Plant-specific mitochondrial fission machinery connects mitochondrial dynamics and mitophagosome formation for piecemeal mitophagy
Abstract
As the energy center of the cell, mitochondria display enormous metabolic plasticity to meet the cellular demand for plant growth and development, which is tightly linked to their structural and dynamic plasticity. Mitochondrial number and morphology are coordinated through the actions of the mitochondrial division and fusion. Meanwhile, damaged mitochondrial contents are removed to avoid excess toxicity to the plant cells. Mitophagy, a selective degradation pathway of mitochondria through a double-membrane sac named autophagosome (also known as mitophagosome), plays a crucial role in maintaining mitochondrial homeostasis. Typically, wholesale mitophagy requires the elongation of a cup-shaped phagophore along the entire mitochondrion, which finally seals and closes as a mitophagosome. How plant mitophagosome formation and mitochondria sequestration are coordinated remains incompletely understood. In this work, we report an unappreciated role of the plant-specific mitochondrial fission regulator ELM1, together with the dynamin-related protein family DRP3 and the autophagic regulator SH3P2, to coordinate mitochondria segregation for piecemeal mitophagy under heat stress conditions. Dysfunction in mitochondrial fission activity impairs heat-induced mitophagy, leading to an accumulation of interconnected megamitochondria which are partially sequestered by the ATG8-positive phagophore. Furthermore, we show that the ELM1-mediated piecemeal mitophagy also engages the plant archetypal selective autophagic receptor NBR1. Using 3D tomography analysis, we illustrate the morphological features and spatial relationship of the megamitochondria and phagophore intermediates in connection with the mitochondrial fission sites. Collectively, our study provides an updated model of mitophagosome formation for piecemeal mitophagy mediated by the plant-unique mitochondrial fission machinery.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (11)
Juncai Ma
School of Life Sciences, Centre for Plant Vacuole Biology and Biotechnology, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong
Chaorui Li
School of Life Sciences, Centre for Plant Vacuole Biology and Biotechnology, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong
Kaike Ren
Areas of Excellence Centre for Organelle Biogenesis and Function, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong
Kaiyan Zhang
Areas of Excellence Centre for Organelle Biogenesis and Function, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong
Lanlan Feng
Areas of Excellence Centre for Organelle Biogenesis and Function, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong
Kai Ching Law
School of Life Sciences, Centre for Plant Vacuole Biology and Biotechnology, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong
Ka Kit Chung
School of Life Sciences, Centre for Plant Vacuole Biology and Biotechnology, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong
Yizhou Bing
Areas of Excellence Centre for Organelle Biogenesis and Function, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong
Caiji Gao
Byung-Ho Kang
Areas of Excellence Centre for Organelle Biogenesis and Function, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, School of Life Sciences, The Chinese University of Hong Kong
Xiaohong Zhuang
School of Life Sciences, Centre for Plant Vacuole Biology and Biotechnology, Centre for Cell & Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong