Skip to main content
SpringerLink
Log in

Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances

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

Abstract

To investigate the role of plant mitochondria in drought tolerance, the response to water deprivation was compared between Nicotiana sylvestris wild type (WT) plants and the CMSII respiratory complex I mutant, which has low-efficient respiration and photosynthesis, high levels of amino acids and pyridine nucleotides, and increased antioxidant capacity. We show that the delayed decrease in relative water content after water withholding in CMSII, as compared to WT leaves, is due to a lower stomatal conductance. The stomatal index and the abscisic acid (ABA) content were unaffected in well-watered mutant leaves, but the ABA/stomatal conductance relation was altered during drought, indicating that specific factors interact with ABA signalling. Leaf hydraulic conductance was lower in mutant leaves when compared to WT leaves and the role of oxidative aquaporin gating in attaining a maximum stomatal conductance is discussed. In addition, differences in leaf metabolic status between the mutant and the WT might contribute to the low stomatal conductance, as reported for TCA cycle-deficient plants. After withholding watering, TCA cycle derived organic acids declined more in CMSII leaves than in the WT, and ATP content decreased only in the CMSII. Moreover, in contrast to the WT, total free amino acid levels declined whilst soluble protein content increased in CMSII leaves, suggesting an accelerated amino acid remobilisation. We propose that oxidative and metabolic disturbances resulting from remodelled respiration in the absence of Complex I activity could be involved in bringing about the lower stomatal and hydraulic conductances.

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
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ABA:

Abscissic acid

An:

Net CO2 assimilation by leaves

Ca, Ci, Cc, CO2 :

Molar ratios in the ambient atmosphere, the leaf intercellular air space and in the chloroplasts, respectively

CMS:

Cytoplasmic male sterile

Gs:

Stomatal conductance

GC–TOF-MS:

Gas chromatography–time of flight-mass spectrometry

HPLC:

High-performance liquid chromatography

Kl:

Leaf hydraulic conductance

NAD:

Nicotinamide adenine dinucleotide

RWC:

Relative water content

ROS:

Reactive oxygen species

RuBP:

Ribulose 1,5-bisphosphate

WT:

Wild type

Π0, ΠTLP, Π80:

Leaf osmotic potential at water saturation, turgor lost pressure (TLP) and after 5 days at a leaf relative water content (RWC) of 80%

References

  • Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597

    Article  PubMed  CAS  Google Scholar 

  • Barnett NM, Naylor AW (1966) Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol 41:1222–1230

    Article  PubMed  CAS  Google Scholar 

  • Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846

    Article  PubMed  Google Scholar 

  • Charlton AJ, Donarski JA, Harrison M, Jones SA, Godward J, Oehlschlager S, Arques JL, Ambrose M, Chinoy C, Mullineaux PM, Domoney C (2008) Responses of the pea (Pisum sativum L.) leaf metabolome to drought stress assessed by nuclear magnetic resonance spectroscopy. Metabolomics 4:312–327

    Article  CAS  Google Scholar 

  • Cochard H, Nardini H, Coll L (2004) Hydraulic architecture of leaf blades: where is the main resistance? Plant Cell Environ 27:1257–1267

    Article  Google Scholar 

  • Cochard H, Venisse J-S, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143:122–133

    Article  PubMed  CAS  Google Scholar 

  • Cornic G, Briantais J-M (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183:178–184

    Article  CAS  Google Scholar 

  • De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41:95–106

    Article  PubMed  Google Scholar 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212

    Article  PubMed  CAS  Google Scholar 

  • Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003a) Tobacco leaves require functional mitochondrial complex I for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 313:264–275

    Article  Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, De Paepe R (2003b) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226

    Article  PubMed  CAS  Google Scholar 

  • Dutilleul C, Lelarge 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 

  • Falk K, Behal RH, Xiang C, Oliver DJ (1998) Metabolic bypass of the tricarboxylic acid cycle during lipid mobilization in germinating oilseeds. Regulation of NAD+-dependent isocitrate dehydrogenase versus fumarase. Plant Physiol 117:473–481

    Article  PubMed  CAS  Google Scholar 

  • Gallé A, Florez-Sarasa I, Thameur A, De Paepe R, Flexas J, Ribas-Carbo M (2010) Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant. J Exp Bot 61:765–775

    Article  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  PubMed  CAS  Google Scholar 

  • Good AG, Zaplachinski ST (1994) The effects of drought stress on free amino acids accumulation and protein synthesis in Brassica napus. Physiol Plant 90:9–14

    Article  CAS  Google Scholar 

  • Guo FQ, Young J, Crawford NM (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117

