Skip to main content
SpringerLink
Log in

Over-expression of phosphoenolpyruvate carboxylase cDNA from C4 millet (Seteria italica) increase rice photosynthesis and yield under upland condition but not in wetland fields

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Phosphoenolpyruvate carboxylase (PEPC) catalyzes the initial fixation of CO2 in C4 plants. Under the control of the rice Rubisco small subunit promoter, cDNA of a C4 SiPPC gene cloned from Seteria italica was introduced into Japonica rice by Agrobacterium-mediated transformation. Integration of the gene was confirmed by PCR analysis. RT-PCR showed expression of the gene at the RNA level in transgenic plants, and enzyme activity measurements confirmed the increase in PEPC protein. The transformants showed improvements in both photosynthesis rate and yield only under upland field cultivation. The possible function of PEPC in rice stress tolerance is discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarie S, Miura A, Sumikura R, Tsukamoto S, Nose A, Arima S, Matsuoka M, Miyao M (2002) Overexpression of C4 PEPC caused O2-insensitive photosynthesis in transgenic rice plant. Plant Sci 162:257–265. doi:10.1016/S0168-9452(01)00572-6

    Article  CAS  Google Scholar 

  • Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Datta SK (2007) Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci 172:1204–1209. doi:10.1016/j.plantsci.2007.02.016

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Spreitzer RJ (1992) How various factors influence the CO2/O2 specificity of ribulose-1,5-biphosphate carboxylase/oxygenase. Photosynth Res 31:157–164. doi:10.1007/BF00028792

    Article  CAS  Google Scholar 

  • Cretin C, Santi S, Keryer E, Lepiniec L, Tagu D, Vidal J, Gadal P (1991) The phosphoenolpyruvate carboxylase gene family of Sorghum: promoter structures, amino acid sequences and expression of genes. Gene 99:87–94. doi:10.1016/0378-1119(91)90037-C

    Article  PubMed  CAS  Google Scholar 

  • Da Silva JM, Arrabaca MC (2004) Photosynthetic enzymes of C4 grass Seteria sphacelata under water stress: a comparison between rapid and slowly imposed water deficit. Photosynthetica 42:43–47. doi:10.1023/B:PHOT.0000040568.58103.ca

    Article  CAS  Google Scholar 

  • Dieffenbach CW, Dveksler GS (1995) PCR primer: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Ding Z-S, Zhao M, Jing Y-X, Li L-B, Kuang T-Y (2006) Efficient Agrobacterium-mediated transformation of rice by phosphomannose isomerase/mannose selection. Plant Mol Biol Rep 24:295–303. doi:10.1007/BF02913456

    Article  CAS  Google Scholar 

  • Ding Z-S, Zhao M, Jing Y-X, Li L-B, Kuang T-Y (2007) Effect of over-expression of maize PPC gene on photosynthesis in transgenic rice plants (in Chinese with English abstract). Acta Agron Sin 33:717–722. doi:CNKI:ISSN:0496-3490.0.2007-05-003

    Google Scholar 

  • Fukayama H, Hatch MD, Tamai T, Tsuchida H, Sudoh S, Furbank RT, Miyao-Tokutomi M (2003) Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants. Photosynth Res 77:227–239. doi:10.1023/A:1025861431886

    Article  PubMed  CAS  Google Scholar 

  • Furbank RT, Hatch MD, Jenkins CLD (2000) C4 photosynthesis: mechanism and regulation. In: Leegood RC, Sharkey TD, von de Caemmerer S (eds) Advances in photosynthesis, vol 9, photosynthesis: physiology and metabolism. Kluwer, Ordrecht, pp 435–457

  • Gehlen J, Panstruga R, Smets H, Merkelbach S, Kleines M, Porsch P, Fladung M, Becker I, Rademacher T, Häusler RE, Hirsch HJ (1996) Effects of altered phosphoenolpyruvate carboxylase activities on transgenic C3 plant Solanum tuberosum. Plant Mol Biol 32:831–848. doi:10.1007/BF00020481

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez MC, Sanchez R, Cejudo FJ (2003) Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings. Planta 216:985–992. doi:10.1007/s00425-002-0951-x

    PubMed  CAS  Google Scholar 

  • Häusler RE, Kleines M, Uhrig H, Hirsch HJ, Smets H (1999) Over-expression of phosphoenolpyruvate carboxylase from Corynebacterium glutamicum lowers the CO2 compensation point and enhances dark and light respiration in transgenic potato. J Exp Bot 50:1231–1242. doi:10.1093/jxb/50.336.1231

    Article  Google Scholar 

  • Hudspeth RL, Grula JW (1989) Structure and expression of the maize gene encoding the phosphoenolpyruvte carboxylse isozyme involved in C4 photosynthesis. Plant Mol Biol 12:579–589

    Article  CAS  Google Scholar 

  • Hudspeth RL, Grula JW, Dai Z, Edwards GE, Ku MSB (1992) Expression of maize phosphoenolpyruvate carboxylase in transgenic tobacco. Plant Physiol 98:458–464. doi:10.1104/pp.98.2.458

    Article  PubMed  CAS  Google Scholar 

  • Jeanneau M, Gerentes D, Foueillassar X, Zivy M, Vidal J, Toppan A, Perez P (2002) Improvement of drought tolerance in maize: towards the functional validation of the Zm-Asr1 gene and increase of water use efficiency by over-expressing C4-PEPC. Biochimie 84:1127–1135. doi:10.1016/S0300-9084(02)00024-X

