Perturbation of Melatonin Signaling Modulates Respiration and Mitochondrial Gene Expression in Arabidopsis thaliana During Photooxidative Stress

Abstract Melatonin (MT) is a critical regulator of mitochondria that affects bioenergetics, dynamics, and gene expression, and effectively protects them from oxidative stress. In this study we elucidated the role of the putative melatonin receptor CAND2/PMTR1 in mitochondrial respiration and the melatonin-mediated expression of mitochondrial genes under high light (HL) stress. Disruption of CAND2 and its associated partner GPA1 in Arabidopsis thaliana resulted in an increase in the respiration rate predominantly due to cytochrome respiration (CP), in contrast to wild type (WT) plants and 35SCAND2 overexpressing line in which an increase of alternative respiration (AP) prevails. MT treatment decreased AP activation under HL and reduced the overall leaf respiration rate, however, these effects were less pronounced in cand2 and gpa1 mutants. Increase in an AP capacity under HL stress positively correlated with an increase in transcript accumulation of the alternative oxidase (AOX) genes ( AOX1a , AOX1d ). At the same time, under stress conditions, the expression of the studied CP genes ( cob, cox1 ) and the ATPase gene ( atp6-1 ) was suppressed. MT treatment completely removed this inhibition, but only in WT and 35SCAND2 plants. Moreover, cand2 showed elevated steady state transcript levels of genes associated with mitochondrial dysfunction, suggesting an initial stress state of the mutant. The effects of exogenous melatonin on mitochondrial gene activity were mainly dependent on CAND2 receptor activity, although some genes were regulated by melatonin independently of CAND2, indicating the multiple mechanisms of melatonin perception in plants. Thus, disruption of MT signaling has a significant impact on mitochondrial respiration and mitochondrial gene expression.