TPS1 gene expression vector driven by the rd29a promoter, transformed immature embryos using Agrobacterium-mediated methods, and screened the transgenic maize plants. As a result, trehalose accumulated in rd29a::TPS1 transgenic maize plants even though it was not detected in wild-type (WT) maize. After determination under repeated drought conditions, we found that the survival rate of the rd29a::TPS1 maize was 70 % higher than that of the WT. Photosynthetic physiological indicators of transgenic maize under drought conditions were better than those of the WT. Microscopic observations of the detached newborn leaves showed that stomata density on the leaf surface of rd29a::TPS1 transgenic maize after drought treatment was reduced by 20 % rom that on the WT leaf, while there were fewer and shorter villi on the leaf surface of transgenic maize than on the WT leaf. In addition, real-time PCR analyses showed that stomata density and distribution 1 (SDD1) expression in the rd29a::TPS1 transgenic maize increased. We concluded that TPS1 improves drought-resistance in maize not only by increasing trehalose content but also by decreasing stomata density and reducing the transpiration rate in transgenic maize plants.
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References
Almeida AM, Cardoso LA, Santos DM, Torné JM, Fevereiro PS (2007) Trehalose and its applications in plant biotechnology. In Vitro Cell Dev Biol-Plant 43:167–177
Basu SK, Dutta M, Goyal A, Bhowmik PK, Kumar J, Nandy S, Scagliusi SM, Prasad R (2010) Is genetically modified crop the answer for the next green revolution? GM crops 1:68–79
Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev 14:1119–1131
Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–1497
Bhave NS, Veley KM, Nadeau JA, Lucas JR, Bhave SL, Sack FD (2009) TOO MANY MOUTHS promotes cell fate progression in stomatal development of Arabidopsis stems. Planta 229:357–367
Cai R, Zhao Y, Wang Y, Lin Y, Peng X, Li Q, Chang Y, Jiang H, Xiang Y, Cheng B (2014) Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice. Plant Cell Tissue Org Cult 1–13
Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95
Cortina C, Culiáñez-Macià FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75–82
Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223:701–703
de Carvalho JFRP, de Carvalho CRdP, Otoni WC (2005) In vitro induction of polyploidy in annatto (Bixa orellana). Plant Cell Tissue Org Cult 80:69–75
Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R
Frame BR, Shou H, Chikwamba RK, Zhang Z, Xiang C, Fonger TM, Pegg SE, Li B, Nettleton DS, Pei D, Wang K (2002) Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiol 129:13–22
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
Han S-E, Park S-R, Kwon H-B, Yi B-Y, Lee G-B, Byun M-O (2005) Genetic engineering of drought-resistant tobacco plants by introducing the trehalose phosphorylase (TP) gene from Pleurotus sajor-caju. Plant Cell Tissue Org Cult 82:151–158
Holmstrom K-O, Mantyla E, Welin B, Mandal A, Palva ET, Tunnela OE, Londesborough J (1996) Drought tolerance in tobacco. Nature 379:683–684
Hottiger T, De Virgilio C, Hall MN, Boller T, Wiemken A (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro. Eur J Biochem 219:187–193
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Kaasen I, Falkenberg P, Styrvold OB, Strom AR (1992) Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR). J Bacteriol 174:889–898
Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116
Li S-H, Kuoh C-S, Chen Y-H, Chen H-H, Chen W-H (2005) Osmotic sucrose enhancement of single-cell embryogenesis and transformation efficiency in Oncidium. Plant Cell Tissue Org Cult 81:183–192
Lyu JI, Min SR, Lee JH, Lim YH, Kim JK, Bae CH, 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 Org 112:257–262
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
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441
Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493–500
Purohit VK, Tamta S, Chandra S, Vyas P, Palni LMS, Nandi SK (2002) In vitro multiplication of Quercus leucotrichophora and Q.glauca: important Himalayan oaks. Plant Cell Tissue Org Cult 69:121–133
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
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
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293
Stiller I, Dulai S, Kondrak M, Tarnai R, Szabo L, Toldi O, Banfalvi 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
Suarez R, Wong A, Ramirez M, Barraza A, del Orozco MC, Cevallos MA, Lara M, Hernandez 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
Tao D, Mu Y, Fu F-L, Li W-C (2008) Transformation of maize with trehalose synthase gene cloned from Saccharomyces cerevisiae. Biotechnology 7:258–265
Von Groll U, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14:1527–1539
Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73
Wang XM, Li ZG, Yan F, Khalil R, Ren ZX, Yang CW, Yang YW, Deng W (2013) ZmSKIP, a homologue of SKIP in maize, is involved in response to abiotic stress in tobacco. Plant Cell Tissue Org 112:203–216
Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440
Yan Q, Hou H, Singer SD, Yan X, Guo R, Wang X (2014) The grape VvMBF1 gene improves drought stress tolerance in transgenic Arabidopsis thaliana. Plant Cell Tissue Org 118:571–582
Yeo ET, Kwon HB, Han SE, Lee JT, Ryu JC, Byu 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
Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141
Yoshida M, Nakamura N, Horikoshi K (1998) Production of trehalose by a dual enzyme system of immobilized maltose phosphorylase and trehalose phosphorylase. Enzyme Microb Technol 22:71–75
Yun S, Jun Y, Hong S (2012) Social perception and response to the drought process: a case study of the drought during 2009–2010 in the Qianxi’nan Prefecture of Guizhou Province. Nat Hazards 64:839–851
Zhang W, Zhao Z, Bai G, Fu F (2008) Study and evaluation of drought resistance of different genotype maize inbred lines. Front Agric China 2:428–434
Zhao X, Tan HJ, Liu YB, Li XR, Chen GX (2009) Effect of salt stress on growth and osmotic regulation in thellungiella and arabidopsis callus. Plant Cell Tissue Org 98:97–103
Zhou L, He H, Liu R, Han Q, Liu B, Shou H (2014) Overexpression of GmAKT2 potassium channel enhances resistance to soybean mosaic virus. BMC Plant Biol 14:154
Zhu L, Yu Z, Zou C, Li Q (2010) Plant stress-inducible promoters and their function. Hereditas 32:229–234
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This work supported by the Genetically Breeding Major Project of the Ministry of Agriculture of China (2014ZX0801008B-002, 2014ZX08010-003) and Genetically Breeding Project of Science and Technology Agency of Guizhou Province (2004NZ004).
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Liu, Y., Han, L., Qin, L. et al. Saccharomyces cerevisiae gene TPS1 improves drought tolerance in Zea mays L. by increasing the expression of SDD1 and reducing stomatal density. Plant Cell Tiss Organ Cult 120, 779–789 (2015). https://doi.org/10.1007/s11240-014-0647-5
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DOI: https://doi.org/10.1007/s11240-014-0647-5