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New Insight into Signaling and Autophagy in Plants

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (31 March 2021) | Viewed by 52382

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Dr. Sławomir Borek

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Department of Plant Physiology, Faculty of Biology, Adam Mickiewicz University, 61-712 Poznań, Poland
Interests: autophagy; pexophagy; plant physiology; plant cell biology; plant molecular biology; lipid metabolism; seed development and germination; transcriptomics; proteomics
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Dr. Małgorzata Pietrowska-Borek

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Faculty of Agronomy, Horticulture and Bioengineering, Poznań University of Life Sciences, Poznań, Poland
Interests: abiotic and biotic stress; autophagy; cell signaling; cyclic nucleotides; uncommon nucleotides; molecular plant physiology; plant biochemistry; plant biotechnology; plant cell biology; plant molecular biology; plant tissue culture; signal transduction pathways
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

During the entire ontogenesis plants are forced to sense signals, react, and adapt to changing and often adverse environmental conditions. Intracellular signal networks are involved in activating, regulating, and silencing various plant responses to environmental stimuli. Plants must also possess systems to exchange information throughout the entire organism to ensure the coordination of development and defense. The signaling systems transmitting this information are complex and involve multiple components, which are far from being understood.

One of the processes that enable plants to respond efficiently to a changing environment, both internal and external, is autophagy. The efficient functioning of autophagy ensures proper growth and development of plants at every stage of ontogenesis. Under normal conditions, autophagy is a housekeeping process, allowing the recycling of damaged or unnecessary organelles and protein complexes, and under various types of biotic and abiotic stresses can be an essential element of plant defense responses. The autophagic turnover of organelles and protein complexes occurs in a controlled and selective manner. The attention of many scientists is currently focused on identifying the elements of signaling pathways and the mechanisms of marking, recognizing, and directing particular cell components to autophagic degradation in the vacuole.

This Special Issue will publish original research papers, reviews, short reviews, opinion articles, and hypotheses within the scope of the newest discoveries in signaling and autophagy in plants. In particular, we welcome papers showing molecular data on signal perception and transduction as well as selective types of autophagy in plants.

Dr. Sławomir Borek
Dr. Małgorzata Pietrowska-Borek
Guest Editors

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Keywords

Autophagy cargo receptors
Autophagy in plant development
Autophagy in plant stress
Crosstalk between autophagy and phytohormones
Plant cell homeostasis
Nutrients recycling
Plant cell biology
Plant signal transduction
Selective autophagy
Signaling molecules

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Related Special Issues

New Insight into Signaling and Autophagy in Plants 2.0 in International Journal of Molecular Sciences (9 articles)
New Insight into Signaling and Autophagy in Plants 3.0 in International Journal of Molecular Sciences (3 articles)

Published Papers (13 papers)

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Research

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13 pages, 24561 KiB

Open AccessArticle

Silencing Autophagy-Related Gene 2 (ATG2) Results in Accelerated Senescence and Enhanced Immunity in Soybean

by Said M. Hashimi, Ni-Ni Wu, Jie Ran and Jian-Zhong Liu

Int. J. Mol. Sci. 2021, 22(21), 11749; https://doi.org/10.3390/ijms222111749 - 29 Oct 2021

Cited by 17 | Viewed by 2606

Abstract

Autophagy plays a critical role in nutrient recycling and stress adaptations. However, the role of autophagy has not been extensively investigated in crop plants. In this study, soybean autophagy-related gene 2 (GmATG2) was silenced, using virus-induced silencing (VIGS) mediated by Bean pod mottle virus (BPMV). An accelerated senescence phenotype was exclusively observed for the GmATG2-silenced plants under dark conditions. In addition, significantly increased accumulation of both ROS and SA as well as a significantly induced expression of the pathogenesis-related gene 1 (PR1) were also observed on the leaves of the GmATG2-silenced plants, indicating an activated immune response. Consistent with this, GmATG2-silenced plants exhibited a significantly enhanced resistance to Pseudomonas syringae pv. glycinea (Psg) relative to empty vector control plants (BPMV-0). Notably, the activated immunity of the GmATG2-silenced plants was independent of the MAPK signaling pathway. The fact that the accumulation levels of ATG8 protein and poly-ubiquitinated proteins were significantly increased in the dark-treated GmATG2-silenced plants relative to the BPMV-0 plants indicated that the autophagic degradation is compromised in the GmATG2-silenced plants. Together, our results indicated that silencing GmATG2 compromises the autophagy pathway, and the autophagy pathway is conserved in different plant species. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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14 pages, 31638 KiB

