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      Autophagy in Plant: A New Orchestrator in the Regulation of the Phytohormones Homeostasis

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          Abstract

          Autophagy is a highly evolutionarily-conserved catabolic process facilitating the development and survival of organisms which have undergone favorable and/or stressful conditions, in particular the plant. Accumulating evidence has implicated that autophagy is involved in growth and development, as well as responses to various stresses in plant. Similarly, phytohormones also play a pivotal role in the response to various stresses in addition to the plant growth and development. However, the relationship between autophagy and phytohormones still remains poorly understood. Here, we review advances in the crosstalk between them upon various environmental stimuli. We also discuss how autophagy coordinates the phytohormones to regulate plant growth and development. We propose that unraveling the regulatory role(s) of autophagy in modulating the homeostasis of phytohormones would benefit crop breeding and improvement under variable environments, in particular under suboptimal conditions.

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          Most cited references72

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          Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis.

          Autophagy is an evolutionarily conserved intracellular process for vacuolar degradation of cytoplasmic components. In higher plants, autophagy defects result in early senescence and excessive immunity-related programmed cell death (PCD) irrespective of nutrient conditions; however, the mechanisms by which cells die in the absence of autophagy have been unclear. Here, we demonstrate a conserved requirement for salicylic acid (SA) signaling for these phenomena in autophagy-defective mutants (atg mutants). The atg mutant phenotypes of accelerated PCD in senescence and immunity are SA signaling dependent but do not require intact jasmonic acid or ethylene signaling pathways. Application of an SA agonist induces the senescence/cell death phenotype in SA-deficient atg mutants but not in atg npr1 plants, suggesting that the cell death phenotypes in the atg mutants are dependent on the SA signal transducer NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1. We also show that autophagy is induced by the SA agonist. These findings imply that plant autophagy operates a novel negative feedback loop modulating SA signaling to negatively regulate senescence and immunity-related PCD.
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            Autophagy: The Master of Bulk and Selective Recycling.

            Plants have evolved sophisticated mechanisms to recycle intracellular constituents, which are essential for developmental and metabolic transitions; for efficient nutrient reuse; and for the proper disposal of proteins, protein complexes, and even entire organelles that become obsolete or dysfunctional. One major route is autophagy, which employs specialized vesicles to encapsulate and deliver cytoplasmic material to the vacuole for breakdown. In the past decade, the mechanics of autophagy and the scores of components involved in autophagic vesicle assembly have been documented. Now emerging is the importance of dedicated receptors that help recruit appropriate cargo, which in many cases exploit ubiquitylation as a signal. Although operating at a low constitutive level in all plant cells, autophagy is upregulated during senescence and various environmental challenges and is essential for proper nutrient allocation. Its importance to plant metabolism and energy balance in particular places autophagy at the nexus of robust crop performance, especially under suboptimal conditions.
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              Reciprocal Regulation of the TOR Kinase and ABA Receptor Balances Plant Growth and Stress Response

              As sessile organisms, plants must adapt to variations in the environment. Environmental stress triggers various responses, including growth inhibition, mediated by the plant hormone abscisic acid (ABA). The mechanisms that integrate stress responses with growth are poorly understood. Here, we discovered that the Target of Rapamycin (TOR) kinase phosphorylates PYL ABA receptors at a conserved serine residue to prevent activation of the stress response in unstressed plants. This phosphorylation disrupts PYL association with ABA and with PP2C phosphatase effectors, leading to inactivation of SnRK2 kinases. Under stress, ABA-activated SnRK2s phosphorylate Raptor, a component of the TOR complex, triggering TOR complex dissociation and inhibition. Thus, TOR signaling represses ABA signaling and stress responses in unstressed conditions, whereas ABA signaling represses TOR signaling and growth during times of stress. Plants utilize this conserved phospho-regulatory feedback mechanism to optimize the balance of growth and stress responses.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                14 June 2019
                June 2019
                : 20
                : 12
                : 2900
                Affiliations
                [1 ]State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou 510642, China; gwtscau@ 123456163.com (W.G.); 18826231837@ 123456163.com (X.L.); syguo6688@ 123456163.com (S.G.)
                [2 ]State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Life Sciences and Technology, Guangxi University, Nanning 530004, China; yunfengliu_bio@ 123456126.com
                [3 ]College of Life Sciences, South China Agricultural University, Guangzhou 510642, China; fqli@ 123456scau.edu.cn
                Author notes
                [* ]Correspondence: qjxie@ 123456scau.edu.cn ; Tel.: +86-20-87574953
                Author information
                https://orcid.org/0000-0002-4166-9056
                https://orcid.org/0000-0002-6372-3260
                Article
                ijms-20-02900
                10.3390/ijms20122900
                6627538
                31197094
                3f9a78df-f21c-43d8-a7ce-4ec3c017f860
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 09 May 2019
                : 13 June 2019
                Categories
                Review

                Molecular biology
                autophagy,phytohormones,crosstalk,stress response,plant growth and development
                Molecular biology
                autophagy, phytohormones, crosstalk, stress response, plant growth and development

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