Friendly regulates membrane depolarization induced mitophagy in Arabidopsis

Abstract

The oxidative environment within the mitochondria makes them particularly vulnerable to proteotoxic stress. To maintain a healthy mitochondrial network, eukaryotes have evolved multi-tiered quality control pathways. If the stress cannot be alleviated, defective mitochondria are selectively removed by autophagy via a process termed mitophagy. Despite significant advances in metazoans and yeast, in plants, the molecular underpinnings of mitophagy are largely unknown. Here, using time-lapse imaging, electron tomography and biochemical assays, we show that uncoupler treatments cause loss of mitochondrial membrane potential and induce autophagy in Arabidopsis. The damaged mitochondria are selectively engulfed by autophagosomes that are ATG5 dependent and labelled by ATG8 proteins. Friendly, a member of the Clustered Mitochondria protein family, is recruited to the damaged mitochondria to mediate mitophagy. In addition to stress, mitophagy is also induced during de-etiolation, a major cellular transformation during photomorphogenesis that involves chloroplast maturation. De-etiolation triggered mitophagy regulates cotyledon greening, pointing towards an inter-organellar cross-talk mechanism. Altogether our results demonstrate how plants employ mitophagy to recycle damaged mitochondria during stress and development.

Autophagy Contributes to the Quality Control of Leaf Mitochondria

“…Here, we observed an additive effect on the morphology and function of mitochondria in friendly atg double mutant leaves ( Figs.�8, 9 ), suggesting the independent functions of FRIENDLY and autophagy in leaves. By contrast, the study in uncoupler-treated roots indicated that FRIENDLY directly contributes to the induction of mitophagy ( Ma et al 2020 ). Therefore, the different roles of FRIENDLY in the induction of mitophagy in distinct stresses or organs should be further elucidated.…”

“…A recent preprint article reported the contribution of mitophagy to the quality control of mitochondria in Arabidopsis roots treated with an uncoupler ( Ma et al 2020 ). Uncouplers act as proton ionophores; they dissipate the proton gradient across the mitochondrial inner membrane, resulting in the loss of ATP synthesis capacity within mitochondria.…”

Autophagy promotes photomorphogenesis during seedling development in Arabidopsis in carbon limiting conditions

“…Very recently, mitophagy was shown to take place in cotyledons during de-etiolation (6h post illumination) and an analogous delay in greening capacity of atg5 was presented (Ma et al 2021), suggesting that autophagy plays a role in adjusting the number of mitochondria during photomorphogenesis and proposing cross-talk with delayed plastid biogenesis. We show here that the atg greening phenotype is not specific to atg5 and is not constitutive, but conditional on C status.…”

Plant Mitophagy in Comparison to Mammals: What Is Still Missing?

“…It has been shown that mitochondria in friendly mutant cells formed large clusters. Interestingly, a recent study also uncovered a unique role of FRIENDLY in plant mitophagy [ 21 ]. In friendly mutants, abnormal mitophagosomes accumulated, and the level of mitophagy was significantly reduced upon mitochondrial uncoupler treatment, implying a defect in mitophagy due to the loss of FRIENDLY.…”

“…In germinating Arabidopsis seedlings, it has been observed that inactive mitochondria are engulfed by autophagosomes, suggesting that mitophagy facilitates the degradation of mitochondria that fail to recover from dormancy [ 20 ]. Recently, it has been also demonstrated that the de-etiolation process is suppressed in atg5 mutant plants during the transition from darkness to light [ 21 ]. In addition, intact mitochondria were observed in the vacuole of Arabidopsis under oxidative stress, implying the occurrence of mitophagy in response to stress [ 15 ].…”