The lack of mitochondrial complex I in a CMSII mutant of Nicotiana sylvestris increases photorespiration through an increased internal resistance to CO2 diffusion

Abstract

The cytoplasmic male sterile II (CMSII) mutant lacking complex I of the mitochondrial electron transport chain has a lower photosynthetic activity but exhibits higher rates of excess electron transport than the wild type (WT) when grown at high light intensity. In order to examine the cause of the lower photosynthetic activity and to determine whether excess electrons are consumed by photorespiration, light, and intercellular CO(2), molar fraction (c(i)) response curves of carbon assimilation were measured at varying oxygen molar fractions. While oxygen is the major acceptor for excess electrons in CMSII and WT leaves, electron flux to photorespiration is favoured in the mutant as compared with the WT leaves. Isotopic mass spectrometry measurements showed that leaf internal conductance to CO(2) diffusion (g(m)) in mutant leaves was half that of WT leaves, thus decreasing the c(c) and favouring photorespiration in the mutant. The specificity factor of Rubisco did not differ significantly between both types of leaves. Furthermore, carbon assimilation as a function of electrons used for carboxylation processes/electrons used for oxygenation processes (J(C)/J(O)) and as a function of the calculated chloroplastic CO(2) molar fraction (c(c)) values was similar in WT and mutant leaves. Enhanced rates of photorespiration also explain the consumption of excess electrons in CMSII plants and agreed with potential ATP consumption. Furthermore, the lower initial Rubisco activity in CMSII as compared with WT leaves resulted from the lower c(c) in ambient air, since initial Rubisco activity on the basis of equal c(c) values was similar in WT and mutant leaves. The retarded growth and the lower photosynthetic activity of the mutant were largely overcome when plants were grown in high CO(2) concentrations, showing that limiting CO(2) supply for photosynthesis was a major cause of the lower growth rate and photosynthetic activity in CMSII.

The Mechanistic Basis of Internal Conductance: A Theoretical Analysis of Mesophyll Cell Photosynthesis and CO2 Diffusion

“…This effect may be partially explained by higher rates of photorespiration after stomatal closure. Lastly, Priault et al (2006) showed a link between photorespiration and internal conductance in a mutant lacking complex I of the mitochondrial electron transport chain. Our results (Fig.…”

The Pentatricopeptide Repeat GeneOTP43Is Required fortrans-Splicing of the Mitochondrialnad1Intron 1 inArabidopsis thaliana

“…This mutant carries a mitochondrial deletion in the nad7 gene encoding a 40-kD subunit of Complex I (Pla et al, 1995). The mutant plants develop slowly, exhibit conditional male sterility, and have no detectable Complex I, increased amounts and activity of AOX, and multiple perturbations to primary metabolism (Gutierres et al, 1997(Gutierres et al, , 1999Lelandais et al, 1998;Sabar et al, 2000;Dutilleul et al, 2003aDutilleul et al, , 2003bDutilleul et al, , 2005Pineau et al, 2005;Priault et al, 2006aPriault et al, , 2006bVidal et al, 2007). A second Complex I mutant has been described from maize (Karpova and Newton, 1999).…”

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

“…The properties of the CMS II mutant of Nicotiana sylvestris have been studied in some detail (Noctor et al 2004;Dutilleul et al 2005;Priault et al 2006Priault et al , 2007. It lacks a functional Complex I of the mitochondrial electron transport chain, has lower photosynthetic activity, and has higher respiratory rate than WTt (Dutilleul et al 2003).…”