Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover

McLoughlin, Fionn; Augustine, Robert C.; Marshall, Richard S.; Li, Faqiang; Kirkpatrick, Liam D.; Otegui, Marisa S.; Vierstra, R.D.

doi:10.1038/s41477-018-0299-2

Cited by 122 publications

(142 citation statements)

References 80 publications

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“…Recently McLoughlin et al . () confirmed flavonoids modifications in the atg12 maize mutant that were also associated to changes in the abundance of the transcript of their biosynthetic enzymes.…”

Section: Discussionmentioning

confidence: 99%

“…The fact that proteomic analysis reveals an accumulation of peroxisome proteins in atg5 and atg5/sid2 could reflect a lower pexophagy rate in autophagy mutants, as suggested by McLoughlin et al . (). However, the fact that many of the overaccumulated peroxisomal proteins are dedicated to the amino acid and lipid catabolisms is in good accordance with the decay of chloroplast and a role of β‐oxidation in alternative energy supply.…”

Section: Discussionmentioning

confidence: 99%

“…They provided several lines of evidence that autophagy plays an important role in plant adaptation to stresses (Liu et al ., for a review). Dysregulations of sugar, amino acid and lipid contents were investigated (Izumi et al ., ; Kurusu et al ., ; Masclaux‐Daubresse et al ., ; Avin‐Wittenberg et al ., ; McLoughlin et al ., ). The transcriptomic study performed by Masclaux‐Daubresse et al .…”

Section: Introductionmentioning

confidence: 99%

“…(), confirmed many of the metabolic features found in Arabidopsis. From proteome/transcriptome comparisons, authors established the role of autophagy in clearing peroxisomes, Golgi bodies, ER, ribosomes and proteasome, and found possible role of autophagy in regulating fatty acid catabolism (McLoughlin et al ., ).…”

Section: Introductionmentioning

confidence: 99%

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Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition

et al. 2019

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Summary Autophagy is a universal mechanism in eukaryotic cells that facilitates the degradation of unwanted cell constituents and is essential for cell homeostasis and nutrient recycling. The salicylic acid‐independent effects of autophagy defects on leaf metabolism were determined through large‐scale proteomic and lipidomic analyses of atg5 and atg5/sid2 mutants under different nitrogen and sulfur growth conditions. Results revealed that irrespective of the growth conditions, plants carrying the atg5 mutation presented all the characteristics of endoplasmic reticulum (ER) stress. Increases in peroxisome and ER proteins involved in very long chain fatty acid synthesis and β‐oxidation indicated strong modifications of lipid metabolism. Lipidomic analyses revealed changes in the concentrations of sphingolipids, phospholipids and galactolipids. Significant accumulations of phospholipids and ceramides and changes in GIPCs (glycosyl‐inositol‐phosphoryl‐ceramides) in atg5 mutants indicated large modifications in endomembrane‐lipid and especially plasma membrane‐lipid composition. Decreases in chloroplast proteins and galactolipids in atg5 under low nutrient conditions, indicated that chloroplasts were used as lipid reservoirs for β‐oxidation in atg5 mutants. In conclusion, this report demonstrates the strong impact of autophagy defect on ER stress and reveals the role of autophagy in the control of plant lipid metabolism and catabolism, influencing both lipid homeostasis and endomembrane composition.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition

et al. 2019

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“…Disruption of autophagy has been shown to affect lipid turnover in maize (Zea mays;McLoughlin et al, 2018) and Arabidopsis seedlings under carbon starvation (Avin-Wittenberg et al, 2015), but whether lipophagy occurs in Arabidopsis and the molecular mechanism involved remain unknown.…”

Section: Introductionmentioning

confidence: 99%

Dual Role for Autophagy in Lipid Metabolism in Arabidopsis

Fan

2019

Plant Cell

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Autophagy is a major catabolic pathway whereby cytoplasmic constituents including lipid droplets (LDs), storage compartments for neutral lipids, are delivered to the lysosome or vacuole for degradation. The autophagic degradation of cytosolic LDs, a process termed lipophagy, has been extensively studied in yeast and mammals, but little is known about the role for autophagy in lipid metabolism in plants. Organisms maintain a basal level of autophagy under favorable conditions and upregulate the autophagic activity under stress including starvation. Here, we demonstrate that Arabidopsis (Arabidopsis thaliana) basal autophagy contributes to triacylglycerol (TAG) synthesis, whereas inducible autophagy contributes to LD degradation. We found that disruption of basal autophagy impedes organellar membrane lipid turnover and hence fatty acid mobilization from membrane lipids to TAG. We show that lipophagy is induced under starvation as indicated by colocalization of LDs with the autophagic marker and the presence of LDs in vacuoles. We additionally show that lipophagy occurs in a process morphologically resembling microlipophagy and requires the core components of the macroautophagic machinery. Together, this study provides mechanistic insight into lipophagy and reveals a dual role for autophagy in regulating lipid synthesis and turnover in plants.

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Metabolism and autophagy in plants—a perfect match

et al. 2022

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Autophagy is a eukaryotic cellular transport mechanism that delivers intracellular macromolecules, proteins, and even organelles to a lytic organelle (vacuole in yeast and plants/lysosome in animals) for degradation and nutrient recycling. The process is mediated by highly conserved autophagy-related (ATG) proteins. In plants, autophagy maintains cellular homeostasis under favorable conditions, guaranteeing normal plant growth and fitness. Severe stress such as nutrient starvation and plant senescence further induce it, thus ensuring plant survival under unfavorable conditions by providing nutrients through the removal of damaged or aged proteins, or organelles. In this article, we examine the interplay between metabolism and autophagy, focusing on the different aspects of this reciprocal relationship. We show that autophagy has a strong influence on a range of metabolic processes, whereas at the same time, even single metabolites can activate autophagy. We highlight the involvement of ATG genes in metabolism, examine the role of the macronutrients carbon and nitrogen, and various micronutrients, and take a closer look at how the interaction between autophagy and metabolism impacts on plant phenotypes and yield.

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Maize multi-omics reveal roles for autophagic recycling in proteome remodelling and lipid turnover

Cited by 122 publications

References 80 publications

Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition

Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition

Dual Role for Autophagy in Lipid Metabolism in Arabidopsis

Metabolism and autophagy in plants—a perfect match

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