Micromitophagy in plant spermatogenesis.

Abstract

Mitochondria of embryos in most plants and animals are inherited from the egg cell rather than the sperm cell, a phenomenon known as mitochondrial maternal inheritance. Nevertheless, how plants regulate paternal mitochondrial elimination (PME) has long remained a mystery. We discovered micromitophagy in higher plants and revealed that micromitophagy could serve as a specific mechanism underlying PME, which is triggered by fate determination of male germline (MG) cells. This process underpins maternal mitochondrial inheritance and normal early embryogenesis. Mechanistically, we demonstrate that the vacuole-localized ATG5 (autophagy-related protein 5) undergoes neofunctionalization and interacts with the mitochondrion-localized HSP90.2 (heat shock protein 90.2) to mediate paternal micromitophagy. Collectively, through interdisciplinary research on spermatogenesis, micromitophagy and mitochondrial inheritance, our work fills a long-standing gap in plant PME, and offers new insights into the functional divergence of autophagy-related genes and the adaptive evolution of autophagy.Abbreviations: PME, paternal mitochondrial elimination; 3-MA, 3-Methyladenine; ATG5, autophagy-related protein 5; HSP90.2, heat shock protein 90.2; MG, male germline; TEM, transmission electron microscopy; MVB, Multivesicular body.