    Article  PubMed  CAS  Google Scholar 

  • Jiao D, Huang X, Li X, Chi W, Kuang T, Zhang Q, Ku MSB, Cho D (2002) Photosynthetic characteristics and tolerance to photo-oxidation of transgenic rice expressing C4 photosynthesis enzymes. Photosynth Res 72:85–93. doi:10.1023/A:1016062117373

    Article  PubMed  CAS  Google Scholar 

  • Kogami H, Shono M, Koike T, Yanagisawa S, Izui K, Sentoku N, Tanifuji S, Uchimiya H, Toki S (1994) Molecualr and physiological evaluation of transgenic tobacco plants expression a maize phosphoenolpyruvate carboxylase gene under the control of the cauliflower mosaic virus 35S promoter. Transgen Res 3:287–296. doi:10.1007/BF01973588

    Article  CAS  Google Scholar 

  • Ku MSB, Agarie S, Nomura M, Fukayama H, Tsuchida H, Ono K, Hirose S, Toki S, Miyao M, Matsuoka M (1999) High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants. Nat Biotechnol 17:76–80. doi:10.1080/15421400490481188

    Article  PubMed  CAS  Google Scholar 

  • Ku MSB, Cho D, Ranade U, Hsu T-P, Li X, Jiao D-M, Ehleringer J, Miyao M, Matsuoka M (2000) Photosynthetic performance of transgenic rice plants overexpressing maize C4 photosynthesis enzymes. In: Sheehy JE, Mitchell PL, Hardy B (eds) Redesigning rice photosynthesis to increase yield. Elsevier, Amsterdam, pp 193–204 doi:10.1016/S0928-3420(00)80015-4

  • Lebouteiller B, Gousset-Dupont A, Pierre J-N, Bleton J, Tchapla A, Maucourt M, Moing A, Rolin D, Vidal J (2007) Physiological impacts of modulating phosphoenolpyruvate carboxylase levels in leaves and seeds of Arabidopsis thaliana. Plant Sci 172:265–272. doi:10.1016/j.plantsci.2006.09.008

    Article  CAS  Google Scholar 

  • Lin R-C, Ding Z-S, Li L-B, Kuang T-Y (2001) A rapid and efficient DNA minipreparation suitable for screening transgenic plants. Plant Mol Biol Rep 19:379a–379e. doi:10.1007/BF02772839

    Article  CAS  Google Scholar 

  • Matsuoka M, Furbank RT, Fukayama H, Miyao M (2001) Molecular engineering of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 52:297–314. doi:10.1146/annurev.arplant.52.1.297

    Article  PubMed  CAS  Google Scholar 

  • Rademacher T, Häusler RE, Hirsch HJ, Zhang L, Lipka V, Weier D, Kreuzaler F, Peterhänsel C (2002) An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 32:25–39. doi:10.1046/j.1365-313X.2002.01397.x

    Article  PubMed  CAS  Google Scholar 

  • Rogers SG, Horsch RB, Fraley RT (1986) Gene transfer in plants: production of transformed plants using Ti-plasmid vectors. Methods Enzymol 118:627–640

    Article  CAS  Google Scholar 

  • Rydzik E, Berry J (1996) The C4 photosynthetic phosphoenolpyruvate carboxylase from grain amaranth. Plant Physiol 110:713

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (2001) Molecular Cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

  • Sanchez R, Cehudo FJ (2003) Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiol 132:949–957. doi:10.1104/pp.102.019653

    Article  PubMed  CAS  Google Scholar 

  • Suzuki S, Murai N, Burnell JN, Arai M (2000) Changes in photosynthetic carbon flow in transgenic rice plants that express C4-type phosphoenolpyruvate carboxykinase from Urochloa panicoides. Plant Physiol 124:163–172. doi:10.1104/pp.124.1.163

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Akagi H, Kamasawa N, Osumi M, Honda H (2000) Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211:265–274. doi:10.1007/s004250000282

    Article  PubMed  CAS  Google Scholar 

  • Toki S (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol Biol Rep 15:16–21. doi:10.1007/BF02772109

    Article  CAS  Google Scholar 

  • Tsuchida H, Tamai T, Fukayama H, Agarie S, Nomura M, Onodera H, Ono K, Nishizawa Y, Lee B-H, Hirose S, Toki S, Ku MSB, Matsuoka M, Miyao M (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol 42:138–145. doi:10.1093/pcp/pce013

    Article  PubMed  CAS  Google Scholar 

  • Van Quy L, Foter C, Champigny M (1991) Effect of light and NO -3 on wheat leaf phosphoenolpyruvate carboxylase activity: evidence for covalent modulation of the C3 enzyme. Plant Physiol 97:1476–1482. doi:10.1104/pp.97.4.1476

    Article  Google Scholar 

Download references

Acknowledgments

This work was partially funded by the National Basic Research Program of China (2009CB118605).

Author information

Authors and Affiliations

  1. Institute of Crop Science, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology and Production of MOA, Beijing, 100081, China

    Zai-Song Ding, Su-Hua Huang, Bao-Yuan Zhou, Xue-Fang Sun & Ming Zhao

Authors
  1. Zai-Song Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Su-Hua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bao-Yuan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xue-Fang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ming Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ming Zhao.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ding, ZS., Huang, SH., Zhou, BY. et al. Over-expression of phosphoenolpyruvate carboxylase cDNA from C4 millet (Seteria italica) increase rice photosynthesis and yield under upland condition but not in wetland fields. Plant Biotechnol Rep 7, 155–163 (2013). https://doi.org/10.1007/s11816-012-0244-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-012-0244-1

Keywords

Search

Navigation