Open AccessArticle

Autophagy Mediates the Degradation of Plant ESCRT Component FREE1 in Response to Iron Deficiency

by Tianrui Zhang, Zhidan Xiao, Chuanliang Liu, Chao Yang, Jiayi Li, Hongbo Li, Caiji Gao and Wenjin Shen

Int. J. Mol. Sci. 2021, 22(16), 8779; https://doi.org/10.3390/ijms22168779 - 16 Aug 2021

Cited by 10 | Viewed by 3317

Abstract

Multivesicular body (MVB)-mediated endosomal sorting and macroautophagy are the main pathways mediating the transport of cellular components to the vacuole and are essential for maintaining cellular homeostasis. The interplay of these two pathways remains poorly understood in plants. In this study, we show that FYVE DOMAIN PROTEIN REQUIRED FOR ENDOSOMAL SORTING 1 (FREE1), which was previously identified as a plant-specific component of the endosomal sorting complex required for transport (ESCRT), essential for MVB biogenesis and plant growth, can be transported to the vacuole for degradation in response to iron deficiency. The vacuolar transport of ubiquitinated FREE1 protein is mediated by the autophagy pathway. As a consequence, the autophagy deficient mutants, atg5-1 and atg7-2, accumulate more endogenous FREE1 protein and display hypersensitivity to iron deficiency. Furthermore, under iron-deficient growth condition autophagy related genes are upregulated to promote the autophagic degradation of FREE1, thereby possibly relieving the repressive effect of FREE1 on iron absorption. Collectively, our findings demonstrate a unique regulatory mode of protein turnover of the ESCRT machinery through the autophagy pathway to respond to iron deficiency in plants. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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12 pages, 31317 KiB

Open AccessArticle

Functional Specialization within the EXO70 Gene Family in Arabidopsis

by Vedrana Marković, Ivan Kulich and Viktor Žárský

Int. J. Mol. Sci. 2021, 22(14), 7595; https://doi.org/10.3390/ijms22147595 - 15 Jul 2021

Cited by 10 | Viewed by 3460

Abstract

Localized delivery of plasma-membrane and cell-wall components is a crucial process for plant cell growth. One of the regulators of secretory-vesicle targeting is the exocyst tethering complex. The exocyst mediates first interaction between transport vesicles and the target membrane before their fusion is performed by SNARE proteins. In land plants, genes encoding the EXO70 exocyst subunit underwent an extreme proliferation with 23 paralogs present in the Arabidopsis (Arabidopsis thaliana) genome. These paralogs often acquired specialized functions during evolution. Here, we analyzed functional divergence of selected EXO70 paralogs in Arabidopsis. Performing a systematic cross-complementation analysis of exo70a1 and exo70b1 mutants, we found that EXO70A1 was functionally substituted only by its closest paralog, EXO70A2. In contrast, none of the EXO70 isoforms tested were able to substitute EXO70B1, including its closest relative, EXO70B2, pointing to a unique function of this isoform. The presented results document a high degree of functional specialization within the EXO70 gene family in land plants. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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13 pages, 8337 KiB

Open AccessArticle

Cell Cycle-Dependence of Autophagic Activity and Inhibition of Autophagosome Formation at M Phase in Tobacco BY-2 Cells

by Shigeru Hanamata, Takamitsu Kurusu and Kazuyuki Kuchitsu

Int. J. Mol. Sci. 2020, 21(23), 9166; https://doi.org/10.3390/ijms21239166 - 1 Dec 2020

Cited by 4 | Viewed by 3679

Abstract

Autophagy is ubiquitous in eukaryotic cells and plays an essential role in stress adaptation and development by recycling nutrients and maintaining cellular homeostasis. However, the dynamics and regulatory mechanisms of autophagosome formation during the cell cycle in plant cells remain poorly elucidated. We here analyzed the number of autophagosomes during cell cycle progression in synchronized tobacco BY-2 cells expressing YFP-NtATG8a as a marker for the autophagosomes. Autophagosomes were abundant in the G2 and G1 phases of interphase, though they were much less abundant in the M and S phases. Autophagosomes drastically decreased during the G2/M transition, and the CDK inhibitor roscovitine inhibited the G2/M transition and the decrease in autophagosomes. Autophagosomes were rapidly increased by a proteasome inhibitor, MG-132. MG-132-induced autophagosome formation was also markedly lower in the M phases than during interphase. These results indicate that the activity of autophagosome formation is differently regulated at each cell cycle stage, which is strongly suppressed during mitosis. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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20 pages, 101220 KiB

