AtMic60 Is Involved in Plant Mitochondria Lipid Trafficking and Is Part of a Large Complex

Abstract

The mitochondrion is an organelle originating from an endosymbiotic event and playing a role in several fundamental processes such as energy production, metabolite syntheses, and programmed cell death. This organelle is delineated by two membranes whose synthesis requires an extensive exchange of phospholipids with other cellular organelles such as endoplasmic reticulum (ER) and vacuolar membranes in yeast. These transfers of phospholipids are thought to occur by a non-vesicular pathway at contact sites between two closely apposed membranes. In plants, little is known about the biogenesis of mitochondrial membranes. Contact sites between ER and mitochondria are suspected to play a similar role in phospholipid trafficking as in yeast, but this has never been demonstrated. In contrast, it has been shown that plastids are able to transfer lipids to mitochondria during phosphate starvation. However, the proteins involved in such transfer are still unknown. Here, we identified in Arabidopsis thaliana a large lipid-enriched complex called the mitochondrial transmembrane lipoprotein (MTL) complex. The MTL complex contains proteins located in the two mitochondrial membranes and conserved in all eukaryotic cells, such as the TOM complex and AtMic60, a component of the MICOS complex. We demonstrate that AtMic60 contributes to the export of phosphatidylethanolamine from mitochondria and the import of galactoglycerolipids from plastids during phosphate starvation. Furthermore, AtMic60 promotes lipid desorption from membranes, likely as an initial step for lipid transfer, and binds to Tom40, suggesting that AtMic60 could regulate the tethering between the inner and outer membranes of mitochondria.

Glycerolipid synthesis and lipid trafficking in plant mitochondria

“…In addition, the MICOS complex shows genetic interactions in yeast with components of the ERMES complex and consequently, a role of the MICOS complex in lipid trafficking from ER to the IM of mitochondria has been proposed [66]. This hypothesis is supported by a recent study in plants showing the involvement of Mic60 in mitochondria lipid trafficking (see below) [8].…”

“…The quantity of AtMic60 and Tom40 increases in the MTL complex during Pi starvation similar to the content of DGDG suggesting that the MTL complex, via AtMic60 and OM partners such as Tom40, could mediate the traffic of DGDG in mitochondria during Pi starvation . In addition, some proteins, of unknown functions, that localize to the outer envelope of plastids have been characterized as components of the MTL complex . These proteins are putative candidates to mediate membrane tethering and/or lipid trafficking between mitochondria and plastids.…”

The plastid outer membrane localized LPTD1 is important for glycerolipid remodelling under phosphate starvation

“…Under this condition, the cellular content of DGDG and SQDG is increased, and DGDG is distributed to other organelles (Fig. ; Haertel et al , Jouhet et al , Moellering & Benning , Michaud et al ). This is accompanied with enhanced expression of genes coding for atMGD2 and atMGD3 (Fig.…”

Plant–microbe interactions: organelles and the cytoskeleton in action

“…In addition, morphological changes have been observed for some organelles. Under high light conditions, peroxisomes produce tubular protrusions, called peroxules, that extend over the surface of the chloroplast and mitochondria (Jouhet et al, 2004;Michaud et al, 2016). Stromules, dynamic extensions of the chloroplast stroma, have been observed to be associated with the nucleus and the plasma membrane (Kwok & Hanson, 2004;Caplan et al, 2015).…”

“…Connections between the chloroplast envelope and the ER membrane are observed following the trans-organellar complementation of a mutant that is defective in tocopherol biogenesis (Mehrshahi et al, 2013). During phosphate starvation, translocation of digalactosylglycerol (DGDG) lipids synthesized in the plastids to the mitochondrial membranes at mitochondria-plastid contact sites has been shown using transmission electron microscopy and biochemical approaches (Jouhet et al, 2004;Michaud et al, 2016). Under high light stress conditions, peroxisomes also produce tubular structures, called peroxules, that extend to the chloroplast and mitochondrial surface (Oikawa et al, 2015;Jaipargas et al, 2016).…”