Autophagy modulates Arabidopsis male gametophyte fertility and controls actin organization

Abstract

Autophagy, a crucial mechanism for cellular degradation, is regulated by conserved autophagy-related (ATG) core proteins across species. Impairments in autophagy result in significant developmental and reproductive aberrations in mammals. However, autophagy is thought to be functionally dispensable in Arabidopsis thaliana since most of the ATG mutants lack severe growth and reproductive defects. Here, we challenge this perception by unveiling a role for autophagy in male gametophyte development and fertility in Arabidopsis. A detailed re-assessment of atg5 and atg7 mutants found that reduced autophagy activity in germinated pollen accompanied by partial aberrations in sperm cell biogenesis and pollen tube growth, leading to compromised seed formation. Furthermore, we revealed autophagy modulates the spatial organization of actin filaments via targeted degradation of actin depolymerization factors ADF7 and Profilin2 in pollen grains and tubes through a key receptor, Neighbor of BRCA1 (NBR1). Our findings advance the understanding of the evolutionary conservation and diversification of autophagy in modulating male fertility in plants contrasting to mammals.