Open AccessArticle

Genome-Wide Identification of CsATGs in Tea Plant and the Involvement of CsATG8e in Nitrogen Utilization

by Wei Huang, Dan-Ni Ma, Hong-Ling Liu, Jie Luo, Pu Wang, Ming-Le Wang, Fei Guo, Yu Wang, Hua Zhao and De-Jiang Ni

Int. J. Mol. Sci. 2020, 21(19), 7043; https://doi.org/10.3390/ijms21197043 - 24 Sep 2020

Cited by 11 | Viewed by 2581

Abstract

Nitrogen (N) is a macroelement with an indispensable role in the growth and development of plants, and tea plant (Camellia sinensis) is an evergreen perennial woody species with young shoots for harvest. During senescence or upon N stress, autophagy has been shown to be induced in leaves, involving a variety of autophagy-related genes (ATGs), which have not been characterized in tea plant yet. In this study, a genome-wide survey in tea plant genome identified a total of 80 Camellia Sinensis autophagy-related genes, CsATGs. The expression of CsATG8s in the tea plant showed an obvious increase from S1 (stage 1) to S4 (stage 4), especially for CsATG8e. The expression levels of AtATGs (Arabidopsis thaliana) and genes involved in N transport and assimilation were greatly improved in CsATG8e-overexpressed Arabidopsis. Compared with wild type, the overexpression plants showed earlier bolting, an increase in amino N content, as well as a decrease in biomass and the levels of N, phosphorus and potassium. However, the N level was found significantly higher in APER (aerial part excluding rosette) in the overexpression plants relative to wild type. All these results demonstrated a convincing function of CsATG8e in N remobilization and plant development, indicating CsATG8e as a potential gene for modifying plant nutrient utilization. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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12 pages, 3346 KiB

Open AccessArticle

ATG4 Mediated Psm ES4326/AvrRpt2-Induced Autophagy Dependent on Salicylic Acid in Arabidopsis Thaliana

by Wenjun Gong, Bingcong Li, Baihong Zhang and Wenli Chen

Int. J. Mol. Sci. 2020, 21(14), 5147; https://doi.org/10.3390/ijms21145147 - 21 Jul 2020

Cited by 6 | Viewed by 3970

Abstract

Psm ES4326/AvrRpt2 (AvrRpt2) was widely used as the reaction system of hypersensitive response (HR) in Arabidopsis. The study showed that in npr1 (GFP-ATG8a), AvrRpt2 was more effective at inducing the production of autophagosome and autophagy flux than that in GFP-ATG8a. The mRNA expression of ATG1, ATG6 and ATG8a were more in npr1 during the early HR. Based on transcriptome data analysis, enhanced disease susceptibility 1 (EDS1) was up-regulated in wild-type (WT) but was not induced in atg4a4b (ATG4 deletion mutant) during AvrRpt2 infection. Compared with WT, atg4a4b had higher expression of salicylic acid glucosyltransferase 1 (SGT1) and isochorismate synthase 1 (ICS1); but less salicylic acid (SA) in normal condition and the same level of free SA during AvrRpt2 infection. These results suggested that the consumption of free SA should be occurred in atg4a4b. AvrRpt2 may trigger the activation of Toll/Interleukin-1 receptor (TIR)-nucleotide binding site (NB)-leucine rich repeat (LRR)—TIR-NB-LRR—to induce autophagy via EDS1, which was inhibited by nonexpressor of PR genes 1 (NPR1). Moreover, high expression of NPR3 in atg4a4b may accelerate the degradation of NPR1 during AvrRpt2 infection. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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Review

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11 pages, 626 KiB

Open AccessReview

Research Progress of ATGs Involved in Plant Immunity and NPR1 Metabolism

by Shuqin Huang, Baihong Zhang and Wenli Chen

Int. J. Mol. Sci. 2021, 22(22), 12093; https://doi.org/10.3390/ijms222212093 - 9 Nov 2021

