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Cells
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Advances in the Plant Autophagy
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Advances in the Plant Autophagy

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (29 February 2020) | Viewed by 51820

Special Issue Editors

Prof. Agnieszka Sirko

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Guest Editor
Institute of Biochemistry and Biophysics of the Polish Academy of Sciences, 02-106 Warsaw, Poland
Interests: selective autophagy in plants; Arabidopsis; sulfur starvation; autophagy cargo receptors; NBR1; protein interaction; gene expression regulation; cysteine; abscisic acid
Prof. Celine Masclaux-Daubresse

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Guest Editor
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, 78000 Versailles, France
Interests: nutrient recycling; plant senescence; autophagy; nitrogen use efficiency

Special Issue Information

Dear Colleagues,

Autophagy is defined as a catabolic process participating in the degradation of intracellular components. It is a highly conserved eukaryotic process involving numerous autophagy-related (ATG) proteins and protein complexes responsible for the initiation and formation of the double-membrane vesicle (autophagosome) and its intracellular transport and fusion with the vacuolar membrane, where its cargo is degraded. The autophagy process and its regulation are relatively well characterized in animals but its details in plants are less known. Autophagy is implicated in almost every aspect of plant growth and development, from embryogenesis to leaf senescence. Plant mutants defective in the autophagy process are hypersensitive to carbon and nitrogen starvation and display early senescence even under nutrient-rich conditions. Autophagy contributes to nutrients remobilization not only during nutrient starvation but also during organ senescence and is involved in nitrogen remobilization from the senescing leaves to the seeds. It promotes plant survival under nutrients deficiency and supports plant tolerance to a plethora of stresses. It is also implicated in plant defence against pathogens. Autophagy must be well controlled to avoid excessive degradation of the cellular content. At the stage of initiation, it is negativelly controlled by the Target of Rapamycin (TOR) kinase. One could expect that the autophagy activity (or autophagy flux) is regulated by posttranslational protein modifications, but also other levels of control are possible. For example, transciption factors regulating the expression of ATG genes in Arabidopais thaliana were recently identified. Moreover, autophagy does not simply entail the bulk degradation of the cellular content but it can be highly selective. Cargo selectivity in autophagy is ensured by the involvement of proteins called selective autophagy cargo receptors, which specifically recognize the cellular elements marked for degradation.

This Special Issue of Cells will help us to improve the general knowledge about the autophagy process in plants. Both experimental papers revealing various aspects of autophagy in plants and algae and review articles are welcome.

Prof. Agnieszka Sirko
Prof. Celine Masclaux-Daubresse
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Cells is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • autophagy flux
  • nutrients recycling
  • autophagy cargo receptors
  • selective autophagy
  • crosstalk of autophagy with phytohormons
  • autophagy initiation
  • ATG
  • autophagosome
  • autophagy in plant stress
  • autophagy in plant development

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Published Papers (10 papers)

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Editorial

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3 pages, 206 KiB  
Editorial
Advances in Plant Autophagy
by Agnieszka Sirko and Céline Masclaux-Daubresse
Cells 2021, 10(1), 194; https://doi.org/10.3390/cells10010194 - 19 Jan 2021
Cited by 1 | Viewed by 3833
Abstract
Ubiquitin–proteasome and lysosome–autophagy are the two main cellular degradation systems controlling cellular homeostasis in eukaryotes [...] Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)

