ATG5-HSP90.2-mediated micromitophagy as 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 a micromitophagy-mediated PME, in which vacuoles directly engulf paternal mitochondria via tonoplast invagination. We show that the 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 evidence that ATG5 is translocated to vacuole 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. The ingenious mechanism not only contributes to maternal inheritance of plant mitochondria, but also supports zygote-to-embryo transition. We further determine that micromitophagy is conserved in angiosperms but was continually optimized during evolution to ensure a highly efficient PME strategy in MG cells with different properties. These findings bridge a long-standing gap in understanding plant PME with emerging mechanistic knowledge.