Bryophyte spermiogenesis occurs through multimode autophagic and nonautophagic degradation

Abstract

Mitochondria change their morphology in response to developmental and environmental cues. During sexual reproduction, bryophytes produce spermatozoids with two mitochondria in the cell body. Although intensive morphological analyses have been conducted thus far, how this fixed number of mitochondria is realized remains unknown. Here, we investigated how mitochondria are reorganized during spermiogenesis in Marchantia polymorpha. We found that the mitochondrial number is reduced to one through fission followed by autophagic degradation during early spermiogenesis, and then the posterior mitochondrion arises by fission of the anterior mitochondrion. Autophagy is also responsible for the removal of other organelles, including peroxisomes, but these other organelles are removed at distinct developmental stages from mitochondrial degradation. We also found that spermiogenesis involves nonautophagic organelle degradation. Our findings highlight the dynamic reorganization of mitochondria, which is regulated distinctly from that of other organelles, and multiple degradation mechanisms operate in organelle remodeling during spermiogenesis in M. polymorpha.

Plant autophagosomes mature into amphisomes prior to their delivery to the central vacuole

“…Macroautophagy (hereafter autophagy) is a conserved vacuolar trafficking pathway that mediates three Rs in eukaryotic cells, including plants: (i) It remodels the cellular environment for developmental and temporary reprogramming events that underlie cellular differentiation and adaptation. In plants, for example, autophagy is essential for callus regeneration in Arabidopsis thaliana , wound-induced de-differentiation in Physcomitrium patens , sperm maturation in Marchantia polymorpha , and pollen formation in rice ( Rodriguez et al, 2020 ; Norizuki et al, 2021 Preprint ; Kurusu et al, 2014 ). Autophagy-mediated cellular adaptation is also crucial for stress tolerance including drought, infection, and high temperature stress.…”