Autophagic Recycling Plays a Central Role in Maize Nitrogen Remobilization

Abstract

Autophagy is a primary route for nutrient recycling in plants by which superfluous or damaged cytoplasmic material and organelles are encapsulated and delivered to the vacuole for breakdown. Central to autophagy is a conjugation pathway that attaches AUTOPHAGY-RELATED8 (ATG8) to phosphatidylethanolamine, which then coats emerging autophagic membranes and helps with cargo recruitment, vesicle enclosure, and subsequent vesicle docking with the tonoplast. A key component in ATG8 function is ATG12, which promotes lipidation upon its attachment to ATG5. Here, we fully defined the maize (Zea mays) ATG system transcriptionally and characterized it genetically through atg12 mutants that block ATG8 modification. atg12 plants have compromised autophagic transport as determined by localization of a YFP-ATG8 reporter and its vacuolar cleavage during nitrogen or fixed-carbon starvation. Phenotypic analyses showed that atg12 plants are phenotypically normal and fertile when grown under nutrient-rich conditions. However, when nitrogen-starved, seedling growth is severely arrested, and as the plants mature, they show enhanced leaf senescence and stunted ear development. Nitrogen partitioning studies revealed that remobilization is impaired in atg12 plants, which significantly decreases seed yield and nitrogen-harvest index.Together, our studies demonstrate that autophagy, while nonessential, becomes critical during nitrogen stress and severely impacts maize productivity under suboptimal field conditions.

Impacts of autophagy on nitrogen use efficiency in plants

“…In plants, ATG8 is encoded by a large multigene family: Arabidopsis has nine ATG8 genes (AtATG8a-i) (Yoshimoto et al 2004), maize has five (ZmATG8a-e) (Li et al 2015a), and the rice genome has five to seven ATG8 gene candidates (Chung et al 2009;Xia et al 2011). The biological significance of ATG8 multigene families in plants is currently not known, and it is not clear whether different ATG8 proteins have different cargo specificities, or whether they are redundant.…”

“…Maize autophagy-deficient mutants, harboring the core ATG ZmATG12 inactivated by insertion of the UniformMu transposon, have recently been isolated and physiologically analyzed (Li et al 2015a). Under low-N conditions, Zmatg12 mutants show a delayed growth stage, and reduced leaf elongation and ear development.…”

“…The remobilization of N from senescing leaves to growing organs is particularly important in NUE (MasclauxDaubresse et al 2010). Recent studies have shown that autophagy, a eukaryotic process whereby cellular components are degraded in bulk, is crucial for N remobilization in Arabidopsis (Guiboileau et al 2012), maize (Li et al 2015a), and rice .…”

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

“…When genes involved in autophagosome biogenesis are knocked-out, plants can still complete a full life cycle under normal growing conditions. Autophagy mutants, however, often show some developmental phenotypes, such as decreased plant size or reduced seed yield, suggesting autophagy is required for normal development Li et al 2015). Rice, however, requires autophagy for reproductive organ development.…”

“…In fact, the majority of leaf nitrogen is found in the chloroplast photosynthetic enzyme rubisco. Autophagy is involved in this re-mobilization of nutrients from the leaves and in the shrinkage and degradation of chloroplasts Wada et al 2009;Guiboileau et al 2013;Li et al 2015). Although mutant Arabidopsis plants defective in autophagy are able to proliferate under normal conditions, they do show earlier leaf senescence and accelerated bolting compared to wild-type plants, implicating autophagy in some developmental processes (Yoshimoto et al 2010;.…”