Planta

, Volume 235, Issue 3, pp 603–614 | Cite as

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

  • Reda Djebbar
  • Touhami Rzigui
  • Pierre Pétriacq
  • Caroline Mauve
  • Pierrick Priault
  • Chantal Fresneau
  • Marianne De Paepe
  • Igor Florez-Sarasa
  • Ghouziel Benhassaine-Kesri
  • Peter Streb
  • Bertrand Gakière
  • Gabriel Cornic
  • Rosine De Paepe
Original Article

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.

Keywords

Drought Mitochondria Nicotiana Pyridine nucleotides Stomatal and hydraulic conductances TCA cycle-derived metabolites 

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%

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Reda Djebbar
    • 1
    • 2
    • 3
  • Touhami Rzigui
    • 2
    • 4
  • Pierre Pétriacq
    • 3
  • Caroline Mauve
    • 5
  • Pierrick Priault
    • 2
  • Chantal Fresneau
    • 2
  • Marianne De Paepe
    • 3
  • Igor Florez-Sarasa
    • 6
  • Ghouziel Benhassaine-Kesri
    • 7
  • Peter Streb
    • 2
  • Bertrand Gakière
    • 3
  • Gabriel Cornic
    • 2
  • Rosine De Paepe
    • 3
  1. 1.Laboratoire de Physiologie et Biologie des Organismes, Faculté des Sciences BiologiquesUniversité des Sciences et de la Technologie Houari BoumedieneBab EzzouarAlgeria
  2. 2.Université Paris-Sud 11, Ecologie, Systématique et EvolutionOrsay CedexFrance
  3. 3.Université Paris-Sud 11, Institut de Biologie des PlantesOrsay CedexFrance
  4. 4.Département de BiologieLaboratoire de Physiologie et Biotechnologie Végétales, Faculté des Sciences de TunisTunisTunisia
  5. 5.Université Paris-Sud 11 Plateforme Métabolisme Métabolome, IFR87 La Plante et son Environnement, Institut de Biologie des PlantesOrsayFrance
  6. 6.Grup de Recerca en Biologia de les Plantes en Condicions Mediterrànies, Departament de BiologiaUniversitat de les Illes BalearsPalma de MallorcaSpain
  7. 7.Université Pierre et Marie Curie, Laboratoire de Physiologie Cellulaire et Moléculaire UMR 7180 CNRSIvry sur SeineFrance

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