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An Essential Metabolite for Plant Growth and Stress Acclimation

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An Essential Metabolite for Plant Growth and Stress Acclimation molecules Review L-Aspartate: An Essential Metabolite for Plant Growth and Stress Acclimation Mei Han 1, Can Zhang 1, Peter Suglo 1, Shuyue Sun 1, Mingyao Wang 1 and Tao Su 1,2,* 1 Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China; [email protected] (M.H.); [email protected] (C.Z.); [email protected] (P.S.); [email protected] (S.S.); [email protected] (M.W.) 2 Key Laboratory of State Forestry Administration on Subtropical Forest Biodiversity Conservation, Nanjing Forestry University, Nanjing 210037, China * Correspondence: [email protected] Abstract: L-aspartate (Asp) serves as a central building block, in addition to being a constituent of proteins, for many metabolic processes in most organisms, such as biosynthesis of other amino acids, nucleotides, nicotinamide adenine dinucleotide (NAD), the tricarboxylic acid (TCA) cycle and glycolysis pathway intermediates, and hormones, which are vital for growth and defense. In animals and humans, lines of data have proved that Asp is indispensable for cell proliferation. However, in plants, despite the extensive study of the Asp family amino acid pathway, little attention has been paid to the function of Asp through the other numerous pathways. This review aims to elucidate the most important aspects of Asp in plants, from biosynthesis to catabolism and the role of Asp and its metabolic derivatives in response to changing environmental conditions. It considers the distribution of Asp in various cell compartments and the change of Asp level, and its significance in the whole plant under various stresses. Moreover, it provides evidence of the interconnection between Asp and phytohormones, which have prominent functions in plant growth, development, and defense. Citation: Han, M.; Zhang, C.; Suglo, P.; Sun, S.; Wang, M.; Su, T. The updated information will help improve our understanding of the physiological role of Asp and L-Aspartate: An Essential Metabolite Asp-borne metabolic fluxes, supporting the modular operation of these networks. for Plant Growth and Stress Acclimation. Molecules 2021, 26, 1887. Keywords: aspartate; stress; aspartate aminotransferase; aspartate transporter/carrier; compartmen- https://doi.org/10.3390/ tation; hormone molecules26071887 Academic Editor: William D. Lubell 1. Introduction Received: 31 January 2021 L-aspartate (Asp), in addition to constituting proteins and being an active residue in Accepted: 23 March 2021 many enzymes, is a precursor leading to the biosynthesis of multiple biomolecules required Published: 26 March 2021 for plant growth and defense, such as nucleotides, nicotinamide adenine dinucleotide (NAD), organic acids, amino acids, and their derived metabolites. Though it cannot be Publisher’s Note: MDPI stays neutral simply quantified, given that in Escherichia coli, approximately 27% of nitrogen flows with regard to jurisdictional claims in through Asp (https://MetaCyc.org, accessed on 30 January 2021) [1], the contribution of published maps and institutional affil- Asp to plants is highly conspicuous. It has been well documented that methionine (Met), iations. threonine (Thr), lysine (Lys), and isoleucine (Ile), of the eight essential amino acids, are derived from Asp, through a pathway commonly known as the Asp family amino acids [2]. Further metamorphosis of Asp can yield glutamate (Glu) to glutamine (Gln) through the action of glutamine synthetase (GS). Asp and Glu, along with asparagine (Asn) and Gln, Copyright: © 2021 by the authors. are the common nitrogen carriers [3], which have been noted for their primary role in the Licensee MDPI, Basel, Switzerland. recycling, storage, and transport of nitrogen in germinating seeds, vegetative organs, and This article is an open access article senescence organs [4]. Asp is also involved in the biosynthesis of some other amino acids distributed under the terms and such as arginine (Arg) and the aromatic amino acids (tyrosine (Tyr) and phenylalanine conditions of the Creative Commons (Phe)), through the aspartate–argininosuccinate synthase and the aspartate–prephenate Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ aminotransferase pathways, respectively [5]. Moreover, Asp is the building block for de 0 4.0/). novo pyrimidine manufacturing and is required to convert ionosine-5 -monophosphate to Molecules 2021, 26, 1887. https://doi.org/10.3390/molecules26071887 https://www.mdpi.com/journal/molecules MoleculesMolecules 2021, 26, x2021 FOR, 26PEER, 1887 REVIEW 2 of 17 2 of 17 aminotransferase pathway0 s, respectively [5]. Moreover, Asp is the building block for de novo pyrimidineadenine-5 manufacturing-monophosphate and is required in purine to biosynthesisconvert ionosine [6].