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Oxidative stress induced in tobacco leaves by chloroplast over-expression of maize plastidial transglutaminase

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An Erratum to this article was published on 22 June 2010

Abstract

As part of a project aiming to characterize the role of maize plastidial transglutaminase (chlTGZ) in the plant chloroplast, this paper presents results on stress induced by continuous chlTGZ over-expression in transplastomic tobacco leaves. Thylakoid remodelling induced by chlTGZ over-expression in young leaves of tobacco chloroplasts has already been reported (Ioannidis et al. in Biochem Biophys Acta 1787:1215–1222, 2009). In the present work, we determined the induced alterations in the photosynthetic apparatus, in the chloroplast ultrastructure, and, particularly, the activation of oxidative and antioxidative metabolism pathways, regarding ageing and functionality of the tobacco transformed plants. The results revealed that photochemistry impairment and oxidative stress increased with transplastomic leaf age. The decrease in pigment levels in the transformed leaves was accompanied by an increase in H2O2 and lipid peroxidation. The rise in H2O2 correlated with a decrease in catalase activity, whereas there was an increase in peroxidase activity. In addition, chlTGZ over-expression lead to a drop in reduced glutathione, while Fe-superoxide dismutase activity was higher in transformed than in wild-type leaves. Together with the induced oxidative stress, the over-expressed chlTGZ protein accumulated progressively in chloroplast inclusion bodies. These traits were accompanied by thylakoid scattering, membrane degradation and reduction of thylakoid interconnections. Consequently, the electron transport between photosystems decrease in the old leaves. In spite of these alterations, transplastomic plants can be maintained and reproduced in vitro. These results are discussed in line with chlTGZ involvement in chloroplast functionality.

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Abbreviations

ΦPSII :

Quantum yield of PSII

Fv/Fm:

Maximum quantum yield of PSII

qP:

Photochemical quenching

\( F^{\prime}_{\text{v}} /F^{\prime}_{\text{m}} \) :

Intrinsic efficiency of open PSII centres

NPQ:

Non-photochemical quenching

ETR:

Relative rate of electron transport

PPFD:

Photosynthetic photon flux density

ASC–GSH cycle:

Ascorbate–glutathione cycle

APX:

Ascorbate peroxidase

CAT:

Catalase

DHAR:

Dehydroascorbate reductase

G6PDH:

Glucose-6-phosphate dehydrogenase

GPX:

Glutathione peroxidase

GR:

Glutathione reductase

GSH:

Glutathione reduced form

GSSG:

Glutathione oxidized form

GST:

Glutathione-S-transferase

MDHAR:

Monodehydroascorbate reductase

NADH-POX:

NADH-peroxidase

POX:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

Chl:

Chlorophyll

IBs:

Inclusion bodies

PG:

Pale green leaves

TGase:

Transglutaminase

TGZ:

Maize transglutaminase

Y:

Yellow leaves

W:

White leaves

Wt:

Wild type

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Acknowledgments

This study was supported by the Spanish projects MEC BFU2006-15115-01/BMC, BIO2005-00155 and AGL2006-07143/AGR. S.M. Ortigosa was the recipient of a predoctoral fellowship from CSIC. M.J. Clemente-Moreno thanks the Spanish Ministry of Science and Education for the FPI research fellowship. P. Diaz-Vivanco thanks the Séneca Foundation (Region of Murcia) for his post-doctoral research fellowship. We thank N. Cortadellas, E. Fernandez and A. García (Serveis Cientifico-Tècnics, UB) for their technical assistance and Shirley Burgess for English corrections. We also thank CERBA (Generalitat de Catalunya) for partial financial support.

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Authors and Affiliations

  1. Instituto de Agrobiotecnología, Universidad Pública de Navarra-CSIC-Gobierno de Navarra, Campus Arrosadía, 31006, Pamplona, Spain

    Susana M. Ortigosa & Jon Veramendi

  2. Group of Fruit Biotechnology, Department of Plant Breeding, CEBAS-CSIC, 301000, Espinardo-Murcia, Spain

    Pedro Díaz-Vivancos, María José Clemente-Moreno & José Antonio Hernandez

  3. Departament de Fisiología Vegetal, Facultad de Biología, Universitat de Barcelona, Diagonal, 08034, Barcelona, Spain

    Marta Pintó-Marijuan & Isabel Fleck

  4. Molecular Genetics Department, Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB, Jordi Girona 18-26, 08034, Barcelona, Spain

    Mireya Santos & José M. Torné

Authors
  1. Susana M. Ortigosa
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  2. Pedro Díaz-Vivancos
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  3. María José Clemente-Moreno
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  4. Marta Pintó-Marijuan
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  6. Jon Veramendi
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  7. Mireya Santos
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  8. José Antonio Hernandez
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  9. José M. Torné
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Corresponding author

Correspondence to José M. Torné.

Additional information

S. M. Ortigosa and P. Díaz-Vivancos contributed equally to this work.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00425-010-1210-1

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Ortigosa, S.M., Díaz-Vivancos, P., Clemente-Moreno, M.J. et al. Oxidative stress induced in tobacco leaves by chloroplast over-expression of maize plastidial transglutaminase. Planta 232, 593–605 (2010). https://doi.org/10.1007/s00425-010-1185-y

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