Cited by 4 | Viewed by 3445

Abstract

Autophagy is an important pathway of degrading excess and abnormal proteins and organelles through their engulfment into autophagosomes that subsequently fuse with the vacuole. Autophagy-related genes (ATGs) are essential for the formation of autophagosomes. To date, about 35 ATGs have been identified in Arabidopsis, which are involved in the occurrence and regulation of autophagy. Among these, 17 proteins are related to resistance against plant pathogens. The transcription coactivator non-expressor of pathogenesis-related genes 1 (NPR1) is involved in innate immunity and acquired resistance in plants, which regulates most salicylic acid (SA)-responsive genes. This paper mainly summarizes the role of ATGs and NPR1 in plant immunity and the advancement of research on ATGs in NPR1 metabolism, providing a new idea for exploring the relationship between ATGs and NPR1. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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15 pages, 1564 KiB

Open AccessReview

Autophagy in Plant Abiotic Stress Management

by Hong Chen, Jiangli Dong and Tao Wang

Int. J. Mol. Sci. 2021, 22(8), 4075; https://doi.org/10.3390/ijms22084075 - 15 Apr 2021

Cited by 30 | Viewed by 4212

Abstract

Plants can be considered an open system. Throughout their life cycle, plants need to exchange material, energy and information with the outside world. To improve their survival and complete their life cycle, plants have developed sophisticated mechanisms to maintain cellular homeostasis during development and in response to environmental changes. Autophagy is an evolutionarily conserved self-degradative process that occurs ubiquitously in all eukaryotic cells and plays many physiological roles in maintaining cellular homeostasis. In recent years, an increasing number of studies have shown that autophagy can be induced not only by starvation but also as a cellular response to various abiotic stresses, including oxidative, salt, drought, cold and heat stresses. This review focuses mainly on the role of autophagy in plant abiotic stress management. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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23 pages, 3000 KiB

Open AccessReview

Jasmonic Acid Signaling and Molecular Crosstalk with Other Phytohormones

by Hai Liu and Michael P. Timko

Int. J. Mol. Sci. 2021, 22(6), 2914; https://doi.org/10.3390/ijms22062914 - 13 Mar 2021

Cited by 72 | Viewed by 7665

Abstract

Plants continually monitor their innate developmental status and external environment and make adjustments to balance growth, differentiation and stress responses using a complex and highly interconnected regulatory network composed of various signaling molecules and regulatory proteins. Phytohormones are an essential group of signaling molecules that work through a variety of different pathways conferring plasticity to adapt to the everchanging developmental and environmental cues. Of these, jasmonic acid (JA), a lipid-derived molecule, plays an essential function in controlling many different plant developmental and stress responses. In the past decades, significant progress has been made in our understanding of the molecular mechanisms that underlie JA metabolism, perception, signal transduction and its crosstalk with other phytohormone signaling pathways. In this review, we discuss the JA signaling pathways starting from its biosynthesis to JA-responsive gene expression, highlighting recent advances made in defining the key transcription factors and transcriptional regulatory proteins involved. We also discuss the nature and degree of crosstalk between JA and other phytohormone signaling pathways, highlighting recent breakthroughs that broaden our knowledge of the molecular bases underlying JA-regulated processes during plant development and biotic stress responses. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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14 pages, 1725 KiB

Open AccessReview

Nitric Oxide (NO) Scaffolds the Peroxisomal Protein–Protein Interaction Network in Higher Plants

by Francisco J. Corpas, Salvador González-Gordo and José M. Palma

Int. J. Mol. Sci. 2021, 22(5), 2444; https://doi.org/10.3390/ijms22052444 - 28 Feb 2021

Cited by 14 | Viewed by 3232

Abstract

The peroxisome is a single-membrane subcellular compartment present in almost all eukaryotic cells from simple protists and fungi to complex organisms such as higher plants and animals. Historically, the name of the peroxisome came from a subcellular structure that contained high levels of hydrogen peroxide (H₂O₂) and the antioxidant enzyme catalase, which indicated that this organelle had basically an oxidative metabolism. During the last 20 years, it has been shown that plant peroxisomes also contain nitric oxide (NO), a radical molecule than leads to a family of derived molecules designated as reactive nitrogen species (RNS). These reactive species can mediate post-translational modifications (PTMs) of proteins, such as S-nitrosation and tyrosine nitration, thus affecting their function. This review aims to provide a comprehensive overview of how NO could affect peroxisomal metabolism and its internal protein-protein interactions (PPIs). Remarkably, many of the identified NO-target proteins in plant peroxisomes are involved in the metabolism of reactive oxygen species (ROS), either in its generation or its scavenging. Therefore, it is proposed that NO is a molecule with signaling properties with the capacity to modulate the peroxisomal protein-protein network and consequently the peroxisomal functions, especially under adverse environmental conditions. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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21 pages, 3100 KiB

