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A research team led by Professor Zhuang Xiaohong from School of Life Sciences at The Chinese University of Hong Kong (CUHK) has unveiled a novel mechanism by which plant cells selectively degrade parts of their mitochondria under heat stress, shedding light on how plants adapt to rising global temperatures. The research findings have been recently published in top multidisciplinary scientific journal Proceedings of the National Academy of Sciences of the United States of America (PNAS). 

Global warming poses a serious threat to crop productivity and food security. When adapting to rising temperature, plant cells employ autophagy, a process of “self-eating” that recycles damaged cellular components. Mitochondria, often referred to as the powerhouses of plant cells, provide the main energy source. Damaged mitochondria are detrimental and might lead to cell death if they are not removed in a timely fashion. Recent studies have highlighted mitophagy, a selective form of autophagy targeting mitochondria, as important for maintaining mitochondrial health. However, how plant cells execute this process under heat stress has remained unclear.

A choice of diet in the cell

In the general model of mitophagy, a cup-like precursor membrane fragment (also known as phagophore or isolation membrane) grows along the mitochondrion and bends into a spherical double-membrane structure called an autophagosome. In this study, the research team identified key players in piecemeal plant mitophagy and illustrated how mitochondrial dynamics contribute to this process, enabling the selective degradation of mitochondrial parts.

Unlike the typically networked mitochondria in mammals, plant mitochondria are often physically discrete. While wholesale degradation of an entire mitochondrion has been observed; under heat stress, mitochondria reshape into a swollen, network-like pattern (Figure 1). Using a combination of biochemical, cellular and advanced imaging techniques, the research team has illustrated a new model of autophagosome assembly for piecemeal mitophagy, linked to the mitochondrial division process (Figure 2). When exposed to a higher temperature, mitochondria change their shapes and sizes through a cell-division like process, which may help isolate and remove damaged parts.

Mitochondrial fission controversy in mitophagy resolved

By characterising the key molecular complex involved in plant mitochondrial fission (Figure 3), the research team demonstrated that dysfunction in the plant-specific mitochondrial fission factor ELM1 significantly delays piecemeal mitophagy and leads to the accumulation of megamitochondria sequestered by multiple phagophore precursors. Mutations in these key components suppress mitochondrial protein degradation, making plants less tolerant of heat stress.

Professor Zhuang said: “This is the first study that describes piecemeal mitophagy for plant mitochondrial degradation. There has long been a debate about whether mitochondrial fission is required for mitophagy. Plant mitochondria have a unique patten in the cell, but they also have to reorganise and reshape membranes to help cells to survive under changeable and stressful conditions. We suspect that besides mitochondria, the turnover of other cellular structures might also be governed by piecemeal autophagy. It will be exciting to further investigate the molecular mechanisms.”

These findings underscore the importance of mitochondrial fission machinery in heat-induced piecemeal mitophagy across diverse organisms, providing valuable insights into mitophagosome formulation and plant stress resilience. Further investigation into the detailed molecular mechanism could provide new solutions to help mitigate the effect of climate change on crop production.

The full text of journal paper: https://doi.org/10.1073/pnas.2504921122