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In Nitrogen Assimilation (Plant Mutant/Biochemical Genetics/Ammonia Assimilation/Gene Expression) ROSANA MELO-OLIVEIRA, IGOR CUNHA OLIVEIRA, and GLORIA M

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In Nitrogen Assimilation (Plant Mutant/Biochemical Genetics/Ammonia Assimilation/Gene Expression) ROSANA MELO-OLIVEIRA, IGOR CUNHA OLIVEIRA, and GLORIA M Proc. Natl. Acad. Sci. USA Vol. 93, pp. 4718-4723, May 1996 Plant Biology Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation (plant mutant/biochemical genetics/ammonia assimilation/gene expression) ROSANA MELO-OLIVEIRA, IGOR CUNHA OLIVEIRA, AND GLORIA M. CORUZZI Department of Biology, New York University, New York, NY 10003 Communicated by William L. Ogren, Champaign, IL, December 18, 1995 (received for review June 2, 1995) ABSTRACT Glutamate dehydrogenase (GDH) is ubiqui- similating photorespiratory ammonia (6). However, several tous to all organisms, yet its role in higher plants remains pieces of data argue against this proposed role. Inhibitors of enigmatic. To better understand the role of GDH in plant GS, such as phosphinothricin, specifically kill plants grown nitrogen metabolism, we have characterized an Arabidopsis under photorespiratory growth conditions (4, 10, 11). Second, mutant (gdhl-1) defective in one of two GDH gene products the characterization of photorespiratory mutants has sup- and have studied GDHI gene expression. GDHI mRNA accu- ported a major role for GS/GOGAT in this process. Plant mulates to highest levels in dark-adapted or sucrose-starved mutants deficient in chloroplast GS2 or ferredoxin-dependent plants, and light or sucrose treatment each repress GDHI GOGAT are chlorotic when grown under photorespiratory mRNA accumulation. These results suggest that the GDHI conditions (in air), yet they display a normal phenotype when gene product functions in the direction of glutamate catabo- grown under conditions that suppress photorespiration (high lism under carbon-limiting conditions. Low levels of GDHI CO2) (12-15). Together these data suggest that GDH plays a mRNA present in leaves of light-grown plants can be induced minor role, if any, in the reassimilation of photorespiratory by exogenously supplied ammonia. Under such conditions of ammonia. An alternate role has been proposed in which GDH carbon and ammonia excess, GDH1 may function in the functions in ammonia detoxification, because its activity is direction of glutamate biosynthesis. The Arabidopsis gdh- increased in plants exposed to high levels of ammonia (16). deficient mutant allele gdhl-l cosegregates with the GDHI Finally, a catabolic function for GDH has been proposed to be gene and behaves as a recessive mutation. The gdhl-l mutant important for remobilization of ammonia from glutamate displays a conditional phenotype in that seedling growth is during germination, senescence, and seed set (6, 7). specifically retarded on media containing exogenously sup- Despite decades of biochemical studies on plant GDH, the plied inorganic nitrogen. These results suggest that GDH1 in vivo role of this enzyme in plant nitrogen metabolism plays a nonredundant role in ammonia assimilation under remains equivocal. Because the mechanisms controlling the conditions of inorganic nitrogen excess. This notion is further intra- and intercellular transport of inorganic nitrogen and supported by the fact that the levels of mRNA for GDH1 and organic nitrogen are presently unknown, the in