Research

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18 pages, 1765 KiB  
Article
Transcriptional Plasticity of Autophagy-Related Genes Correlates with the Genetic Response to Nitrate Starvation in Arabidopsis Thaliana
by Magali Bedu, Anne Marmagne, Céline Masclaux-Daubresse and Fabien Chardon
Cells 2020, 9(4), 1021; https://doi.org/10.3390/cells9041021 - 20 Apr 2020
Cited by 14 | Viewed by 3321
Abstract
In eukaryotes, autophagy, a catabolic mechanism for macromolecule and protein recycling, allows the maintenance of amino acid pools and nutrient remobilization. For a better understanding of the relationship between autophagy and nitrogen metabolism, we studied the transcriptional plasticity of autophagy genes (ATG [...] Read more.
In eukaryotes, autophagy, a catabolic mechanism for macromolecule and protein recycling, allows the maintenance of amino acid pools and nutrient remobilization. For a better understanding of the relationship between autophagy and nitrogen metabolism, we studied the transcriptional plasticity of autophagy genes (ATG) in nine Arabidopsis accessions grown under normal and nitrate starvation conditions. The status of the N metabolism in accessions was monitored by measuring the relative expression of 11 genes related to N metabolism in rosette leaves. The transcriptional variation of the genes coding for enzymes involved in ammonium assimilation characterize the genetic diversity of the response to nitrate starvation. Starvation enhanced the expression of most of the autophagy genes tested, suggesting a control of autophagy at transcriptomic level by nitrogen. The diversity of the gene responses among natural accessions revealed the genetic variation existing for autophagy independently of the nutritive condition, and the degree of response to nitrate starvation. We showed here that the genetic diversity of the expression of N metabolism genes correlates with that of the ATG genes in the two nutritive conditions, suggesting that the basal autophagy activity is part of the integral response of the N metabolism to nitrate availability. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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22 pages, 9422 KiB  
Article
Overexpression of the Selective Autophagy Cargo Receptor NBR1 Modifies Plant Response to Sulfur Deficit
by Leszek Tarnowski, Milagros Collados Rodriguez, Jerzy Brzywczy, Dominik Cysewski, Anna Wawrzynska and Agnieszka Sirko
Cells 2020, 9(3), 669; https://doi.org/10.3390/cells9030669 - 10 Mar 2020
Cited by 20 | Viewed by 5146
Abstract
Plants exposed to sulfur deficit elevate the transcription of NBR1 what might reflect an increased demand for NBR1 in such conditions. Therefore, we investigated the role of this selective autophagy cargo receptor in plant response to sulfur deficit (-S). Transcriptome analysis of the [...] Read more.
Plants exposed to sulfur deficit elevate the transcription of NBR1 what might reflect an increased demand for NBR1 in such conditions. Therefore, we investigated the role of this selective autophagy cargo receptor in plant response to sulfur deficit (-S). Transcriptome analysis of the wild type and NBR1 overexpressing plants pointed out differences in gene expression in response to -S. Our attention focused particularly on the genes upregulated by -S in roots of both lines because of significant overrepresentation of cytoplasmic ribosomal gene family. Moreover, we noticed overrepresentation of the same family in the set of proteins co-purifying with NBR1 in -S. One of these ribosomal proteins, RPS6 was chosen for verification of its direct interaction with NBR1 and proven to bind outside the NBR1 ubiquitin binding domains. The biological significance of this novel interaction and the postulated role of NBR1 in ribosomes remodeling in response to starvation remain to be further investigated. Interestingly, NBR1 overexpressing seedlings have significantly shorter roots than wild type when grown in nutrient deficient conditions in the presence of TOR kinase inhibitors. This phenotype probably results from excessive autophagy induction by the additive effect of NBR1 overexpression, starvation, and TOR inhibition. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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18 pages, 7059 KiB  
Article
Autophagy Controls Sulphur Metabolism in the Rosette Leaves of Arabidopsis and Facilitates S Remobilization to the Seeds
by Aurélia Lornac, Marien Havé, Fabien Chardon, Fabienne Soulay, Gilles Clément, Jean-Christophe Avice and Céline Masclaux-Daubresse
Cells 2020, 9(2), 332; https://doi.org/10.3390/cells9020332 - 31 Jan 2020
Cited by 23 | Viewed by 3268
Abstract
Sulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, [...] Read more.
Sulphur deficiency in crops became an agricultural concern several decades ago, due to the decrease of S deposition and the atmospheric sulphur dioxide emissions released by industrial plants. Autophagy, which is a conserved mechanism for nutrient recycling in eukaryotes, is involved in nitrogen, iron, zinc and manganese remobilizations from the rosette to the seeds in Arabidopsis thaliana. Here, we have compared the role of autophagy in sulphur and nitrogen management at the whole plant level, performing concurrent labelling with 34S and 15N isotopes on atg5 mutants and control lines. We show that both 34S and 15N remobilizations from the rosette to the seeds are impaired in the atg5 mutants irrespective of salicylic acid accumulation and of sulphur nutrition. The comparison in each genotype of the partitions of 15N and 34S in the seeds (as % of the whole plant) indicates that the remobilization of 34S to the seeds was twice more efficient than that of 15N in both autophagy mutants and control lines under high S conditions, and also in control lines under low S conditions. This was different in the autophagy mutants grown under low S conditions. Under low S, the partition of 34S to their seeds was indeed not twice as high but similar to that of 15N. Such discrepancy shows that when sulphate availability is scarce, autophagy mutants display stronger defects for 34S remobilization relative to 15N remobilization than under high S conditions. It suggests, moreover, that autophagy mainly affects the transport of N-poor S-containing molecules and possibly sulphate. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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16 pages, 3658 KiB  
Article
Is Autophagy Involved in Pepper Fruit Ripening?
by Omar López-Vidal, Adela Olmedilla, Luisa María Sandalio, Francisca Sevilla and Ana Jiménez
Cells 2020, 9(1), 106; https://doi.org/10.3390/cells9010106 - 1 Jan 2020
Cited by 17 | Viewed by 4237
Abstract
Autophagy is a universal self-degradation process involved in the removal and recycling of cellular constituents and organelles; however, little is known about its possible role in fruit ripening, in which the oxidation of lipids and proteins and changes in the metabolism of different [...] Read more.
Autophagy is a universal self-degradation process involved in the removal and recycling of cellular constituents and organelles; however, little is known about its possible role in fruit ripening, in which the oxidation of lipids and proteins and changes in the metabolism of different cellular organelles occur. In this work, we analyzed several markers of autophagy in two critical maturation stages of pepper (Capsicum annuum L.) fruits where variations due to ripening become clearly visible. Using two commercial varieties that ripen to yellow and red fruits respectively, we studied changes in the gene expression and protein content of several autophagy (ATG) components, ATG4 activity, as well as the autophagy receptor NBR1 and the proteases LON1 and LON2. Additionally, the presence of intravacuolar vesicles was analyzed by electron microscopy. Altogether, our data reveal that autophagy plays a role in the metabolic changes which occur during ripening in the two studied varieties, suggesting that this process may be critical to acquiring final optimal quality of pepper fruits. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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Review

