Effect of Mitochondrial Dysfunction on Carbon Metabolism and Gene Expression in Flower Tissues of Arabidopsis thaliana

Abstract

We characterized the transcriptomic response of transgenic plants carrying a mitochondrial dysfunction induced by the expression of the unedited form of the ATP synthase subunit 9. The u-ATP9 transgene driven by A9 and APETALA3 promoters induce mitochondrial dysfunction revealed by a decrease in both oxygen uptake and adenine nucleotides (ATP, ADP) levels without changes in the ATP/ADP ratio. Furthermore, we measured an increase in ROS accumulation and a decrease in glutathione and ascorbate levels with a concomitant oxidative stress response. The transcriptome analysis of young Arabidopsis flowers, validated by qRT-PCR and enzymatic or functional tests, showed dramatic changes in u-ATP9 plants. Both lines display a modification in the expression of various genes involved in carbon, lipid, and cell wall metabolism, suggesting that an important metabolic readjustment occurs in plants with a mitochondrial dysfunction. Interestingly, transcript levels involved in mitochondrial respiration, protein synthesis, and degradation are affected. Moreover, the levels of several mRNAs encoding for transcription factors and DNA binding proteins were also changed. Some of them are involved in stress and hormone responses, suggesting that several signaling pathways overlap. Indeed, the transcriptome data revealed that the mitochondrial dysfunction dramatically alters the expression of genes involved in signaling pathways, including those related to ethylene, absicic acid, and auxin signal transduction. Our data suggest that the mitochondrial dysfunction model used in this report may be useful to uncover the retrograde signaling mechanism between the nucleus and mitochondria in plant cells.

Mitochondrial dysfunction affects chloroplast functions

“…13 In contrast with these observations, we found an increase of 6 and 5 times in AtCLH2 mRNA levels in A9:u-ATP9 and ap3:u-ATP9 plants respectively, compared with wild type plants (Fig. 2B) which agrees with the results of microarray data.…”

“…13 Previous studies indicate that AtCLH2 is constitutively expressed throughout leaf development, and that its expression is unaffected by stress or senescence. [16][17][18] …”

“…15 Among relevant enzymes in chlorophyll catabolism, chlorophyllase (CLH) which catalyzes the hydrolysis of ester bond to yield chlorophyllide and phytol, was found affected in the microarray experiments of u-ATP9 plants, particularly AtCLH2 (At5g43860) one of two CLHs from Arabidopsis. 13 Previous studies indicate that AtCLH2 is constitutively expressed throughout leaf development, and that its expression is unaffected by stress or senescence. chelating substances (MCS) or by Mg-releasing proteins (MRP), which differs by their substrate specificity.…”

“…[5][6][7][8][9][10][11][12] The recent study of the transcriptome Keywords: mitochondria, chloroplasts, mitochondrial dysfunction, arabidopsis in Arabidopsis plants carrying a mitochondrial dysfunction, revealed important modifications in the expression of some genes from the carbon metabolic pathways with inhibition of glycolysis and the induction of the MDH alternative pathways. 13 This model, where the mitochondrial flaw was induced by the expression of the unedited form of the ATP synthase subunit 9 (u-ATP9), 8 is useful to uncover the interactions between organelles in plant cells.…”

“…2B) which agrees with the results of microarray data. 13 An indicator of the chlorophyll breakdown is the release of Mg atoms from these molecules. The Mg-dechelatase activity is performed either by heat stable low-molecular weight metal …”