Abstract
The ability to coordinate carbon (C) and nitrogen (N) metabolism enables plants to regulate development and metabolic responses to different environmental conditions. The regulator(s) or sensor(s) that monitor crosstalk between biosynthetic pathways and ultimately control the flow of C or N through them have remained elusive. We used an antisense strategy to demonstrate that the putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of C and N metabolism in Arabidopsis. Seeds from AtGLR1.1-deficient Arabidopsis (antiAtGLR1.1) lines did not germinate in the presence of an animal ionotropic glutamate receptor (iGLR) antagonist, but germination was restored upon coincubation with an iGLR agonist or the putative ligand glutamate. In antiAtGLR1.1 lines, endogenous abscisic acid (ABA) concentrations increased with iGLR antagonist treatments and decreased with coincubation with an iGLR agonist, suggesting that germination was controlled by ABA. antiAtGLR1.1 seedlings also exhibited sensitivity to increased levels of Ca2+ compared with wild type, and they exhibited a conditional phenotype that was sensitive to the C:N ratio. In the presence of C, specifically sucrose, but not glucose, mannitol, or sorbitol, antiAtGLR1.1 seeds did not germinate, but germination was restored upon coincubation with NO3-, but not NH4+. Immunoblot, isoenzyme, and RT-PCR analyses indicate that AtGLR1.1 regulates the accumulation of distinct C- and N-metabolic enzymes, hexokinase 1 (HXK1) and zeaxanthin epoxidase (ABA1), by transcriptional control. We provide a model to describe the role of AtGLR1.1 in C/N metabolism and ABA biosynthesis, which in turn controls seed germination.
MeSH Terms
Amino Acid Sequence
Arabidopsis/metabolism
Base Sequence
Carbon/metabolism
DNA Primers
Nitrogen/metabolism
Receptors, Glutamate/physiology
Reverse Transcriptase Polymerase Chain Reaction
Chemicals
DNA Primers
Receptors, Glutamate
Carbon
Nitrogen
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Kang Jiman
Department of Biological Sciences, George Washington University, Washington, DC 20052, USA.
Turano Frank J
References (26)
26 references, click to expand
-
Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar.
Genes Dev. 2000 Aug 15;14(16):2085-96
PMID: 10950871
-
Characterization of a single soybean cDNA encoding cytosolic and glyoxysomal isozymes of aspartate aminotransferase.
Plant Mol Biol. 1998 May;37(1):99-108
PMID: 9620268
-
Screening for non-protein amino acids in seeds of the Guam cycad, Cycas circinalis, by an improved GC-MS method.
Planta Med. 1995 Feb;61(1):66-70
PMID: 7700995
-
The glutamate receptor ion channels.
Pharmacol Rev. 1999 Mar;51(1):7-61
PMID: 10049997
-
Glutamate-receptor genes in plants.
Nature. 1998 Nov 12;396(6707):125-6
PMID: 9823891
-
Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'.
Curr Opin Plant Biol. 2001 Jun;4(3):247-53
PMID: 11312136
-
Glutamate-gated calcium fluxes in Arabidopsis.
Plant Physiol. 2000 Dec;124(4):1511-4
PMID: 11115867
-
A PII-like protein in Arabidopsis: putative role in nitrogen sensing.
Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13965-70
PMID: 9811909
-
Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis.
Plant Physiol. 1987 Jan;83(1):155-8
PMID: 16665193
-
Arabidopsis mutants resistant to S(+)-beta-methyl-alpha, beta-diaminopropionic acid, a cycad-derived glutamate receptor agonist.
Plant Physiol. 2000 Dec;124(4):1615-24
PMID: 11115879
-
Hexokinase as a sugar sensor in higher plants.
Plant Cell. 1997 Jan;9(1):5-19
PMID: 9014361
-
Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation.
Plant Physiol. 2000 Jul;123(3):817-24
PMID: 10889231
-
The identity of plant glutamate receptors.
Science. 2001 May 25;292(5521):1486-7
PMID: 11379626
-
In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration.
Methods Mol Biol. 1998;82:259-66
PMID: 9664431
-
Expression and distribution of cytosolic 6-phosphogluconate dehydrogenase isozymes in maize.
Biochem Genet. 1992 Jun;30(5-6):233-46
PMID: 1616479
-
Chloroplast and cytosolic glutamine synthetase are encoded by homologous nuclear genes which are differentially expressed in vivo.
J Biol Chem. 1988 Jul 15;263(20):9651-7
PMID: 2898472
-
Isolation and characterization of a soybean cDNA clone encoding the plastid form of aspartate aminotransferase.
Plant Mol Biol. 1993 Mar;21(6):993-1009
PMID: 7683917
-
A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions.
Plant Cell. 2002 Nov;14(11):2723-43
PMID: 12417697
-
Characterization and expression of NAD(H)-dependent glutamate dehydrogenase genes in Arabidopsis.
Plant Physiol. 1997 Apr;113(4):1329-41
PMID: 9112779
-
Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants.
Plant Cell Physiol. 2001 Jan;42(1):74-84
PMID: 11158446
-
Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged.
Mol Biol Evol. 1999 Jun;16(6):826-38
PMID: 10368960
-
Abscisic acid inhibits germination of mature Arabidopsis seeds by limiting the availability of energy and nutrients.
Planta. 1997 Oct;203(2):182-7
PMID: 9362564
-
Regulation of Arabidopsis root development by nitrate availability.
J Exp Bot. 2000 Jan;51(342):51-9
PMID: 10938795
-
Nitrogen and carbon nutrient and metabolite signaling in plants.
Plant Physiol. 2001 Jan;125(1):61-4
PMID: 11154297
-
The aspartate aminotransferase gene family of Arabidopsis encodes isoenzymes localized to three distinct subcellular compartments.
Plant J. 1995 Jan;7(1):61-75
PMID: 7894512
-
Purification and characterization of NADP+-linked isocitrate dehydrogenase from scots pine . Evidence for different physiological roles of the enzyme in primary development
Plant Physiol. 1998 Oct;118(2):617-26
PMID: 9765548