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13 pages, 655 KiB  
Review
Microautophagy in Plants: Consideration of Its Molecular Mechanism
by Katarzyna Sieńko, Andisheh Poormassalehgoo, Kenji Yamada and Shino Goto-Yamada
Cells 2020, 9(4), 887; https://doi.org/10.3390/cells9040887 - 4 Apr 2020
Cited by 47 | Viewed by 6961
Abstract
Microautophagy is a type of autophagy. It is characterized by direct enclosing with the vacuolar/lysosomal membrane, which completes the isolation and uptake of cell components in the vacuole. Several publications present evidence that plants exhibit microautophagy. Plant microautophagy is involved in anthocyanin accumulation [...] Read more.
Microautophagy is a type of autophagy. It is characterized by direct enclosing with the vacuolar/lysosomal membrane, which completes the isolation and uptake of cell components in the vacuole. Several publications present evidence that plants exhibit microautophagy. Plant microautophagy is involved in anthocyanin accumulation in the vacuole, eliminating damaged chloroplasts and degrading cellular components during starvation. However, information on the molecular mechanism of microautophagy is less available than that on the general macroautophagy, because the research focusing on microautophagy has not been widely reported. In yeast and animals, it is suggested that microautophagy can be classified into several types depending on morphology and the requirements of autophagy-related (ATG) genes. This review summarizes the studies on plant microautophagy and discusses possible techniques for a future study in this field while taking into account the information on microautophagy obtained from yeast and animals. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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19 pages, 703 KiB  
Review
Coordination and Crosstalk between Autophagosome and Multivesicular Body Pathways in Plant Stress Responses
by Mengxue Wang, Xifeng Li, Shuwei Luo, Baofang Fan, Cheng Zhu and Zhixiang Chen
Cells 2020, 9(1), 119; https://doi.org/10.3390/cells9010119 - 3 Jan 2020
Cited by 20 | Viewed by 4754
Abstract
In eukaryotic cells, autophagosomes and multivesicular bodies (MVBs) are two closely related partners in the lysosomal/vacuolar protein degradation system. Autophagosomes are double membrane-bound organelles that transport cytoplasmic components, including proteins and organelles for autophagic degradation in the lysosomes/vacuoles. MVBs are single-membrane organelles in [...] Read more.
In eukaryotic cells, autophagosomes and multivesicular bodies (MVBs) are two closely related partners in the lysosomal/vacuolar protein degradation system. Autophagosomes are double membrane-bound organelles that transport cytoplasmic components, including proteins and organelles for autophagic degradation in the lysosomes/vacuoles. MVBs are single-membrane organelles in the endocytic pathway that contain intraluminal vesicles whose content is either degraded in the lysosomes/vacuoles or recycled to the cell surface. In plants, both autophagosome and MVB pathways play important roles in plant responses to biotic and abiotic stresses. More recent studies have revealed that autophagosomes and MVBs also act together in plant stress responses in a variety of processes, including deployment of defense-related molecules, regulation of cell death, trafficking and degradation of membrane and soluble constituents, and modulation of plant hormone metabolism and signaling. In this review, we discuss these recent findings on the coordination and crosstalk between autophagosome and MVB pathways that contribute to the complex network of plant stress responses. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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16 pages, 2103 KiB  
Review
Structural Biology and Electron Microscopy of the Autophagy Molecular Machinery
by Louis Tung Faat Lai, Hao Ye, Wenxin Zhang, Liwen Jiang and Wilson Chun Yu Lau
Cells 2019, 8(12), 1627; https://doi.org/10.3390/cells8121627 - 12 Dec 2019
Cited by 11 | Viewed by 5553
Abstract
Autophagy is a highly regulated bulk degradation process that plays a key role in the maintenance of cellular homeostasis. During autophagy, a double membrane-bound compartment termed the autophagosome is formed through de novo nucleation and assembly of membrane sources to engulf unwanted cytoplasmic [...] Read more.
