OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development

Abstract

In flowering plants, the tapetum, the innermost layer of the anther, provides both nutrient and lipid components to developing microspores, pollen grains, and the pollen coat. Though the programmed cell death of the tapetum is one of the most critical and sensitive steps for fertility and is affected by various environmental stresses, its regulatory mechanisms remain mostly unknown. Here we show that autophagy is required for the metabolic regulation and nutrient supply in anthers and that autophagic degradation within tapetum cells is essential for postmeiotic anther development in rice. Autophagosome-like structures and several vacuole-enclosed lipid bodies were observed in postmeiotic tapetum cells specifically at the uninucleate stage during pollen development, which were completely abolished in a retrotransposon-insertional OsATG7 (autophagy-related 7)-knockout mutant defective in autophagy, suggesting that autophagy is induced in tapetum cells. Surprisingly, the mutant showed complete sporophytic male sterility, failed to accumulate lipidic and starch components in pollen grains at the flowering stage, showed reduced pollen germination activity, and had limited anther dehiscence. Lipidomic analyses suggested impairment of editing of phosphatidylcholines and lipid desaturation in the mutant during pollen maturation. These results indicate a critical involvement of autophagy in a reproductive developmental process of rice, and shed light on the novel autophagy-mediated regulation of lipid metabolism in eukaryotic cells.

Autophagic Recycling Plays a Central Role in Maize Nitrogen Remobilization

“…In addition, autophagy is activated in response to other extra-or intracellular stress signals, such as endoplasmic reticulum stress, heat shock, and pathogen infection, presumably to clear abnormal/dysfunctional organelles and proteins that accumulate (Hayward and DineshKumar, 2011;Zhou et al, 2013). For rice, the ATG system has also been implicated in pollen development through control(s) on tapetal lipid metabolism (Kurusu et al, 2014).…”

Impacts of autophagy on nitrogen use efficiency in plants

“…Osatg7-1 shows delayed growth of young panicles, incomplete pollen maturation, reduced pollen germination activity, and limited anther dehiscence. A T-DNA-insertional mutant of another core ATG, OsATG9, also has a completely sterile phenotype, indicating that autophagy is critical in reproductive developmental processes in rice (Kurusu et al 2014).…”

“…An Osatg7 mutant (Osatg7-1), in which OsATG7 is disrupted by insertion of the Tos17 retrotransposon, lacks autophagy activity (Kurusu et al 2014;Izumi et al 2015). Surprisingly, unlike autophagydefective Arabidopsis and maize mutants, Osatg7-1 exhibits complete sporophytic male sterility irrespective of nutrient conditions.…”

“…Rice knockout mutants of core ATGs have recently been isolated and characterized (Kurusu et al 2014). An Osatg7 mutant (Osatg7-1), in which OsATG7 is disrupted by insertion of the Tos17 retrotransposon, lacks autophagy activity (Kurusu et al 2014;Izumi et al 2015).…”

Analysis of the role of RNS2 and autophagy in the turnover of ribosomal RNA in Arabidopsis thaliana

“…Rice, however, requires autophagy for reproductive organ development. A lack of autophagy renders plants male-sterile, and implicates autophagy in normal male gametophyte development Kurusu et al 2014). …”