    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 mitochondrialdeletion mutants. Proc Natl Acad Sci USA 94:3436–3441

    Article  PubMed  CAS  Google Scholar 

  • Hager J, Pellny TK, Mauve C, Lelarge-Trouverie C, De Paepe R, Foyer CH, Noctor G (2010) Conditional modulation of NAD levels and metabolite profiles in Nicotiana sylvestris by mitochondrial electron transport and carbon/nitrogen supply. Planta 231:1145–1157

    Article  PubMed  CAS  Google Scholar 

  • Hanning I, Heldt HW (1993) On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves. Partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products. Plant Physiol 103:1147–1154

    PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation in plants. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Hashida SN, Itami T, Takahashi H, Takahara K, Nagano M, Kawai-Yamada M, Shoji K, Goto F, Yoshihara T, Uchimiya H (2010) Nicotinate/nicotinamide mononucleotide adenyltransferase-mediated regulation of NAD biosynthesis protects guard cells from reactive oxygen species in ABA-mediated stomatal movement in Arabidopsis. J Exp Bot 61:3813–3825

    Article  PubMed  CAS  Google Scholar 

  • Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteillé M, Stitt M, Gibon Y, Muller B (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372

    Article  PubMed  CAS  Google Scholar 

  • Karakas B, Ozias-Akins P, Stushnoff C, Suefferheld M, Rieger M (1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant Cell Environ 20:609–616

    Article  Google Scholar 

  • Kim YX, Steudle M (2009) Gating of aquaporins by light and reactive oxygen species in leaf parenchyma cells of the midrib of Zea mays. J Exp Bot 60:547–556

    Article  PubMed  CAS  Google Scholar 

  • Kwak JM, Nguyen V, Schroeder JI (2006) Update on reactive oxygen species in hormone responses: the role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329

    Article  PubMed  CAS  Google Scholar 

  • Li XQ, Chétrit P, Mathieu C, Vedel F, De Paepe R, Rémy R, Ambard-Bretteville F (1988) Regeneration of cytoplasmic male sterile protoclones of Nicotiana sylvestris with mitochondrial variations. Curr Genet 13:261–266

    Article  CAS  Google Scholar 

  • Lu YX, Li CJ, Zhang FS (2005) Transpiration, potassium uptake and flow in tobacco as affected by nitrogen forms and nutrient levels. Ann Bot 95:991–998

    Article  PubMed  CAS  Google Scholar 

  • Magné C, Larher F (1992) High sugar content of extracts interferences with colorimetric determination of amino acids and free proline. Anal Biochem 200:115–118

    Article  PubMed  Google Scholar 

  • Meyer EH, Tomaz T, Carroll AJ, Estavillo G, Delannoy E, Tanz SK, Small ID, Pogson BJ, Millar AH (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol 151:603–619

    Article  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 

  • Nardini A, Gortan E, Ramani M, Salleo S (2008) Heterogeneity of gas exchange rates over the leaf surface in tobacco: an effect of hydraulic architecture? Plant Cell Environ 31:804–812

    Article  PubMed  Google Scholar 

  • Noctor G, De Paepe R, Foyer CH (2007a) Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci 12:125–134

    Article  PubMed  CAS  Google Scholar 

  • Noctor G, Quéval G, Gakière B (2007b) NAD(P) synthesis and pyridine nucleotide cycling in plants and their potential importance in stress conditions. J Exp Bot 57:1603–1620

    Article  Google Scholar 

  • Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50:1093–1106

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Araújo WL, Fernie AR (2011) Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol 155:101–107

    Article  PubMed  CAS  Google Scholar 

  • Pellny TK, Van Aken O, Dutilleul C, Wolff T, Groten K, Bor M, De Paepe R, Reyss A, Van Breusegem F, Noctor G, Foyer CH (2008) Mitochondrial respiratory pathways modulate nitrate sensing and nitrogen-dependent regulation of plant architecture in Nicotiana sylvestris. Plant J 54:976–992

    Article  PubMed  CAS  Google Scholar 

  • Priault P, Fresneau C, Noctor G, De Paepe R, Cornic G, Streb P (2006a) The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance. J Exp Bot 57:2075–2085

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Priault 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 

  • Queval G, Noctor G (2007) A plate-reader method for the measurement of NAD, NADP, glutathione and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal Biochem 363:58–69

    Article  PubMed  CAS  Google Scholar 

  • Sabar M, De Paepe R, de Kouchkovsky Y (2000) Complex I impairment, respiratory compensations and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol 124:1239–1250

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  PubMed  CAS  Google Scholar 

