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Friendly regulates membrane depolarization induced mitophagy in Arabidopsis

Juncai Ma, Zizhen Liang, Jierui Zhao, Pengfei Wang, Wenlong Ma, Juan A. Fernandez Andrade, Yonglun Zeng, Nenad Grujic, Liwen Jiang, Yasin Dagdas, Byung-Ho Kang

Preprint posted on July 12, 2020 https://www.biorxiv.org/content/10.1101/2020.07.12.198424v1

Getting rid of mitochondria can be FRIENDLY: mitophagy is required for plant de-etiolation

Selected by Alvaro Montiel-Jorda

Background

Plant cells have several mechanisms to control the abundance of proteins and even entire organelles according to the physiological needs of the organism.

For example, upon pathogen perception, the plasma membrane receptor FLS2 senses flagellin and activates the immune response. This response cannot go on forever, so the same molecule that serves as recognition of the pathogen can also trigger the internalization of the receptor into endosomes to attenuate the response (Robatzek et al., 2006). Similarly, when plants are exposed to a toxic amount of metals, the plasma membrane metal transporter IRT1 is internalized and degraded to avoid a metal overload (Dubeaux et al., 2018).

Soluble proteins, on the other hand, can be degraded via the proteasome or via the autophagy pathway. The autophagy pathway consists of the formation of double membrane vesicles called autophagosomes , which will engulf a certain cargo and then fuse to the vacuole so that the cargo can be degraded. The formation of the autophagosome requires the so-called AUTOPHAGY (ATG) genes (Reviewed in Üstün et al., 2017).

Fig. 1 The autophagy pathway in plants. Adapted from Üstün et al., 2017.

Not only soluble proteins, but even entire organelles such as chloroplasts can be degraded through autophagy (Izumi et al., 2017).  Autophagy of non-specific cargo is just named autophagy or macroautophagy. However, if autophagy has a specific cargo, it receives another name. Such is the case for chloroplast autophagy, chloroplagy.

There is considerable evidence in animals that mitochondria can be degraded by autophagy (mitophagy). On the other hand, even if it is likely also the case for plants, the evidence is missing. Here, Ma et al., demonstrate that mitophagy also exists in plants and identify a key molecular player, the protein FRIENDLY.

Key findings

The authors demonstrate that mitochondria membrane depolarization caused by the uncouplers DNP and FCCP can lead to mitophagy. This finding is extremely important because it provides a framework to then figure out the molecular actors involved in this process in plants.

They go on to prove that mitophagy requires ATG5, a well-known protein required for general autophagy (macroautophagy) (Fig.2), and the vacuole, meaning that mitochondria removed by this process end up in the vacuole for degradation. Very interestingly, they show that DNP/FCCP treatment specifically triggers mitophagy and not other types of autophagy such as aggrephagy (selective degradation of protein aggregates by autophagy).

Fig. 2 (a,b) DNP treatment causes mitophagy. (c) Time-lapse of a mitophagy event . (d,e) DNP triggers mitophagy. (f) Finished mitophagy event. (g, h, i) 3D reconstructions of d,e,f. (l) atg5-1 mutants are impaired in mitophagy .

The authors then face what would seem as a contradiction. Mitophagy is highly specific, however it requires the macroautophagy protein ATG5. Is there maybe a player that can interact with the autophagosome marker ATG8 to confer that specificity? To test that hypothesis, they select the protein FRIENDLY (hereafter FMT), which is involved in mitochondrial dynamics  (El Zawily et al., 2014).  Upon DNP treatment, FMT relocates from the cytoplasm to mitochondria (Fig. 3a). Moreover, DNP also triggers the association of FMT with ATG8 (Fig. 3b). Importantly, in the fmt mutant, ATG8-labeled autophagosomes are associated with mitochondria but no engulfement whatsoever is observed, contrary to the wild-type (Fig.3c).

Fig. 3 (a) Relocation of FMT to mitochondria upon DNP treatment. (b) CoIP of ATG8 and FMT upon DNP treatment. (c) An autophagosome can be seen completely engulfing a mitochondria in wild-type but not in the fmt mutant.

Lastly, the authors sought to pinpoint the biological role of mitophagy in plants. Several lines of evidence suggest that the electron transport chain in mitochondria is slowed down in de-etiolation (transition from darkness to light). Mitophagy could explain this phenomenon, so they investigate one of the characteristics of de-etiolation, the greening of the cotyledons, in wild-type and atg5-1 mutants. As expected, atg5-1 fail to become green upon light exposure (Fig.4). It remains an open question whether fmt mutants display the same phenotype, as one would expect.

Fig. 4 (a) Imaging of cotyledons of wild-type and atg5-1 plants during de-etiolation. (b) Quantification. (c) An autophagosome can be seen completely engulfing a mitochondria 6h after light exposure.

What I like about this work

Whereas a proper experimental setup to study mitophagy already existed for animal cells, it was lacking for plants. This paper lays the foundation to study the molecular mechanisms responsible for plant mitophagy. The paper produces a solid conclusion by combining complementary imaging techniques, thoughtful image analysis, biochemistry and genetics.

Further reading

El Zawily, A. M., Schwarzländer, M., Finkemeier, I., Johnston, I. G., Benamar, A., Cao, Y., … & Macherel, D. (2014). FRIENDLY regulates mitochondrial distribution, fusion, and quality control in Arabidopsis. Plant physiology166(2), 808-828.

 

Tags: arabidopsis, autophagy, mitochondria, mitophagy

Posted on: 24th July 2020

doi: https://doi.org/10.1242/prelights.22282

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