ATG5-HSP90.2-mediated micromitophagy as a cytological basis for maternal inheritance of plant mitochondria.

Mitochondria are inherited maternally in most plants as a classical paradigm of non-Mendelian inheritance, but the mechanism underlying paternal mitochondrial elimination (PME) remains almost unknown. We report here that angiosperms have evolved micromitophagy-mediated PME, in which vacuoles directly engulf paternal mitochondria via tonoplast invagination. We show that micromitophagy occurs specifically in male germline (MG) cells. To gain mechanistic insights, we used a vegetative-to-germline cell fate transition system to establish that micromitophagy is triggered by MG cell fate determination. We found evidence that ATG5 is translocated to vacuoles upon MG-cell-fate determination and interacts with mitochondrion-located HSP90.2 during mitochondrial engulfment by vacuoles, elucidating a cell-type-specific ATG neofunctionalization to mediate micromitophagy. This mechanism not only contributes to maternal inheritance of plant mitochondria but also supports the zygote-to-embryo transition. We further determined that micromitophagy is conserved in angiosperms but was continually optimized during evolution to support the best functioning of PME in MG cells with different properties. These findings bridge a long-standing gap in understanding plant PME with emerging mechanistic knowledge.