Mitochondrial dysfunction associated with ascorbate synthesis in plants

MAZORRA MORALES, LUIS MIGUEL; COSME SILVA, GLÁUCIA MICHELLE; SANTANA, DIEDERSON BORTOLINI; PIREDA, SAULO F.; DORIGHETTO COGO, ANTÔNIO JESUS; HERINGER, ÂNGELO SCHUABB; DE OLIVEIRA, TADEU DOS REIS; REIS, RICARDO S.; DOS SANTOS PRADO, LUÍS ALFREDO; DE OLIVEIRA, ANDRÉ VICENTE; SILVEIRA, VANILDO; DA CUNHA, MAURA; BARROS, CLÁUDIA F.; FAÇANHA, ARNOLDO R.; BALDET, PIERRE; BARTOLI, CARLOS G.; DA SILVA, MARCELO GOMES; OLIVEIRA, JURANDI G.

PLANT PHYSIOLOGY AND BIOCHEMISTRY

ELSEVIER FRANCE-EDITIONS SCIENTIFIQUES MEDICALES ELSEVIER

Año: 2022 vol. 185 p. 55 - 68

0981-9428

Mitochondria are the major organelles of energy production; however, active mitochondria can decline their energetic role and show a dysfunctional status. Mitochondrial dysfunction was induced by high non-physiological level of L-galactone-1,4-lactone (L-GalL), the precursor of ascorbate (AsA), in plant mitochondria. The dysfunction induced by L-GalL was associated with the fault in the mitochondrial electron partition and reactive oxygen species (ROS) over-production. Using mitochondria from RNAi-plant lines harbouring silenced L-galactone-1,4-lactone dehydrogenase (L-GalLDH) activity, it was demonstrated that such dysfunction is dependent on this enzyme activity. The capacity of alternative respiration was strongly decreased by L-GalL, probably mediated by redox-inactivation of the alternative oxidase (AOX) enzyme. Although, alternative respiration was shown to be the key factor that helps support AsA synthesis in dysfunctional mitochondria. Experiments with respiratory inhibitors showed that ROS formation and mitochondrial dysfunction were more associated with the decline in the activities of COX (cytochrome oxidase) and particularly AOX than with the lower activities of respiratory complexes I and III. The application of high L-GalL concentrations induced proteomic changes that indicated alterations in proteins related to oxidative stress and energetic status. However, supra-optimal L-GalL concentration was not deleterious for plants. Instead, the L-GalLDH activity could be positive. Indeed, it was found that wild type plants performed better growth than L-GalLDH-RNAi plants in response to high non-physiological L-GalL concentrations.