Skip to main content
SpringerLink
Log in

Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The MSC16 cucumber (Cucumis sativus L.) mutant with lower activity of mitochondrial Complex I was used to study the influence of mitochondrial metabolism on whole cell energy and redox state. Mutant plants had lower content of adenylates and NADP(H) whereas the NAD(H) pool was similar as in wild type. Subcellular compartmentation of adenylates and pyridine nucleotides were studied using the method of rapid fractionation of protoplasts. The data obtained demonstrate that dysfunction of mitochondrial respiratory chain decreased the chloroplastic ATP pool. No differences in NAD(H) pools in subcellular fractions of mutated plants were observed; however, the cytosolic fraction was highly reduced whereas the mitochondrial fraction was more oxidized in MSC16, as compared to WTc. The NADP(H) pool in MSC16 protoplasts was greatly decreased and the chloroplastic NADP(H) pool was more reduced, whereas the extrachloroplastic pool was much more oxidized, than in WTc protoplast. Changes in nucleotides distribution in cucumber MSC16 mutant were compared to changes found in tobacco (Nicotiana sylvestris) CMS II mitochondrial mutant. In contrast to MSC16 cucumber, the content of adenylates in tobacco mutant was much higher than in tobacco wild type. The differences were more pronounced in leaf tissue collected after darkness than in the middle of the photoperiod. Results obtained after tobacco protoplast fractionating showed that the increase in CMS II adenylate content was mainly due to a higher level in extrachloroplast fraction. Both mutations have a negative effect on plant growth through perturbation of chloroplast/mitochondrial interactions.

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

Similar content being viewed by others

Abbreviations

CMS:

Cytoplasmic male sterile

MSC16:

Mosaic cucumber mutant

NADP-TPD:

NADP-triose phosphate dehydrogenase

WTc:

Cucumber wild type

WTt:

Tobacco wild type

References

  • Bartoszewski G, Malepszy S, Havey MJ (2004) Mosaic (MSC) cucumbers regenerated from independent cell cultures possess different mitochondrial rearrangements. Curr Genet 45:45–53

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bykova NV, Keerberg O, Pärnik T, Bauwe H, Gardeström P (2005) Interaction between photorespiration and respiration in transgenic plants with antisense reduction in glycine decarboxylase. Planta 222:130–140

    Article  PubMed  CAS  Google Scholar 

  • Douce R, Neuburger M (1999) Biochemical dissection of photorespiration. Curr Opin Plant Cell 2:214–222

    Article  CAS  Google Scholar 

  • Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer C, Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131:264–275

    Article  PubMed  CAS  Google Scholar 

  • Dutilleul C, Lelerge C, Prioul JL, De Paepe R, Foyer CH, Noctor G (2005) Mitochondria-driven changes in leaf NAD status exert a crucial influence on the control of nitrate assimilation and the integration of carbon and nitrogen metabolism. Plant Physiol 139:64–78

    Article  PubMed  CAS  Google Scholar 

  • Gardeström P, Wigge B (1988) Influence of photorespiration on ATP/ADP ratios in the chloroplast, mitochondria and cytosol, studied by rapid fractionation of barley (Hordeum vulgare) protoplasts. Plant Physiol 88:69–76

    Article  PubMed  Google Scholar 

  • Gardeström P, Igamberdiev AU, Raghavendra AS (2002) Mitochondrial functions in the light and significance to carbon-nitrogen interactions. In: Foyer CH, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in photosynthesis, vol 12. Kluwer, Dordrecht, pp 151–172

    Google Scholar 

  • Gu J, Miles D, Newton KJ (1993) Analysis of leaf sectors in NCS6 mitochondrial mutant of maize. Plant Cell 5:963–971

    Article  PubMed  CAS  Google Scholar 

  • Gutierres S, Sabar M, Lelandais C, Chétrit P, Diolez P, Degand H, Boutry M, Vedel F, De Kouchkovsky Y, De Paepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 94:3436–3441

    Article  PubMed  CAS  Google Scholar 

  • Hayashi M, Takahashi H, Tamura K, Huang J, Yu LH, Kawai-Yamada M, Tezuka T, Uchimiya H (2005) Enhanced dihydroflavonol-4-reductase activity and NAD homeostasis leading to cell death tolerance in transgenic rice. Proc Natl Acad Sci USA 102:7020–7025

    Article  PubMed  CAS  Google Scholar 

  • Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim Biophys Acta 1366:235–255

    Article  CAS  Google Scholar 

  • Igamberdiev AU, Gardeström P (2003) Regulation of NAD- and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochim Biophys Acta 1606:117–125

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Bykova NV, Lea PJ, Gardeström P (2001a) The role of photorespiration in redox and energy balance of photosynthetic plant cells: a study with a barley mutant deficient in glycine decarboxylase. Physiol Plant 111:427–438

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Romanowska E, Gardeström P (2001b) Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions. J Plant Physiol 158:1325–1332

    Article  CAS  Google Scholar 

  • Jiao S, Thornsberry JM, Elthon TE, Newton KJ (2005) Biochemical and molecular characterization of photosystem I deficiency in NCS6 mitochondrial mutant of maize. Plant Mol Biol 57:303–313

    Article  PubMed  CAS  Google Scholar 

  • Juszczuk IM, Rychter AM (1997) Changes in pyridine nucleotide levels in leaves and roots of bean plants (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 151:399–404

