The mitochondrial CMSII mutation of Nicotiana sylvestris impairs adjustment of photosynthetic carbon assimilation to higher growth irradiance

Abstract

The CMSII mutant of Nicotiana sylvestris, which lacks a functional mitochondrial complex I, was used to investigate chloroplast-mitochondria interactions in light acclimation of photosynthetic carbon assimilation. CMSII and wild-type (WT) plants were grown at 80 micromol m(-2) s(-1) photosynthetic active radiation (PAR; 80) and 350 micromol m(-2) s(-1) PAR (350). Carbon assimilation at saturating PFD was markedly higher in WT 350 leaves as compared with WT 80 leaves, but was similar in CMS 80 and CMS 350 leaves, suggesting that the mutant is unable to adjust photosynthesis to higher growth irradiance. WT 350 leaves showed several general characteristic light acclimation responses [increases in leaf specific area (LSA), total chlorophyll content, and chlorophyll a/b ratio, and a higher light compensation point]. In contrast, a similar chlorophyll content and chlorophyll a/b ratio were measured for both CMS 80 and CMS 350 leaves, while LSA and the light compensation point acclimated as in the WT. The failure of CMSII to adjust photosynthesis to growth PFD did not result from lower quantum efficiency of PSII, lower whole-chain electron transport rates (ETRs), or lower ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) and sucrose phosphate synthase (SPS) capacities. Excess ETR not used for carbon assimilation was even higher in CMS 350 than in WT 350. Since photochemical fluorescence quenching and the initial activity of NADP malate dehydrogenase (NADP-MDH) were identical in WT 350 and CMS 350 leaves but the activation state of NADP-MDH was different, redox signals from primary ETR are not involved in the signal transduction of light acclimation, while a contribution of stromal redox state cannot be excluded. When mature plants were transferred between 350 and 80 conditions, the mutant showed acclimatory tendencies, although adjustments were not as rapid or as marked as in the WT, and the response of the initial activities of Rubisco and NADP-MDH was impaired or altered. Initial activities of Rubisco and SPS at limiting concentration were also affected in CMS 350 as compared with WT plants when compared at growth irradiance or after in situ activation at 1000 micromol m(-2) s(-1) PAR. The data demonstrate that chloroplast-mitochondria interactions are important in light acclimation, and modulation of the activation state of key photosynthetic enzymes could be an important mechanism in this cross-talk.

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).…”

Complete Mitochondrial Complex I Deficiency Induces an Up-Regulation of Respiratory Fluxes That Is Abolished by Traces of Functional Complex I

“…The best-characterized mutants are cytoplasmic male sterile II (CMSII) in Nicotiana sylvestris, which has no detectable complex I due to a deletion in the mitochondrial NADH dehydrogenase subunit7 (nad7) gene encoding a complex I subunit (Pla et al, 1995;Gutierres et al, 1997;Sabar et al, 2000;Pineau et al, 2005), and Arabidopsis (Arabidopsis thaliana) ndufs4 that is impaired in complex I biogenesis due to loss of the accessory NDUFS4 subunit (Meyer et al, 2009). These studies reported delayed growth and modifications of the metabolite and transcript pools (Meyer et al, 2009), as well as potential secondary effects on other metabolic pathways, such as photosynthesis (Dutilleul et al, 2003;Priault et al, 2006;Meyer et al, 2009). However, the mitochondrial phenotypes observed were restricted to subtle changes of respiratory parameters Meyer et al, 2009).…”

Photoperiod Affects the Phenotype of Mitochondrial Complex I Mutants

“…Also, despite differences in tricarboxylic acid derivatives and some amino acids upon transfer from SD to LD, there is limited metabolic adaptation to LD in both mutants, in agreement with their impaired growth response. The remodeled metabolomes of CMSII Dutilleul et al, 2003a;Priault et al, 2006aPriault et al, , 2007 and ndufs4 (Meyer et al, 2009) mutants were associated with alterations in carbon and nitrogen assimilation under the LD condition. Here, we found that although net CO 2 assimilation (A) was lower in the ndufs8.1 ndufs8.2 mutant than in the wild type under elevated light and was stimulated by LD in both genotypes (light response curves shown in Supplemental Fig.…”

“…Responses of A to photon flux density (light curves) and internal CO 2 molar fraction (A/C i curves) performed under ambient (21%) oxygen content were measured on attached leaves with an open infrared gas analysis system equipped with a leaf chamber fluorometer (Li-Cor 6400-40; Li-Cor) as described by Priault et al (2006a). Leaves were dark adapted for at least 30 min before determining dark respiration.…”

“…CMSII plants showed altered responses to environmental conditions such as light (Priault et al, 2006a), nitrogen, and CO 2 (Pellny et al, 2008;Hager et al, 2010) and were fully male sterile under very low illumination only (De Paepe et al, 1990). They were differentially affected by drought stress (Galle et al, 2010;Djebbar et al, 2012).…”