Skip to main content
SpringerLink
Log in

Effects of ectopically expressed hyperthermophilic archaeon (Pyrococcus furiosus) ribulose-1,5-bisphosphate carboxylase/oxygenase on tobacco photosynthesis

  • Published:
Photosynthetica

Abstract

Pyrococcus furiosus is a hyperthermophilic archaeon. Its ribulose-1,5-bisphosphate carboxylase/oxygenase (PfRubisco) has only large subunit (L). PfRubisco has a novel (L2)5, decameric structure and it possesses higher carboxylase activity and thermotolerance. To assess the potential functionality of PfRubisco in higher plants under high-temperature stress, PfRubisco coding sequence was transiently expressed in Nicotiana benthamiana by Pea early browning virus mediated ectopic expression. The transgenic PfRubisco plants produced chlorotic yellow stripes in their leaves. Relative to the control leaves, those with yellow stripes exhibited decreased net photosynthetic rate and chlorophyll content, altered chloroplast ultrastructure, and more severe photoinhibition of both photosystem I and II. We concluded that the ectopic expression of PfRubisco might disrupt the chloroplast development and function in N. benthamiana. The potential cause of the disruption was 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

Similar content being viewed by others

Abbreviations

Chl:

chlorophyll

C i :

intercellular CO2 concentration

CK:

noninoculated plants as a control

Fm :

maximum yield of chlorophyll fluorescence in dark adapted state

Fv :

variable fluorescence

Fv/Fm :

maximal photochemical efficiency of PSII

GFP:

green fluorescent protein

g s :

stomatal conductance

L:

large subunit

NbTp :

Nicotiana benthamiana ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit transit peptide gene

NPQ:

nonphotochemical quenching

P N :

net photosynthetic rate

PS:

photosystem

qRT-PCR:

quantitative reverse transcription-polymerase chain reaction

rbcL:

large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase

rbcS:

small subunit of Rubisco

RT-PCR:

reverse transcription-polymerase chain reaction

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

ribulose-1,5-bisphosphate

S:

small subunit

T:

inoculated, transgenic PfRubisco plants

VMEE:

virus mediated ectopic expression

References

  • An, X., Yu, C., Wang, D.: Assessment of plant gene functions using viral vectors. — In: Wang, A. (ed.): Principles and Practice of Advanced Technology in Plant Virology. Pp. 311–330. Kerala, India 2010.

    Google Scholar 

  • Ashida, H., Saito, Y., Nakano, T. et al.: RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO. — J. Exp. Bot. 59: 1543–1554, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Atomi, H.: Microbial enzymes involved in carbon dioxide fixation. — J. Biosci. Bioeng. 94: 497–505, 2002.

    PubMed  CAS  Google Scholar 

  • Atomi, H., Ezaki, S., Imanaka, T.: Ribulose-1,5-bisphosphate carboxylase/oxygenase from Thermococcus kodakaraensis KODl. — Methods Enzymol. 331: 353–365, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Brisson, N., Paszkowski, J., Penswick, J.R. et al.: Expression of a bacterial gene in plants by using a viral vector. — Nature 310: 511–514, 1984.

    Article  CAS  Google Scholar 

  • Ekengren, S.K., Liu, Y., Schiff, M. et al.: Two MAPK cascades, NPR1, and TGA transcription factors play a role in Ptomediated disease resistance in tomato. — Plant J. 36: 905–917, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Ezaki, S., Maeda, N., Kishimoto, T. et al.: Presence of a structurally novel type ribulose-bisphosphate carboxylase/oxygenase in the hyperthermophilic archaeon, Pyrococcus kodakaraensis KOD1. — J. Biol. Chem. 274: 5078–5082, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Farquhar, G.D., Sharkey, T.D.: Stomatal conductance and photosynthesis. — Ann. Rev. Plant Physiol. 33: 317–345, 1982.

    Article  CAS  Google Scholar 

  • Finn, M.W., Tabita, F.R.: Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. — J. Bacteriol. 185: 3049–3059, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Kanevski, I., Maliga, P., Rhoades, D.F., Gutteridge, S.: Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. — Plant Physiol. 119: 133–141, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Kitano, K., Maeda, N., Fukui, T., Atomi, H., Imanaka, T., Miki, K.: Crystal structure of a novel-type archaeal Rubisco with pentagonal symmetry. — Structure 9: 473–481, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, A., Li, C., Portis Jr., A.R.: Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. — Photosynth. Res. 100: 143–153, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Larcher, W.: Physiological Plant Ecology, 4th Ed. Springer-Verlag, Berlin, 2003.

    Book  Google Scholar 

  • Li, X.G., Duan, W., Meng, Q.W. et al.: The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. — Plant Cell Physiol. 45: 103–108, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Schiff, M., Dinesh-Kumar, S.P.: Virus-induced gene silencing in tomato. — Plant J. 31: 777–786, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC method. — Method. 25: 402–408, 2001.

