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      ATP homeostasis and signaling in plants

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          Abstract

          ATP is the primary form of energy for plants, and a shortage of cellular ATP is generally acknowledged to pose a threat to plant growth and development, stress resistance, and crop quality. The overall metabolic processes that contribute to the ATP pool, from production, dissipation, and transport to elimination, have been studied extensively. Considerable evidence has revealed that in addition to its role in energy supply, ATP also acts as a regulatory signaling molecule to activate global metabolic responses. Identification of the eATP receptor DORN1 contributed to a better understanding of how plants cope with disruption of ATP homeostasis and of the key points at which ATP signaling pathways intersect in cells or whole organisms. The functions of SnRK1α, the master regulator of the energy management network, in restoring the equilibrium of the ATP pool have been demonstrated, and the vast and complex metabolic network mediated by SnRK1α to adapt to fluctuating environments has been characterized. This paper reviews recent advances in understanding the regulatory control of the cellular ATP pool and discusses possible interactions among key regulators of ATP-pool homeostasis and crosstalk between iATP/eATP signaling pathways. Perception of ATP deficit and modulation of cellular ATP homeostasis mediated by SnRK1α in plants are discussed at the physiological and molecular levels. Finally, we suggest future research directions for modulation of plant cellular ATP homeostasis.

          Abstract

          Disturbance of the ATP reservoir poses a threat to plant development, stress resistance, and crop quality. ATP deficit is sensed by the master energy sensor SnRK1α, which mediates a complex metabolic network to adapt to fluctuating environments. The crosstalk between iATP/eATP signals implies that SnRK1α and the eATP receptor DORN1 may converge to induce physiological and molecular adaptive responses in plants.

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          AMPK: guardian of metabolism and mitochondrial homeostasis.

          Cells constantly adapt their metabolism to meet their energy needs and respond to nutrient availability. Eukaryotes have evolved a very sophisticated system to sense low cellular ATP levels via the serine/threonine kinase AMP-activated protein kinase (AMPK) complex. Under conditions of low energy, AMPK phosphorylates specific enzymes and growth control nodes to increase ATP generation and decrease ATP consumption. In the past decade, the discovery of numerous new AMPK substrates has led to a more complete understanding of the minimal number of steps required to reprogramme cellular metabolism from anabolism to catabolism. This energy switch controls cell growth and several other cellular processes, including lipid and glucose metabolism and autophagy. Recent studies have revealed that one ancestral function of AMPK is to promote mitochondrial health, and multiple newly discovered targets of AMPK are involved in various aspects of mitochondrial homeostasis, including mitophagy. This Review discusses how AMPK functions as a central mediator of the cellular response to energetic stress and mitochondrial insults and coordinates multiple features of autophagy and mitochondrial biology.
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            AMPK phosphorylation of raptor mediates a metabolic checkpoint.

            AMPK is a highly conserved sensor of cellular energy status that is activated under conditions of low intracellular ATP. AMPK responds to energy stress by suppressing cell growth and biosynthetic processes, in part through its inhibition of the rapamycin-sensitive mTOR (mTORC1) pathway. AMPK phosphorylation of the TSC2 tumor suppressor contributes to suppression of mTORC1; however, TSC2-deficient cells remain responsive to energy stress. Using a proteomic and bioinformatics approach, we sought to identify additional substrates of AMPK that mediate its effects on growth control. We report here that AMPK directly phosphorylates the mTOR binding partner raptor on two well-conserved serine residues, and this phosphorylation induces 14-3-3 binding to raptor. The phosphorylation of raptor by AMPK is required for the inhibition of mTORC1 and cell-cycle arrest induced by energy stress. These findings uncover a conserved effector of AMPK that mediates its role as a metabolic checkpoint coordinating cell growth with energy status.
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              PLANT MITOCHONDRIA AND OXIDATIVE STRESS: Electron Transport, NADPH Turnover, and Metabolism of Reactive Oxygen Species.

              The production of reactive oxygen species (ROS), such as O2- and H2O2, is an unavoidable consequence of aerobic metabolism. In plant cells the mitochondrial electron transport chain (ETC) is a major site of ROS production. In addition to complexes I-IV, the plant mitochondrial ETC contains a non-proton-pumping alternative oxidase as well as two rotenone-insensitive, non-proton-pumping NAD(P)H dehydrogenases on each side of the inner membrane: NDex on the outer surface and NDin on the inner surface. Because of their dependence on Ca2+, the two NDex may be active only when the plant cell is stressed. Complex I is the main enzyme oxidizing NADH under normal conditions and is also a major site of ROS production, together with complex III. The alternative oxidase and possibly NDin(NADH) function to limit mitochondrial ROS production by keeping the ETC relatively oxidized. Several enzymes are found in the matrix that, together with small antioxidants such as glutathione, help remove ROS. The antioxidants are kept in a reduced state by matrix NADPH produced by NADP-isocitrate dehydrogenase and non-proton-pumping transhydrogenase activities. When these defenses are overwhelmed, as occurs during both biotic and abiotic stress, the mitochondria are damaged by oxidative stress.
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                Author and article information

                Contributors
                Journal
                Plant Commun
                Plant Commun
                Plant Communications
                Elsevier
                2590-3462
                07 February 2024
                08 April 2024
                07 February 2024
                : 5
                : 4
                : 100834
                Affiliations
                [1 ]Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China
                [2 ]University of Chinese Academy of Sciences, Beijing 100049, China
                [3 ]Guangdong AIB Polytechnic, Guangzhou 510507, China
                [4 ]School of Life Sciences and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China
                Author notes
                []Corresponding author zhuhong@ 123456scbg.ac.cn
                [∗∗ ]Corresponding author q-hxia@ 123456scbg.ac.cn
                Article
                S2590-3462(24)00054-3 100834
                10.1016/j.xplc.2024.100834
                11009363
                38327057
                138b9db9-1cae-434f-bded-da0963b7ed35
                © 2024 The Author(s)

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 16 October 2023
                : 14 January 2024
                : 3 February 2024
                Categories
                Review Article

                atp,dorn1,snrk1α,atp homeostasis and signaling
                atp, dorn1, snrk1α, atp homeostasis and signaling

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