Mitochondria affect photosynthesis through altered tissue levels of O₂

Abstract

Oxygen (O2) availability in plant tissues is dynamically shaped by photosynthesis and respiration and is linked to stress responses and development. While mitochondria are the primary consumers of cellular O2, their impact on chloroplast functions under low-oxygen conditions remains insufficiently understood. Mitochondrial retrograde signaling activates expression of nuclear genes encoding alternative oxidases and other respiratory components, and high abundance of these enzymes coincides not only with changes in respiration but also with alterations in chloroplast functions. For example, plants with induced mitochondrial signaling are tolerant to methyl viologen, which catalyzes the chloroplastic Mehler reaction. The mechanism of this inter-organelle interaction remains unclear. Here, we investigated respiration, photosynthesis, and in vivo O2 levels in Arabidopsis (Arabidopsis thaliana) mutants and transgenic lines with perturbations in diverse mitochondrial functions, including defects in respiratory complex I, ATP synthase, mitochondrial protein processing, transcription, nucleoid organization, and organelle architecture, as well as in lines with altered mitochondrial signaling, alternative oxidase activities, and nitric oxide metabolism. Increased abundance and capacity of alternative oxidases correlated with elevated O2 consumption in darkness, slower O2 re-accumulation in light, and reduced effects of methyl viologen on chloroplasts. The changes are likely mediated by multiple stress-induced alternative respiratory components. Our results support the hypothesis that enhanced mitochondrial O2 consumption under stress lowers tissue O2 levels, thereby modifying chloroplastic electron transfer and ROS metabolism. These data provide insights into the establishment and sensing of hypoxia in plants, plant adaptation to mitochondrial stress and low-oxygen environments, and the roles of chloroplasts in these processes.