-5 In′-monophosphate addition, Asp serves as a critical to adenineprecursor-5′-monophosphate of the aspartate in purine oxidase biosynthesis pathway [6]. in In the addition synthesis, Asp of serve nicotinamides as a adenine dinu- critical precursorcleotide of (NAD), the aspartate an essential oxidase componentpathway in the of synthesis plant abiotic of nicotinamide process, senescence, ade- chlorophyll nine dinucleotideformation, (NAD), and pollenan essential development component [7 –of9 ].plant In addition, abiotic process, Asp deamination senescence, to oxaloacetate by chlorophyllaspartate formation, aminotransferase and pollen development (AspAT) [ in7–9] the. In cytosol addition, is essentialAsp deami fornation the production to of malate oxaloacetateneeded by aspartate in mitochondria aminotransferase for the (AspAT) tricarboxylic in the acid cytosol (TCA) is essential cycle [10 for], whereas the Asp released productionfrom of malate the mitochondrion needed in mitochondria is involved for the in thetricarboxylic biosynthesis acid (TCA) of nucleotides cycle [10], in the cytosol. In- whereas Asptriguingly, released somefrom the recent mitochondrion studies have is involved found that in the cytosolic biosynthesis Asp isof an nucleo- endogenous metabolic tides in thelimiter cytosol. of Intriguingly, cell proliferation some recent [6,11– studies15], moreover, have found Asp that derived cytosolic from Asp glucose is an is indispensable endogenousto metabolic drive biomass limiter synthesis of cell proliferati duringon cellular [6,11–15] hypertrophy, moreover, Asp [16 ].derived Altogether, from apparently, Asp glucose is indispensable to drive biomass synthesis during cellular hypertrophy [16]. represents a critical metabolite hub interconnecting with diverse metabolic pathways that Altogether, apparently, Asp represents a critical metabolite hub interconnecting with diverse metabolicare of significant pathways that importance are of significant for plant importance nutrition, for energy, plant nutrition, and stress energy, responses. and stress respoExchangenses. and competition for Asp and derived intermediates profoundly affect plant Exchangemetabolism, and competition which requiresfor Asp and great derived attention. intermediates The detailed profoundly study affect and research into an- plant metabolism,abolism which and catabolism requires great of Asp attention. and its The related detailed pathways study and (i.e., research the Asp into family amino acids, anabolismnucleotides, and catabolism NAD, of Asp TCA, and andits related glycolysis) pathways are thus(i.e., the necessary Asp family to increase amino our knowledge acids, nucleotides,on cell growth NAD, andTCA, repair and glycolysis) [17], so as are to furtherthus necessary our understanding to increase our of plant growth, de- knowledgevelopment on cell growth and and defense repair [13 [17,15], ,so18 ].as Herein,to further the our various understandin pathwaysg of plant derived from Asp are growth, developmentsummarized and in defense this review [13,15,18] (Figure. Herein,1), andthe various a general pathways overview derived of from Asp metabolism and Asp are summarizedregulation in is this described. review (Fig Inure addition, 1), and thea general dynamism overview of Aspof Asp and metabolism AspAT in plants and their and regulationrole inis thedescribed. plant inIn responseaddition, the to variousdynamism stress of Asp conditions and AspAT are discussed.in plants and Furthermore, some their role in the plant in response to various stress conditions are discussed. Furthermore, recent progress in the interconnection between Asp and phytohormones, such as ethylene some recent progress in the interconnection between Asp and phytohormones, such as and auxin, is highlighted. ethylene and auxin, is highlighted. Figure 1. The central metabolic intermediates derived from L-aspartate (Asp) in plants (adapted Figure 1. The central metabolic intermediates derived from L-aspartate (Asp) in plants (adapted from [5]). AK, aspartate from [5]). AK, aspartate kinase; AO, aspartate oxidase; ASS, argininosuccinate synthase; AS, as- kinase; AO, aspartate oxidase; ASS, argininosuccinate synthase; AS, asparagine synthase; PAT, prephenate aminotransferase; AspAT, aspartate aminotransferase; GS, glutamine synthetase; GOGAT, glutamine oxoglutarate aminotransferase; TCA, tricarboxylic acid cycle; NAD, nicotinamide adenine dinucleotide; PK, pyruvate kinase; PYC, pyruvate carboxylase; PEPC, phosphoenolpyruvate carbosylase; ATC/PYRB/I, aspartate transcarbamoylase or aspartate carbamoyl transferase; PYRC, dihydro-orotase; PYDA, dihydro-orotate dehydrogenase; PYRE, phosphoribosyl transferase; PYRF, orotate decarboxylase. GH3, group II of GRETCHEN
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