ABSTRACT
Autophagy is an essential degradation pathway that assists eukaryote survival under multiple stress conditions. Autophagosomes engulfing cargoes accomplish degradation only when they have matured through fusing with lysosomes or vacuoles. However, the molecular machinery mediating autophagosome maturation in plants remains unknown. Using the combined approaches of mass spectrometry, biochemistry, reverse genetics and microscopy, we uncover that UVRAG, a subunit of the class III phosphatidylinositol 3-kinase complexes in Nicotiana benthamiana, plays an essential role in autophagsome maturation via ATG14-assisted recruitment to autophagosomes and by facilitating RAB7 activation. An interaction between N. benthamiana UVRAG and ATG14 was observed in vitro and in vivo, which strikingly differed from their mutually exclusive appearance in different PI3KC3 complexes in yeast and mammals. This interaction increased the localisation of UVRAG on autophagosomes and enabled the convergence of autophagic and late endosomal structures, where they contributed to fusions between these two types of organelles by recruiting the essential membrane fusion factors RAB7 GTPase and the homotypic fusion and protein sorting (HOPS) complex. In addition, we uncovered a joint contribution of ATG14 and UVRAG to geminiviral infection, beyond autophagy. Our study provides insights into the mechanisms of autophagosome maturation in plants and expands the understanding of organisations and roles of the PI3KC3 complexes.
Subject(s)
Autophagosomes , Geminiviridae , Animals , Autophagosomes/metabolism , Geminiviridae/metabolism , Tumor Suppressor Proteins/metabolism , Autophagy/physiology , Class III Phosphatidylinositol 3-Kinases/metabolism , GTP Phosphohydrolases/metabolism , MammalsABSTRACT
Autophagy is an evolutionarily conserved catabolic process in eukaryotic cells, by which the superfluous or damaged cytoplasmic components can be delivered into vacuoles or lysosomes for degradation and recycling. Two decades of autophagy research in plants uncovers the important roles of autophagy during diverse biological processes, including development, metabolism, and various stress responses. Additionally, molecular machineries contributing to plant autophagy onset and regulation have also gradually come into people's sights. With the advancement of our knowledge of autophagy from model plants, autophagy research has expanded to include crops in recent years, for a better understanding of autophagy engagement in crop biology and its potentials in improving agricultural performance. In this review, we summarize the current research progress of autophagy in crops and discuss the autophagy-related approaches for potential agronomic trait improvement in crop plants.