    CAS  Google Scholar 

  • Juszczuk IM, Flexas J, Szal B, Dąbrowska Z, Ribas-Carbo M, Rychter AM (2007) Effect of mitochondrial genome rearrangement on photosynthesis, photorespiration, respiratory activity and energy status of MSC16 cucumber (Cucumis sativus L.) mutant. Physiol Plant. doi:10.1111/j.1399–3054.2007.00984.x

  • Karpova OV, Newton KJ (1999) A partially assembled complex I in NAD4-deficient mitochondria of maize. Plant J 17:511–521

    Article  CAS  Google Scholar 

  • Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential expression of alternative oxidase genes in maize mitochondrial mutants. Plant Cell 14:3271–3284

    Article  PubMed  CAS  Google Scholar 

  • Krömer S (1995) Respiration during photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 46:45–70

    Article  Google Scholar 

  • Krömer S, Heldt HW (1991) Respiration of pea leaf mitochondria and redox transfer between the mitochondrial and extramitochondrial compartment. Biochim Biophys Acta 1057:42–50

    Article  Google Scholar 

  • Lechevallier D, Vermeersch J, Moneger R (1977) Microanalyse du NADP+ et du NAD+ réduits et oxydés dans les tissues foliaires et dans les plastes isols de Spirodéle et de Blé. 2. Méthode d’analyse des nucléotides pyridiniques de tissus végétaux. Physiol Veg 15:63–93

    CAS  Google Scholar 

  • Lilly JW, Bartoszewski G, Malepszy S, Havey MJ (2001) A major deletion in the cucumber mitochondrial genome sorts with the MSC phenotype. Curr Genet 40:144–151

    Article  PubMed  CAS  Google Scholar 

  • Malepszy S, Burza W, Śmiech M (1996) Characterization of a cucumber (Cucumis sativus L.) somaclonal variant with paternal inheritance. J Appl Genet 37:65–78

    Google Scholar 

  • Marienfeld JR, Newton KJ (1994) The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics 138:855–863

    PubMed  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  Google Scholar 

  • Noctor G, Dutilleul C, De Paepe R, Foyer CH (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J Exp Bot 55:49–57

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Queval G, Gakière B (2006) NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. J Exp Bot 57:1603–1620

    Article  PubMed  CAS  Google Scholar 

  • Pla M, Mathieu C, De Paepe R, Chétrit P, Vedel F (1995) Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. Mol Gen Genet 248:79–88

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Pradet A (1967) Etude des adénosine-5’-mono-,di- et tri-phosphate dans les tissus végétaux I. Dosage enzymatique. Physiol Veg 5:209–221

    CAS  Google Scholar 

  • Priault P, Tcherkez G, Cornic G, De Paepe R, Naik R, Ghashghaie J, Streb P (2006) The lack of mitochondrial complex I in CMSII mutant of Nicotiana sylvestris increases photorespiration though an increased internal resistance to CO2 diffusion. J Exp Bot 57:3195–3207

    Article  PubMed  CAS  Google Scholar 

  • Prilaut P, Vidal G, De Paepe R, Ribas-Carbo M (2007) Leaf age-related changes in respiratory pathways are dependent on complex I activity in Nicotiana sylvestris. Physiol Plant 129:152–162

    Article  CAS  Google Scholar 

  • Raghavendra AS, Padmasree K, Saradadevi K (1994) Interdependence of photosynthesis and respiration in plant cells: interactions between chloroplasts and mitochondria. Plant Sci 97:1–14

    Article  CAS  Google Scholar 

  • Roussell DL, Thompson DL, Pallady SG, Miles D, Newton KJ (1991) Chloroplast structure and function is altered in NCS2 maize mitochondrial mutant. Plant Physiol 96:232–238

    PubMed  CAS  Google Scholar 

  • Sabar M, De Paepe R, de Kouchkovsky Y (2000) Complex I impairment, respiratory compensation and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol 124:1239–1249

    Article  PubMed  CAS  Google Scholar 

  • Wagner AM, Moore AL (1997) Structure and function of the plant alternative oxidase: its putative role in the oxygen defence mechanism. Biosci Rep 17:319–333

    Article  PubMed  CAS  Google Scholar 

  • Wigge B, Krömer S, Gardeström P (1993) Estimation of the red/ox level of subcellular pyridine nucleotide pools in barley protoplasts. Physiol Plant 88:10–18

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grant from the Nordic Academy of Advanced Studies (NorFA) given to P.G. and a grant from the Polish Ministry of Scientific Research and Information Technology (MNII), Grant 2 P04C 099 27, given to A.M.R.

Author information

Authors and Affiliations

  1. Institute of Experimental Plant Biology, University of Warsaw, Miecznikowa 1, 02-096, Warsaw, Poland

    Bożena Szal, Zofia Dąbrowska & Anna M. Rychter

  2. Umea Plant Science Center, Umea University, 901 87, Umea, Sweden

    Gunilla Malmberg & Per Gardeström

Authors
  1. Bożena Szal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zofia Dąbrowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gunilla Malmberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Per Gardeström
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna M. Rychter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bożena Szal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Szal, B., Dąbrowska, Z., Malmberg, G. et al. Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement. Planta 227, 697–706 (2008). https://doi.org/10.1007/s00425-007-0652-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0652-6

Keywords

Search

Navigation