Autophagy is a highly regulated bulk degradation process that plays a key role in the maintenance of cellular homeostasis. During autophagy, a double membrane-bound compartment termed the autophagosome is formed through de novo nucleation and assembly of membrane sources to engulf unwanted cytoplasmic components and targets them to the lysosome or vacuole for degradation. Central to this process are the autophagy-related (ATG) proteins, which play a critical role in plant fitness, immunity, and environmental stress response. Over the past few years, cryo-electron microscopy (cryo-EM) and single-particle analysis has matured into a powerful and versatile technique for the structural determination of protein complexes at high resolution and has contributed greatly to our current understanding of the molecular mechanisms underlying autophagosome biogenesis. Here we describe the plant-specific ATG proteins and summarize recent structural and mechanistic studies on the protein machinery involved in autophagy initiation with an emphasis on those by single-particle analysis. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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14 pages, 849 KiB  
Review
The Ins and Outs of Autophagic Ribosome Turnover
by Zakayo Kazibwe, Ang-Yu Liu, Gustavo C. MacIntosh and Diane C. Bassham
Cells 2019, 8(12), 1603; https://doi.org/10.3390/cells8121603 - 10 Dec 2019
Cited by 21 | Viewed by 6744
Abstract
Ribosomes are essential for protein synthesis in all organisms and their biogenesis and number are tightly controlled to maintain homeostasis in changing environmental conditions. While ribosome assembly and quality control mechanisms have been extensively studied, our understanding of ribosome degradation is limited. In [...] Read more.
Ribosomes are essential for protein synthesis in all organisms and their biogenesis and number are tightly controlled to maintain homeostasis in changing environmental conditions. While ribosome assembly and quality control mechanisms have been extensively studied, our understanding of ribosome degradation is limited. In yeast or animal cells, ribosomes are degraded after transfer into the vacuole or lysosome by ribophagy or nonselective autophagy, and ribosomal RNA can also be transferred directly across the lysosomal membrane by RNautophagy. In plants, ribosomal RNA is degraded by the vacuolar T2 ribonuclease RNS2 after transport by autophagy-related mechanisms, although it is unknown if a selective ribophagy pathway exists in plants. In this review, we describe mechanisms of turnover of ribosomal components in animals and yeast, and, then, discuss potential pathways for degradation of ribosomal RNA and protein within the vacuole in plants. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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17 pages, 2397 KiB  
Review
Autophagy and Nutrients Management in Plants
by Qinwu Chen, Daiki Shinozaki, Jie Luo, Mathieu Pottier, Marien Havé, Anne Marmagne, Michèle Reisdorf-Cren, Fabien Chardon, Sébastien Thomine, Kohki Yoshimoto and Céline Masclaux-Daubresse
Cells 2019, 8(11), 1426; https://doi.org/10.3390/cells8111426 - 12 Nov 2019
Cited by 46 | Viewed by 6861
Abstract
Nutrient recycling and mobilization from organ to organ all along the plant lifespan is essential for plant survival under changing environments. Nutrient remobilization to the seeds is also essential for good seed production. In this review, we summarize the recent advances made to [...] Read more.
Nutrient recycling and mobilization from organ to organ all along the plant lifespan is essential for plant survival under changing environments. Nutrient remobilization to the seeds is also essential for good seed production. In this review, we summarize the recent advances made to understand how plants manage nutrient remobilization from senescing organs to sink tissues and what is the contribution of autophagy in this process. Plant engineering manipulating autophagy for better yield and plant tolerance to stresses will be presented. Full article
(This article belongs to the Special Issue Advances in the Plant Autophagy)
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