vivo function of chloroplastic glutamine synthetase (GS2) are reciprocally GDH can best be judged by characterizing the phenotype of regulated by light. plant mutants defective in GDH. A plant mutant deficient in GDH has been previously isolated from maize (17, 18). Glutamate dehydrogenase (GDH; EC 1.4.1.2) serves as a link However, this maize GDH-deficient mutant cannot be used to between carbon and nitrogen metabolism, as it is capable of assess the in vivo role of GDH in photorespiration, because C4 assimilating ammonia into glutamate or deaminating gluta- plants display low or negligible photorespiratory rates. Here, mate into 2-oxoglutarate and ammonia. The relative impor- we report the characterization of a plant GDH gene, analyze tance of GDH versus nitrogen assimilatory enzymes such as its regulation by light and/or metabolites, and characterize an glutamine synthetase (GS) has been deduced in microorgan- Arabidopsis mutant (gdhl-l) deficient in one of two GDH gene isms using mutants defective in either enzyme (1, 2). In plants, products. This molecular-genetic dissection in Arabidopsis the importance of GDH in nitrogen assimilation has been indicates that GDH plays a nonredundant role in plant nitro- under question since the discovery of the GS/GOGAT [glu- gen metabolism in a C3 plant. tamate synthase (glutamate 2-oxoglutarate aminotransferase)] cycle (3). Current opinion is divided as to whether GDH plays (i) MATERIALS AND METHODS a role in ammonia assimilation, particularly under high ammonia concentrations; (ii) a role in glutamate catabolism; or (iii) a Plant Lines and Growth Conditions. The Columbia ecotype redundant and dispensable role in nitrogen assimilation (4-7). of Arabidopsis was used in all experiments, unless otherwise The proposed roles for GDH in plants have been based noted. The Landsberg ecotype was used to determine a largely on in vitro studies that have uncovered two types of restriction fragment length polymorphism for GDH1. Recom- GDH enzymes, an NADPH-requiring GDH enzyme that is binant inbred lines were obtained from the Ohio State Uni- localized to and an GDH found versity,Arabidopsis Stock Center (19). Plants were grown at 45 chloroplasts NADH-requiring mE-m-2sec-1 (E = einstein, 1 mol of photons) on a 16-h in the mitochondria (6, 8). The GDH enzymes from a variety light/8-h dark cycle unless otherwise indicated. "Light-grown" of higher plants exhibit high Km values for ammonia (> 1 mM), and "dark-adapted" plants were grown initially under the which argues against a major role of GDH in primary nitrogen normal day/night light regime and were subsequently trans- assimilation in vivo (9). Because high levels ofphotorespiratory ferred to continuous h ammonia are released in mitochondria, it has been proposed light or dark, respectively, for 48 before that mitochondrial NADH-GDH plays a major role in reas- Abbreviations: GDH, glutamate dehydrogenase; GS, glutamine syn- thetase; GOGAT, glutamate synthase (glutamate 2-oxoglutarate ami- The publication costs of this article were defrayed in part by page charge notransferase); MS, Murashige and Skoog. payment. This article must therefore be hereby marked "advertisement" in Data deposition: The sequence reported in this paper has been accordance with 18 U.S.C. §1734 solely to indicate this fact. deposited in the GenBank data base (accession no. U53527). 