Three cDNA sequences coding for glutamine synthetase polypeptides in Oryza sativa L.

Sakamoto, Atsushi; Ogawa, Masahiro; Masumura, Takehiro; Shibata, Daisuke; Takeba, Go; Tanaka, Kunisuke; Fujii, Shoji

doi:10.1007/bf00027323

Cited by 67 publications

(52 citation statements)

References 10 publications

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“…2), though each of the two genes is located in the nuclear genome (22)(23)(24)(25). The common ancestor of the two genes diverged 300 million years ago by our estimate, which is earlier than the divergence of the monocot and the dicot as shown in Fig.…”

Section: Discussionmentioning

confidence: 66%

Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes.

Kumada

Benson

Hillemann

et al. 1993

Proc. Natl. Acad. Sci. U.S.A.

220

195

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We performed molecular phylogenetic analyses of glutamine synthetase (GS) genes in order to investigate their evolutionary history. The analyses were done on 30 DNA sequences of the GS gene which included both prokaryotes and eukaryotes. Two types of GS genes are known at present: the GSI gene found so far only in prokaryotes and the GSII gene found in both prokaryotes and eukaryotes. Our study has shown that the two types of GS gene were produced by a gene duplication which preceded, perhaps by >1000 million years, the divergence of eukaryotes and prokaryotes. The results are consistent with the facts that (t0 GS is a key enzyme of nitrogen metabolism found in all extant life forms and (fi) the oldest biological fossils date back 3800 million years. Thus, we suggest that GS genes are one of the oldest existing and functioning genes in the history of gene evolution and that GSI genes should also exist in eukaryotes. Furthermore, our study may stimulate investigation on the evolution of "preprokaryotes," by which we mean the organisms that existed during the era between the origin of life and the divergence of prokaryotes and eukaryotes.Glutamine synthetase (GS) is a key enzyme in nitrogen metabolism; it has dual functions in two essential biochemical reactions, ammonia assimilation and glutamine biosynthesis (1, 2). It is also one of the few amide synthetases found in organisms. Prokaryotes and eukaryotes were once thought to synthesize different GSs: GSI for the former and GSII for the latter. It is now known, however, that GSII is also present in bacteria belonging to Rhizobiaceae (3-6), Frankiaceae (7), and Streptomycetaceae (8, 9). GSI, by contrast, has not been found in any eukaryote.Glutamine produced by GS is essential for protein synthesis, and its amide nitrogen is donated to synthesize many essential metabolites. It is thus natural to consider GS as present in, and probably indispensable to, all organisms. In view of the central roles played by GS, it is reasonable to believe that the GS gene is extremely old. From the sequence alignment of GSI from Salmonella typhimurium and GSII from alfalfa (10), we could observe that the differences in amino acids between them was 0.75 per site. This value is quite large compared with those for other proteins, suggesting also that the GSI and GSII genes share a very old comnmon ancestor.The aforementioned discovery of the GSII gene in plant symbiotic bacteria led to the suggestion that the gene had originated from host plants through lateral gene transfer (3). This was later questioned by the further findings of the GSII gene in plant nonsymbiotic actinomycetes (8, 9). Shatters and Kahn (6) have suggested that the common ancestor of the GSII genes in Rhizobiaceae and in the host plant must be older than the plant itself, and have argued against the gene transfer.In this paper we have traced the evolutionary history of the GS genes, using our own nucleotide sequence data and others' data from prokaryotic and eukaryotic species in order to estimate the age of...

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Section: Discussionmentioning

confidence: 66%

Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes.

Kumada

Benson

Hillemann

et al. 1993

Proc. Natl. Acad. Sci. U.S.A.

220

195

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“…A. glutinosa, cyt (nodule), Y08681, Guan et al, 1996;Arabidopsis cp, S69727, Peterman and Goodman, 1991; Arabidopsis 1 cyt (genomic sequence derived mRNA) NM 105291; Arabidopsis 2 cyt (genomic sequence derived mRNA) BT000753; Arabidopsis 3 cyt (genomic sequence derived mRNA) BT006245; Arabidopsis 4 cyt (genomic sequence derived mRNA) AY128749; Brassica napus-1, cyt (root), X76736, Schock et al, 1994; B. napus-2, cyt (root), Y12459, Ochs et al, 1999;B. napus-3, cyt (root) Temple et al, 1995;Nicotiana plumbaginifolia, cp, M19055, Tingey and Coruzzi, 1987;Nicotiana sylvestris, cp, X66940, Becker et al, 1992; Nicotiana tabacum-1, cyt (seedling), X95932, Dubois et al, 1996; N. tabacum-2, cyt (seedling), X95933, Dubois et al, 1996; Oryza sativa, cyt (shoot), X14245, Sakamoto et al, 1989; O. sativa, cyt (derived from genomic sequence), AB037595, Kojima et al, 2000;O. sativa, cp, X14246, Sakamoto et al, 1989; Pinus sylvestris, cyt (seedling), X74429, Elmlinger et al, 1994; Pisum sativum-1, cyt (nodule), X05515, ; P. sativum-2, cyt (nodule), X04763, ; P. sativum 3 cyt (nodule) M20663, Tingey et al, 1988; P. sativum cp, M20664, Tingey et al, 1988; Phaseolus vulgaris-1, cyt (root), X04001, Gebhardt et al, 1986; P. vulgaris-2, cyt (root), X04002, Gebhardt et al, 1986;P.…”

