Alterations on energy metabolism caused by mitochondrial uncoupling protein 1 (UCP1) overexpression in tobacco induce mitochondrial biogenesis and global stress response

Author(s)

Pedro Paulo Augusto Fabiano Arantes Pereira Barreto

• Document type: Doctoral Thesis
• Institution: Universidade Estadual de Campinas. Instituto de Biologia
• Defense date: 31 jul. 2014

Examining board members

Antonio Galina Filho; Elibio Leopoldo Rech Filho; Márcio José da Silva; Marina Camara Mattos Martins

• Advisor: Paulo Arruda

Abstract

The mitochondrial uncoupling protein 1 (UCP1) is a nuclear-encoded mitochondrial protein capable of uncouple the electrochemical gradient used for ATP synthesis, dissipating energy as heat. The discovery of UCP1 homologues, and its corresponding orthologues suggest diverse physiological functions for these proteins. UCPs may serve as an escape valve, decreasing the proton motive force (PMF) and preventing ROS production under unfavorable conditions. Plants overexpressing UCPs perform better under biotic and abiotic stresses. These plants show diminished ROS production, alteration of cell redox homeostasis, increased energy metabolism and photosynthesis. In this work we investigated the molecular mechanisms underlying cell energy metabolism and stress response in tobacco plants overexpressing an Arabidopsis thaliana UCP1. We demonstrated through molecular, cellular and genomic tools that UCP1 overexpressing plants is capable of increasing uncoupled respiration of isolated mitochondria, decrease intracellular ATP levels, and trigger a retrograde signaling that resulted in a broad induction of mitochondrial and stress response genes. The retrograde signaling resulted in the induction of mitochondrial biogenesis verified by increased mitochondrial number, area and alterations on mitochondrial morphology. The increased mitochondrial biogenesis in these plants accompanied by the broad increase in the expression of stress responsive genes, may be responsible for the diminished ROS production and the better performance of these plants when submitted to several abiotic stresses. We also performed a detailed analysis of the transcriptome expression of the UCP1 overexpressing plants as compared with the wild type plants. We verified that the UCP1 overexpressing plants exhibited a tight connection between mitochondrial, cytoplasm and chloroplast energy metabolism to accommodate the alterations caused by the increased UCP1 activity. A number of uncharacterized transcription factors seem to be good targets for future investigations on the regulation of plant mitochondrial biogenesis and energy metabolism. The results presented in this work allowed a better understanding of the flexibility of energy metabolism in plants, and the use of this mechanism to identify possible regulators of plant mitochondrial biogenesis and stress response. (AU)

• FAPESP's process: 12/00126-1 - Identification of transcription factors possibly involved in mitochondrial biogenesis
• Grantee: Pedro Paulo Augusto Fabiano Arantes Pereira Barreto
• Support type: Scholarships in Brazil - Doctorate (Direct)