4718 Downloaded by guest on September 29, 2021 Plant Biology: Melo-Oliveira et al. Proc. Natl. Acad. Sci. USA 93 (1996) 4719 harvest for RNA isolation. For RNA isolation, plants were grown A. thaliana PRVRSVLIKA PVKVQSTQRE - T KKEEEEVE- EEE 32 H. salinarium -HHAM SKSDSTHDE- S --GDEAAD -- STE 23 on Murashige and Skoog (MS) salts (GIBCO/BRL, catalog no. Human MYRYLGEALL LSRAGPAAL- G SASADSAALL G64ARGQPAAA 40 C. sorokiniana CRPPSSPSLS WPPGLRSPAL PRAVACARGR SAKRDVAAKR LRSRSPRMDA 50 11117) under "semihydroponic" conditions, unless otherwise E. coli --- -- QM 3 noted. For semihydroponics, seeds were sown on nylon nets S. cerevisiae (Tetko, Elmsford, NY, catalog no. 3-250/50) suspended on A. thaliana AMNPRI NFKL------ ---------- ------AARL LG-----LD- 54 MS media containing 3% sucrose and 0.4% agar and grown for H. salinarium PES S QLY-T - AASY LD- -ID- 45 Human PQP RHYSEAVADR EDDPNFFKM------- VEGF FDRGASIVE- 82 16-18 days. Thereafter, the nylon net was lifted, and the plants C. sorokiniana TITGDFTALQK AVKQMATKAG TEGLVHGIKSN PELRQLLTEI FMKDPEQQEF 100 were transferred to fresh MS medium containing the indicated E. coli T---YS - LESFLNHV QKRDPNQTEF 24 supplementations. Ethyl methanesulfonate- and methylnitro- S. cerevisiae MSEP EF----QQAY 10 sourea-mutagenized Arabidopsis seeds (Columbia ecotype) A. thaliana SKLEK-&I-P --- ------- FREEIKVE C LEQ 81 H. salinarium QNIVE YP ---------- ---------- ---KKVHEVT I EI EFDc41_ 72 were obtained from R. Last (Cornell University). For mutant Human DKLVEI L TR ES---EEQKR IRVRGILRII KPCNHVLSLS RPF W 129 C. sorokiniana MQAVREVAVS LQPVFEKRPE L--LPIFKQI VEPERVITFR VSWL A L 148 screening, M2 mutagenized seeds were plated on MS media E. coli AQAVREVMTT LWPFLEQNPK YRQMSLLERL VEPERVIQFR VVIVE QI 74 supplemented with 0.05% aspartate. The ammonia-free, ni- S. cerevisiae EEVVSSLEDS --TLFEQHPE Y--RKVLPIV SVPERIIQFR VTHIENKGEQ 56 trate-containing MS medium (Sigma, catalog no. M2909; used A. thaliana ASF D alE IIPPEEiv-fl iAii 131 in Fig. 5) and the ammonia-free/nitrate-free MS media (Sigma H. salinarium C _ RY r .-vt t 122 Human EVFI R;DSQ .KG T5P 179 catalog no. M0529; used in Fig. 7) were supplemented with the C. sorokiniana QVNRG SSAI GG P LS IHE FEQI ESLTTLPM 198 E. coli QHR SSAI GG HP VS ILK 3FEQT ALTTLPM 124 appropriate MS salts and vitamins, unless otherwise noted. S. cerevisiae EVAQG NSAK KGG HP S ILK PFEQI SLTGLDM 106 RNA and DNA Manipulations. RNA extraction (20), DNA extraction (21), and Northern and Southern blot analyses (22) A. thaliana G GCD RKLSI R P KI --HDL HT APD 179 H.salinarium PGA UAVH |PELSP R ES --RDV*NQ APD 170 were performed as described. The 16S ribosomal RNA cDNA Human G IN YTD K EL AKKGF G AP 229 C. sorokiniana SDFD PKGKSD RFCQSFMTEL --QRHISYVQ DSGVG 246 probe (rRNA, provided by B. Scheres, University of Utrecht, E. coli 3DFD PKGKSE RFCQALMTEL --YRHLGADT DIGVG 172 Utrecht, the Netherlands), a PCR-generated a-tubulin exon 4 S. cerevisiae 5 CVD LKGRS R RICYAFMREL --SRHIGQDT DIGVG 154 probe, spanning nucleotides 1209-1596 (a gift from C. Silflow, A. thaliana PO ;FLR KFEME Y--- S;A : IDL ;LG FG 225 University of Minnesota), and a full-length cDNA for the H. salinarium P _-- -SPATGK PVDG PR Gp 217 Human ER ST DI ISCG RS r HG 279 chloroplastic form of GS2 (GLN2; ref. 23) were labeled by the C. sorokiniana AREIGYLFGQ YKRITKNY-- --TGV34SG4 QE4SG EI? c GAVLF 292 E. coli GREVGFMAGH MKKLSNNT-- --ACVF G43LSPI3GELI EPmGLVYF 218 random primed method. Probe labeling, prehybridization, S. cerevisiae GREIGYLFGA YRSYKNSW-- --EG LNG LIP GLLYY 200 hybridization, and detection were as indicated in the Genius User's Guide A.
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