Open AccessReview

Plant Mitophagy in Comparison to Mammals: What Is Still Missing?

by Kaike Ren, Lanlan Feng, Shuangli Sun and Xiaohong Zhuang

Int. J. Mol. Sci. 2021, 22(3), 1236; https://doi.org/10.3390/ijms22031236 - 27 Jan 2021

Cited by 15 | Viewed by 3924

Abstract

Mitochondrial homeostasis refers to the balance of mitochondrial number and quality in a cell. It is maintained by mitochondrial biogenesis, mitochondrial fusion/fission, and the clearance of unwanted/damaged mitochondria. Mitophagy represents a selective form of autophagy by sequestration of the potentially harmful mitochondrial materials into a double-membrane autophagosome, thus preventing the release of death inducers, which can trigger programmed cell death (PCD). Recent advances have also unveiled a close interconnection between mitophagy and mitochondrial dynamics, as well as PCD in both mammalian and plant cells. In this review, we will summarize and discuss recent findings on the interplay between mitophagy and mitochondrial dynamics, with a focus on the molecular evidence for mitophagy crosstalk with mitochondrial dynamics and PCD. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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17 pages, 659 KiB

Open AccessReview

Cargo Recognition and Function of Selective Autophagy Receptors in Plants

by Shuwei Luo, Xifeng Li, Yan Zhang, Yunting Fu, Baofang Fan, Cheng Zhu and Zhixiang Chen

Int. J. Mol. Sci. 2021, 22(3), 1013; https://doi.org/10.3390/ijms22031013 - 20 Jan 2021

Cited by 19 | Viewed by 4283

Abstract

Autophagy is a major quality control system for degradation of unwanted or damaged cytoplasmic components to promote cellular homeostasis. Although non-selective bulk degradation of cytoplasm by autophagy plays a role during cellular response to nutrient deprivation, the broad roles of autophagy are primarily mediated by selective clearance of specifically targeted components. Selective autophagy relies on cargo receptors that recognize targeted components and recruit them to autophagosomes through interaction with lapidated autophagy-related protein 8 (ATG8) family proteins anchored in the membrane of the forming autophagosomes. In mammals and yeast, a large collection of selective autophagy receptors have been identified that mediate the selective autophagic degradation of organelles, aggregation-prone misfolded proteins and other unwanted or nonnative proteins. A substantial number of selective autophagy receptors have also been identified and functionally characterized in plants. Some of the autophagy receptors in plants are evolutionarily conserved with homologs in other types of organisms, while a majority of them are plant-specific or plant species-specific. Plant selective autophagy receptors mediate autophagic degradation of not only misfolded, nonactive and otherwise unwanted cellular components but also regulatory and signaling factors and play critical roles in plant responses to a broad spectrum of biotic and abiotic stresses. In this review, we summarize the research on selective autophagy in plants, with an emphasis on the cargo recognition and the biological functions of plant selective autophagy receptors. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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29 pages, 2213 KiB

Open AccessReview

Target of Rapamycin in Control of Autophagy: Puppet Master and Signal Integrator

by Yosia Mugume, Zakayo Kazibwe and Diane C. Bassham

Int. J. Mol. Sci. 2020, 21(21), 8259; https://doi.org/10.3390/ijms21218259 - 4 Nov 2020

Cited by 36 | Viewed by 4647

Abstract

The target of rapamycin (TOR) is an evolutionarily-conserved serine/threonine kinase that senses and integrates signals from the environment to coordinate developmental and metabolic processes. TOR senses nutrients, hormones, metabolites, and stress signals to promote cell and organ growth when conditions are favorable. However, TOR is inhibited when conditions are unfavorable, promoting catabolic processes such as autophagy. Autophagy is a macromolecular degradation pathway by which cells degrade and recycle cytoplasmic materials. TOR negatively regulates autophagy through phosphorylation of ATG13, preventing activation of the autophagy-initiating ATG1-ATG13 kinase complex. Here we review TOR complex composition and function in photosynthetic and non-photosynthetic organisms. We also review recent developments in the identification of upstream TOR activators and downstream effectors of TOR. Finally, we discuss recent developments in our understanding of the regulation of autophagy by TOR in photosynthetic organisms. Full article

(This article belongs to the Special Issue New Insight into Signaling and Autophagy in Plants)

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