Section: Discussionmentioning

confidence: 99%

Novel Expression Pattern of Cytosolic Gln Synthetase in Nitrogen-Fixing Root Nodules of the Actinorhizal Host, Datisca glomerata

Berry

Murphy²,

Okubara³

et al. 2004

Plant Physiology

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Gln synthetase (GS) is the key enzyme of primary ammonia assimilation in nitrogen-fixing root nodules of legumes and actinorhizal (Frankia-nodulated) plants. In root nodules of Datisca glomerata (Datiscaceae), transcripts hybridizing to a conserved coding region of the abundant nodule isoform, DgGS1-1, are abundant in uninfected nodule cortical tissue, but expression was not detectable in the infected zone or in the nodule meristem. Similarly, the GS holoprotein is immunolocalized exclusively to the uninfected nodule tissue. Phylogenetic analysis of the full-length cDNA of DgGS1-1 indicates affinities with cytosolic GS genes from legumes, the actinorhizal species Alnus glutinosa, and nonnodulating species, Vitis vinifera and Hevea brasilensis. The D. glomerata nodule GS expression pattern is a new variant among reported root nodule symbioses and may reflect an unusual nitrogen transfer pathway from the Frankia nodule microsymbiont to the plant infected tissue, coupled to a distinctive nitrogen cycle in the uninfected cortical tissue. Arg, Gln, and Glu are the major amino acids present in D. glomerata nodules, but Arg was not detected at high levels in leaves or roots. Arg as a major nodule nitrogen storage form is not found in other root nodule types except in the phylogenetically related Coriaria. Catabolism of Arg through the urea cycle could generate free ammonium in the uninfected tissue where GS is expressed.

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“…Nucleotide probes for detection of GS1 and GS2 mRNA were produced by a DNA synthesizer (Applied Biosystem), according to the sequences of cDNA for rice GS1 (GS28: nucleotide position from +318 to +334) and GS2 (GS3 1: nucleotide position from +486 to +502) described by Sakamoto et al (20 (Fig. 1).…”

Section: Quantitation Of Gs and Other Related Enzymes By Immunoblottimentioning

confidence: 99%

A Role for Glutamine Synthetase in the Remobilization of Leaf Nitrogen during Natural Senescence in Rice Leaves

Kamachi¹,

Yamaya²,

Mae³

et al. 1991

Plant Physiol.

247

171

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Changes in the levels of cytosolic glutamine synthetase (GS1) and chloroplastic glutamine synthetase (GS2) polypeptides and of corresponding mRNAs were determined in leaves of hydroponically grown rice (Oryza sativa) plants during natural senescence. The plants were grown in the greenhouse for 105 days at which time the thirteenth leaf was fully expanded. This was counted as zero time for senescence of the twelfth leaf. The twelfth leaf blade on the main stem was analyzed over a time period of -7 days (98 days after germination) to +42 days (147 days after germination). Total GS activity declined to less than a quarter of its initial level during the senescence for 35 days and this decline was mainly caused by a decrease in the amount of GS2 polypeptide. Immunoblotting analyses showed that contents of other chloroplastic enzymes, such as ribulose-1,5-bisphosphate carboxylase/oxygenase and Fd-glutamate synthase, declined in parallel with GS2. In contrast, the GS1 polypeptide remained constant throughout the senescence period. Translatable mRNA for GS1 increased about fourfold during the senescence for 35 days. During senescence, there was a marked decrease in content of glutamate (to about one-sixth of the zero time value); glutamate is the major form of free amino acid in rice leaves. Glutamine, the major transported amino acid, increased about threefold compared to the early phase of the harvest in the senescing rice leaf blades. These observations suggest that GS1 in senescing leaf blades is responsible for the synthesis of glutamine, which is then transferred to the growing tissues in rice plants.The major source of nitrogen for developing leaves and ears in mature rice plants is the nitrogen released from older senescing leaves. Our previous study with 'sN showed that remobilized nitrogen accounted for 64% of the total nitrogen in the youngest leaf blades (12). Rubisco, the major soluble protein in leaves, decreases with senescence and is the principal source of transported nitrogen (8,12 Glutamate is a major free amino acid in mature leaf blades of rice. Recently, Hayashi and Chino (7) showed that glutamine and asparagine accounted for 42 and 12%, respectively, of the total amino acids in phloem sap of rice plants. These amides are derived from amino acids and ammonia released by the hydrolysis of Rubisco, other leaf proteins, and Chl.GS2 is a candidate for the conversion of glutamate and NH4' to glutamine in senescing leaves and the resultant glutamine could be the precursor for asparagine (18,19).However, GS activity is known to decrease rapidly during either natural senescence of wheat leaves (2, 21) or dark induced senescence of detached Lolium temulentum leaves (24) and radish cotyledons (10). In many plants, there are two isoforms of GS in leaves (17): one located in the cytosol (GS 1) and the other in the chloroplast stroma (GS2). Because the physiological function of GS2 is considered to be the reassimilation of NH4' released during photorespiration (26,27) and because the rate of photosynth...

show abstract

Three cDNA sequences coding for glutamine synthetase polypeptides in Oryza sativa L.

Cited by 67 publications

References 10 publications

Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes.

Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes.

Novel Expression Pattern of Cytosolic Gln Synthetase in Nitrogen-Fixing Root Nodules of the Actinorhizal Host, Datisca glomerata

A Role for Glutamine Synthetase in the Remobilization of Leaf Nitrogen during Natural Senescence in Rice Leaves

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