Friendly regulates membrane depolarization induced mitophagy in Arabidopsis
Posted on: 24 July 2020
Preprint posted on 12 July 2020
Getting rid of mitochondria can be FRIENDLY: mitophagy is required for plant de-etiolation
Selected by Alvaro Montiel-Jorda
Categories: cell biology, genetics, molecular biology, plant biology
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 physiology, 166(2), 808-828.
doi: https://doi.org/10.1242/prelights.22282
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| List by | Nathalie Krauth |
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Also in the plant biology category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
The Society for Developmental Biology 82nd Annual Meeting
This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.
| List by | Joyce Yu, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |