Cytochrome c Deficiency Differentially Affects the In Vivo Mitochondrial Electron Partitioning and Primary Metabolism Depending on the Photoperiod.

Igor Florez-Sarasa,Alisdair R Fernie,Elina Welchen,Sofia Racca,Miquel Ribas-Carbo,Nestor Fernandez Del-Saz,José G Vallarino,Daniel H Gonzalez

doi:10.3390/plants10030444

Abstract

Plant respiration provides metabolic flexibility under changing environmental conditions by modulating the activity of the nonphosphorylating alternative pathways from the mitochondrial electron transport chain, which bypass the main energy-producing components of the cytochrome oxidase pathway (COP). While adjustments in leaf primary metabolism induced by changes in day length are well studied, possible differences in the in vivo contribution of the COP and the alternative oxidase pathway (AOP) between different photoperiods remain unknown. In our study, in vivo electron partitioning between AOP and COP and expression analysis of respiratory components, photosynthesis, and the levels of primary metabolites were studied in leaves of wild-type (WT) plants and cytochrome c (CYTc) mutants, with reduced levels of COP components, under short- and long-day photoperiods. Our results clearly show that differences in AOP and COP in vivo activities between WT and cytc mutants depend on the photoperiod likely due to energy and stress signaling constraints. Parallel responses observed between in vivo respiratory activities, TCA cycle intermediates, amino acids, and stress signaling metabolites indicate the coordination of different pathways of primary metabolism to support growth adaptation under different photoperiods.

Highlights

Respiration is a vital process for leaf primary metabolism because it provides ATP and carbon skeletons to sustain photosynthetic carbon (C) and nitrogen (N) metabolism required for plant growth and survival [1,2,3]
The cytc mutants grown under short-day (SD) and long-day (LD) photoperiods displayed a delay in rosette development (Figure S1A), and all analyses were performed in leaves from plants at the same developmental stage
Western blot (Figure S1B) and qPCR (Figure S1C) analyses confirmed the deficiency in cytochrome c (CYTc) in both mutant lines grown under both photoperiods

Summary

Introduction

Respiration is a vital process for leaf primary metabolism because it provides ATP and carbon skeletons to sustain photosynthetic carbon (C) and nitrogen (N) metabolism required for plant growth and survival [1,2,3]. The inhibition of COP activity occurs under different stress conditions, including drought, low temperature, and nutrient limitation, as well as after exposure of plant tissues to allelochemicals, heavy metals, and nitric oxide [5]. Under such COP restriction, the mETC components become highly reduced, and the generation of reactive oxygen species (ROS) and nitrogen species (RNS) in the mitochondria increases with its consequences for protein oxidation and malfunction [16,17,18,19]. The AOP is thought to preserve COX function by limiting ROS and RNS generation that can lead to protein oxidative damage [3] and, at the same time, keeping the activity of (photo) respiratory metabolism essential for chloroplast redox and carbon balance [5]

Methods

Results

Discussion

Conclusion