Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize

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

doi:10.1105/tpc.20.00226

Cited by 69 publications

(79 citation statements)

References 93 publications

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“…The overall reduction of chloroplast lipids reported here is consistent with the more severe phenotype described previously for atg5-1 and atg7-2 mutants lines under extended darkness (Barros et al, 2017). Interestingly, slightly lower levels of unsaturated MGDG and DGDG were also observed in atg mutants under control conditions, highlighting the potential role of autophagy in basal chloroplast maintenance, as recently verified in different studies using atg mutants (McLoughlin et al, 2018, 2020; Have et al, 2019).…”

Section: Resultssupporting

confidence: 62%

“…During carbon starvation, the importance of lipid metabolism was demonstrated by the characterization of β-oxidation loss-of-function mutants (Kunz et al, 2009). In addition, autophagy association with peroxisomal protein abundance was recently demonstrated (McLoughlin et al, 2018, 2020; Have et al, 2019). The general reduction of chloroplast lipids, together with reduced LD numbers in atg 5 -1 and atg 7- 2 mutants subjected to extended darkness, raised the question of whether these lipids were being quickly oxidized to be used as energetic substrates in atg mutants.…”

Section: Resultsmentioning

confidence: 93%

“…Plants with genetic disruption of ATG genes (hereafter atg mutants) have been well characterized for sensitivity to several stresses, particularly nutrient starvation (Avin-Wittenberg, 2018). The importance of autophagy in plants has been mostly associated with the recycling of proteins to amino acids under starvation conditions (Li et al, 2014, Izumi et al, 2013; Barros et al, 2017: Hirota et al, 2018; Mcloughin et al, 2018, 2020). By contrast, in mammals and yeast, autophagy has been largely associated not only with proteins but also with lipid metabolism (Elander et al, 2018; Barros et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…Notably, this study was based on the analysis of Aradiposis mutants overexpressing the LD marker OLE1-GFP and knockout for SUGAR DEPENDENT-1 (SDP1) lipase, which are genotypes with altered LD and TAG metabolism (Fan et al, 2013, 2017). In maize ( Zea mays ), atg12-1 mutant presented a higher LD number, which could reflect active LD assembly or disruption of LD catabolism (Mcloughin et al, 2020). It remains contentious, however, whether autophagy mediates the biogenesis or degradation of LDs in vegetative tissues (Elander et al, 2018; Barros et al, 2020; Masclaux-Daubresse et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…It remains contentious, however, whether autophagy mediates the biogenesis or degradation of LDs in vegetative tissues (Elander et al, 2018; Barros et al, 2020; Masclaux-Daubresse et al, 2020). Although recent studies have clearly revealed an interplay between autophagy and lipid metabolism (Mcloughin et al,2018, 2020; Have et al, 2019; Fan et al, 2019), relatively little is known about the role of autophagy in the mobilization of lipid components under energy limitation conditions.…”

Section: Introductionmentioning

confidence: 99%

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Autophagy is required for lipid homeostasis during dark-induced senescence in Arabidopsis

Barros

Magen

Lapidot-Cohen

et al. 2020

Preprint

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Autophagy is an evolutionarily conserved mechanism that mediates the degradation of cytoplasmic components in eukaryotic cells. In plants, autophagy has been extensively associated with the recycling of proteins during carbon starvation conditions. Even tough lipids constitute a significant energy reserve, our understanding of the function of autophagy in the management of cell lipid reserves and components remains fragmented. To further investigate the significance of autophagy in lipid metabolism, we performed an extensive lipidomic characterization of Arabidopsis (Arabidopsis thaliana) autophagy mutants (atg) submitted to dark-induced senescence conditions. Our results revealed an altered lipid profile in atg mutants, suggesting that autophagy affects the homeostasis of multiple lipid components under dark-induced senescence. The acute degradation of chloroplast lipids coupled with the differential accumulation of triacylglycerols (TAGs) and plastoglobuli-related transcripts indicates an alternative metabolic reprogramming towards lipid storage in atg mutants. The imbalance of lipid metabolism compromises the production of cytosolic lipid droplets and the regulation of peroxisomal lipid oxidation pathways in atg mutants.One-sentence summaryAutophagy is required for the mobilization of membrane lipid components and lipid droplet dynamics during extended darkness in Arabidopsis.

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Section: Resultssupporting

confidence: 62%

Section: Resultsmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Autophagy is required for lipid homeostasis during dark-induced senescence in Arabidopsis

Barros

Magen

Lapidot-Cohen

et al. 2020

Preprint

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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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Crossing paths: recent insights in the interplay between autophagy and intracellular trafficking in plants

Gouguet

Üstün

2022

FEBS Letters

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Autophagy fulfills a crucial role in plant cellular homeostasis by recycling diverse cellular components ranging from protein complexes to whole organelles. Autophagy cargos are shuttled to the vacuole for degradation, thereby completing the recycling process. Canonical autophagy requires the lipidation and insertion of ATG8 proteins into double-membrane structures, termed autophagosomes, which engulf the cargo to be degraded. As such, the autophagy pathway actively contributes to intracellular membrane trafficking. Yet, the autophagic process is not fully considered a bona fide component of the canonical membrane trafficking pathway. However, recent findings have started to pinpoint the interconnection between classical membrane trafficking pathways and autophagy. This review details the latest advances in our comprehension of the interplay between these two pathways. Understanding the overlap between autophagy and canonical membrane trafficking pathways is important to illuminate the inner workings of both pathways in plant cells.

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Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize

Abstract: Autophagy is critical for recycling amino acids and nitrogenrich nucleotides, adjusting respiratory substrates, and the retention of assimilated nitrogen during fixed-carbon starvation.

Cited by 69 publications

References 93 publications

Autophagy is required for lipid homeostasis during dark-induced senescence in Arabidopsis

Autophagy is required for lipid homeostasis during dark-induced senescence in Arabidopsis

Metabolism and autophagy in plants—a perfect match

Crossing paths: recent insights in the interplay between autophagy and intracellular trafficking in plants

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