Skip to main content
Log in

Saccharomyces cerevisiae gene TPS1 improves drought tolerance in Zea mays L. by increasing the expression of SDD1 and reducing stomatal density

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–1497

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  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  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    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 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    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 

  • 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhu L, Yu Z, Zou C, Li Q (2010) Plant stress-inducible promoters and their function. Hereditas 32:229–234

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Degang Zhao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0647-5

Keywords

Navigation