    Article  CAS  Google Scholar 

  • Lobell, D.B., Field, C.B.: Global scale climate-crop yield relationships and the impacts of recent warming. — Environ. Res. Lett. 2: 014002. doi:10.1088/1748-9326/2/1/014002, 2007.

    Article  Google Scholar 

  • Maeda, N., Kanai, T., Atomi, H., Imanaka, T.: The unique pentagonal structure of an archaeal Rubisco is essential for its high thermostability. — J. Biol. Chem. 277: 31656–31662, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Quinn, P.J., Williams, W.P.: Environmentally induced changes in chloroplast membranes and their effects on photosynthetic function. — In: Barber, J., Baker, N.R. (ed.): Photosynthetic Mechanisms and the Environment. Pp. 1–47. Elsevier Science Publishers, Amsterdam 1985.

    Google Scholar 

  • Ryu, C.M., Anand, A., Lang, L., Mysore, K.S.: Agrodrench: a novel and effective agroinoculation method for virus-induced gene silencing in roots and diverse Solanaceous species. — Plant J. 40: 322–331, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Salvucci, M.E., Crafts-Brandner, S.J.: Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. — Plant Physiol. 134: 1460–1470, 2004a.

    Article  PubMed  CAS  Google Scholar 

  • Salvucci, M.E., Crafts-Brandner, S.J.: Mechanism for deactivation of Rubisco under moderate heat stress. — Physiol. Plant. 122: 513–519, 2004b.

    Article  CAS  Google Scholar 

  • Schlenker, W., Roberts, M.J.: Nonlinear temperature effects indicate severe damages to U.S. crop yields under climate change. — Proc. Natl. Acad. Sci. USA 106: 15594–15598, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Senthil-Kumar, M., Hema, R., Anand, A. et al.: A systematic study to determine the extent of gene silencing in Nicotiana benthamiana and other Solanaceae species when heterologous gene sequences are used for virus-induced gene silencing. — New Phytol. 176: 782–791, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Senthil-Kumar, M., Udayakumar, M.: High throughput virusinduced gene silencing approach to assess the functional relevance of a moisture stress-induced cDNA homologous to Lea4. — J. Exp. Bot. 57: 2291–2302, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Shah, K., Russinova, E., Gadella Jr., T.W. et al.: The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. — Gene Dev. 16: 1707–1720, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Tabita, F.R.: The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. — In: Blankenship, R.E., Madigan, M.T., Bauer, C.E. (ed.): Anoxygenic Photosynthetic Bacteria. Pp. 885–914. Kluwer Academic Publishers, Dordrecht, The Netherlands 1995.

    Google Scholar 

  • Watson, G.M.F., Tabita, F.R.: Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. — FEMS Microbiol. Lett. 146: 13–22, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Whitney, S.M., Andrews, T.J.: Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) supports photosynthesis and growth in tobacco. — Proc. Natl. Acad. Sci. USA 98: 14738–14743, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Whitney, S.M., Baldet, P., Hudson, G.S., Andrews, T.J.: Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. — Plant J. 26: 535–547, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Y.J., Yang, J.S., Guo, S.J. et al.: Over-expression of the Arabidopsis CBF1 gene improves resistance of tomato leaves to low temperature under low irradiance. — Plant Biol. 13: 362–367, 2011.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. High-Tech Research Center, Shandong Academy of Agricultural Sciences and Shandong Provincial Key Laboratory of Genetic Improvement, Ecology and Physiology of Crops, Ji’nan, 250100, China

    X. -G. Li, J. -J. Meng, F. Guo & S. -B. Wan

  2. Zhengzhou Tobacco Research Institute of China, National Tobacco Corporation, Zhengzhou, 450001, China

    J. Yang & R. Wang

  3. College of Life Sciences, Wuhan University, Wuhan, 430212, China

    X. -F. Tang

  4. The State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    H. -J. Qin & X. Liu

Authors
  1. X. -G. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. X. -F. Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. -J. Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. H. -J. Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. X. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. F. Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. S. -B. Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to X. -G. Li or S. -B. Wan.

Additional information

Acknowledgements: This research was supported by the Natural Science Foundation of Shandong Province (ZR2009DZ007, ZR2011CQ042) and the Project of Seed Industry in Shandong Province.

These authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, X.G., Yang, J., Wang, R. et al. Effects of ectopically expressed hyperthermophilic archaeon (Pyrococcus furiosus) ribulose-1,5-bisphosphate carboxylase/oxygenase on tobacco photosynthesis. Photosynthetica 51, 387–394 (2013). https://doi.org/10.1007/s11099-013-0035-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-013-0035-0

Additional key words

Search

Navigation