Miro2 tethers the ER to mitochondria to promote mitochondrial fusion in tobacco leaf epidermal cells

Abstract

Mitochondria are highly pleomorphic, undergoing rounds of fission and fusion. Mitochondria are essential for energy conversion, with fusion favouring higher energy demand. Unlike fission, the molecular components involved in mitochondrial fusion in plants are unknown. Here, we show a role for the GTPase Miro2 in mitochondria interaction with the ER and its impacts on mitochondria fusion and motility. Mutations in AtMiro2's GTPase domain indicate that the active variant results in larger, fewer mitochondria which are attached more readily to the ER when compared with the inactive variant. These results are contrary to those in metazoans where Miro predominantly controls mitochondrial motility, with additional GTPases affecting fusion. Synthetically controlling mitochondrial fusion rates could fundamentally change plant physiology by altering the energy status of the cell. Furthermore, altering tethering to the ER could have profound effects on subcellular communication through altering the exchange required for pathogen defence.

It Started With a Kiss: Monitoring Organelle Interactions and Identifying Membrane Contact Site Components in Plants

“…Oikawa et al (2015) used a femtosecond laser to generate shock waves to quantify the physical interaction between chloroplasts and peroxisomes. This same organelle pairing has been analyzed using optical tweezers (Gao et al, 2016), as have ER-Golgi (Sparkes et al, 2009), ER-chloroplast (Andersson et al, 2007) and ERmitochondria interactions (White et al, 2020). Optical tweezers provide submicron accuracy to trap and "target" a single organelle and micro-manipulate its position relative to other structures ( Figure 1D).…”

“…Membrane contact sites (MCS) are regions at which transient, physical interactions between organelles occur. These interactions allow exchange of molecules such as signals (e.g., calcium, Csordás et al, 2010) and membrane lipids (Michaud and Jouhet, 2019), and are important for regulating the number and positioning of some organelle types (Phillips and Voeltz, 2016;Mueller-Schuessele and Michaud, 2018;White et al, 2020). Direct molecular exchanges between organelles may alternatively be carried out by vesicle-mediated delivery (Scorrano et al, 2019) or by transient interaction between organelles of the same type (e.g., "kiss and run" in mitochondria, Liu et al, 2009).…”

Contribution of Massive Mitochondrial Fusion and Subsequent Fission in the Plant Life Cycle to the Integrity of the Mitochondrion and Its Genome

“…Unlike the situation with fission, obvious orthologues of yeast or mammalian fusion have not been found [ 20 ]. However, recently, the GTPase ATMIRO2 has been investigated in tobacco epidermal cells [ 49 ]. Homologues in yeast (ScGEM1) affect mitochondrial–ER interactions and in mammals (HsMIRO1) affect mitochondrial motility.…”

“…Homologues in yeast (ScGEM1) affect mitochondrial–ER interactions and in mammals (HsMIRO1) affect mitochondrial motility. Evidence was obtained that AtMIRO2 regulates the tethering of mitochondria to the ER, such that ER–mitochondria attachment increases mitochondrial fusion, associated with increased clustering of mitochondria and decreased motility [ 49 ]. It has been shown that actin polymerisation is not required for mitochondrial fusion [ 18 , 50 ], though myosin and microtubule inhibitors reduced fusion [ 18 ].…”

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

“…Although dysfunction of Arabidopsis MIRO1 caused embryo lethality, elongated mitochondria were detected in pollen tubes [ 69 ]. Interestingly, Arabidopsis MIRO2 knockout plants showed no obvious growth defects, but when there was overexpression of an active MIRO2 variant, larger and fewer mitochondria were observed in stable contact with the ER [ 70 ]. Contrary to the dominant function of MIRO in mitochondrial movement, MIRO might function in a plant-specific manner for both mitochondrial fusion and motility.…”