  • Szabados L, Savouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  PubMed  Google Scholar 

  • Szal B, Dabrowska Z, Malmberg G, Gardeström P, Rychter AM (2008) Changes in energy status of leaf cells as a consequence of mitochondrial genome rearrangement. Planta 227:697–706

    Article  PubMed  CAS  Google Scholar 

  • Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics 4:1122–1133

    Article  PubMed  CAS  Google Scholar 

  • Trouverie J, Chateau-Joubert S, Thevenot C, Jacquemot MP, Prioul JL (2004) Regulation of vacuolar invertase by abscisic acid or glucose in leaves and roots from maize plantlets. Planta 219:894–905

    Article  PubMed  CAS  Google Scholar 

  • Valentini R, Epron D, De Angelis P, Matteucci G, Dreyer E (1995) In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply. Plant Cell Environ 18:631–640

    Article  CAS  Google Scholar 

  • Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, Van Breusegem F (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104:15150–15155

    Google Scholar 

  • Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212

    Article  PubMed  CAS  Google Scholar 

  • Vidal G, Ribas-Carbo M, Garmier M, Dubertret G, Rasmusson AG, Mathieu C, Foyer CH, De Paepe R (2007) Lack of respiratory chain Complex I impairs AOX engagement and modulates redox signaling during elicitor-induced cell death in tobacco. Plant Cell 19:640–655

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the coordination of responses to stress in plants. Plant Cell Environ 25:195–210

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the University Paris-Sud 11, the Centre National de la Recherche Scientifique, the French Ministry of Research, and the Algerian and Tunisian Ministries of Research. IF-S was funded by the Spanish Ministry of Science and Innovation (Grant BFU2008-01072/BFI). We wish to thank Drs. Michael Hodges and Guillaume Tcherkez (Institut de Biologie des Plantes, UMR CNRS 8618, Université Paris-Sud 11, Orsay, France) for carefully reading the manuscript and Roland Boyer (University Paris-Sud 11) for the photographic artwork. The constructive comments of two anonymous referees are gratefully acknowledged.

Author information

Authors and Affiliations

  1. Laboratoire de Physiologie et Biologie des Organismes, Faculté des Sciences Biologiques, Université des Sciences et de la Technologie Houari Boumediene, BP 39, El Alia, Bab Ezzouar, Algiers, Algeria

    Reda Djebbar

  2. Université Paris-Sud 11, Ecologie, Systématique et Evolution, UMR-CNRS 8079, Bâtiment 362, 91405, Orsay Cedex, France

    Reda Djebbar, Touhami Rzigui, Pierrick Priault, Chantal Fresneau, Peter Streb & Gabriel Cornic

  3. Université Paris-Sud 11, Institut de Biologie des Plantes, UMR-CNRS 8618, Bâtiment 630, 91405, Orsay Cedex, France

    Reda Djebbar, Pierre Pétriacq, Marianne De Paepe, Bertrand Gakière & Rosine De Paepe

  4. Département de Biologie, Laboratoire de Physiologie et Biotechnologie Végétales, Faculté des Sciences de Tunis, 1060, Tunis, Tunisia

    Touhami Rzigui

  5. Université Paris-Sud 11 Plateforme Métabolisme Métabolome, IFR87 La Plante et son Environnement, Institut de Biologie des Plantes, Orsay, France

    Caroline Mauve

  6. Grup de Recerca en Biologia de les Plantes en Condicions Mediterrànies, Departament de Biologia, Universitat de les Illes Balears, 07122, Palma de Mallorca, Spain

    Igor Florez-Sarasa

  7. Université Pierre et Marie Curie, Laboratoire de Physiologie Cellulaire et Moléculaire UMR 7180 CNRS, Casier 156, Le Raphaël, 3 Rue Galilée, 94200, Ivry sur Seine, France

    Ghouziel Benhassaine-Kesri

Authors
  1. Reda Djebbar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Touhami Rzigui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierre Pétriacq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Caroline Mauve
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pierrick Priault
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chantal Fresneau
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marianne De Paepe
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Igor Florez-Sarasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ghouziel Benhassaine-Kesri
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Peter Streb
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Bertrand Gakière
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Gabriel Cornic
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Rosine De Paepe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gabriel Cornic.

Additional information

R. Djebbar and T. Rzigui participated equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Djebbar, R., Rzigui, T., Pétriacq, P. et al. Respiratory complex I deficiency induces drought tolerance by impacting leaf stomatal and hydraulic conductances. Planta 235, 603–614 (2012). https://doi.org/10.1007/s00425-011-1524-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1524-7

Keywords

Search

Navigation