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Coregulation of glutamine synthetase1;2 (GLN1;2) and NADH-dependent glutamate synthase (GLT1) gene expression in Arabidopsis roots in response to ammonium supply

Kojima, Soichi Minagawa, Haruka Yoshida, Chika Inoue, Eri Takahashi, Hideki Ishiyama, Keiki 東北大学

2023.02.20

概要

Plants absorb nitrogen from the soil to grow (Marschner, 1995).
The nitrogen that plants absorb from the soil is either ammonium
or nitrate. Nitrate is reduced to ammonium. Ammonium is
combined with glutamate and assimilated into glutamine
(Marschner, 1995). Ammonium is assimilated primarily in the
roots where the glutamine synthetase (GS or GLN) catalyzes this
reaction. (Vega-Mas et al., 2019; Kojima et al., 2020). Subsequently,
an amino group of glutamine transfers to 2-OG to synthesize
glutamate. Glutamate synthase (glutamine 2-oxoglutarate
aminotransferase; GOGAT) catalyzes this reaction. Thus, GS and
GOGAT are the enzymes for these conjugate reactions. Ammonium
assimilation through the GS/GOGAT cycle is the major pathway of
nitrogen assimilation in plants (Lea and Miﬂin, 1974).
Genome sequencing has revealed various isoenzymes of GS/
GOGAT in plants. Among them are the isoenzymes expressed in
plant roots in response to ammonium supply, such as GS1;2 and
NADH-GOGAT1 from rice (Tabuchi et al., 2007) and GLN1;2 and
NADH-GOGAT (GLT1) from Arabidopsis (Ishiyama et al., 2004a;
Kojima et al., 2014; Konishi et al., 2014). Their transcript and
protein accumulation that occurs in response to ammonium
manifests the importance of these isoenzymes in ammonium
assimilation. Reverse genetic analysis has provided evidence that
loss of these ammonium-responsive GS/GOGAT isoenzymeencoding genes results in reduced ammonium assimilation in
plants, particularly in the roots, preventing normal growth
(Tamura et al., 2010; Funayama et al., 2013; Konishi et al., 2014;
Konishi et al., 2017; Konishi et al., 2018). These results have
suggested that ammonium-responsive forms of GS/GOGAT play
a central role in the primary assimilation of ammonium in roots
(Yamaya and Kusano, 2014). Since the transcripts levels of these
isoenzyme-encoding genes increase with ammonium supply, it may
be inferred that plants have a transcriptional network to regulate
their gene expression in response to ammonium.
Although much of our knowledge has been focused on gene
expression networks associated with nitrate as a signal (Konishi and
Yanagisawa et al., 2010; Wang et al., 2010; Liseron-Monﬁls et al.,
2013), recent studies also highlight transcriptional networks
modulating ammonium responses (Gao et al., 2020; Coleto et al.,
2021; Di et al., 2021). WRKY46 is a transcription factor induced by
ammonium and regulates ammonium efﬂux by modulating
expression of genes involved in the conjugation of IAA and
NUDX9 in Arabidopsis roots (Di et al., 2021). MYB28 and MYB29
are found as transcription factors whose genetic defects increase
sensitivity to ammonium (Coleto et al., 2021). WRKY23 is another
transcription factor found to be necessary for adaptation of
Arabidopsis to high concentrations of ammonium supply (Gao
et al., 2020). Notably, despite the necessity of this transcription
factor in ameliorating the ammonium toxicity, its loss of function
that led to an increased ammonium accumulation in roots had no
signiﬁcant impact on ammonium responsiveness of GS gene
expression (Gao et al., 2020). ...

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参考文献

Castro-Mondragon, J. A., Riudavets-Puig, R., Rauluseviciute, I., Berhanu Lemma, R.,

Turchi, L., Blanc-Mathieu, R., et al. (2021). JASPAR 2022: the 9th release of the openaccess database of transcription factor binding proﬁles. Nucleic Acids Res. 50 (D1),

D165–D173. doi: 10.1093/nar/gkab1113

Fujiwara, T., Hirai, M. Y., Chino, M., Komeda, Y., and Naito, S. (1992). Effects of

sulfur nutrition on expression of the soybean seed storage protein genes in transgenic

petunia. Plant Physiol. 99 (1), 263–268. doi: 10.1104/pp.99.1.263

Funayama, K., Kojima, S., Tabuchi-Kobayashi, M., Sawa, Y., Nakayama, Y.,

Hayakawa, T., et al. (2013). Cytosolic glutamine synthetase1;2 is responsible for the

primary assimilation of ammonium in rice roots. Plant Cell Physiol. 54 (6), 934–943.

doi: 10.1093/pcp/pct046

Chiu, W. L., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996).

Engineered GFP as a vital reporter in plants. Curr. Biol. 6 (3), 325–330. doi: 10.1016/

S0960-9822(02)00483-9

Clough, S. J., and Bent, A. F. (1998). Floral dip: A simpliﬁed method for

Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16 (6),

735–743. doi: 10.1046/j.1365-313x.1998.00343.x

Gao, K., Zhou, T., Hua, Y., Guan, C., and Zhang, Z. (2020). Transcription factor

WRKY23 is involved in ammonium-induced repression of Arabidopsis primary root

growth under ammonium toxicity. Plant Physiol. Biochem. 150, 90–98. doi: 10.1016/

j.plaphy.2020.02.034

Coleto, I., Bejarano, I., Marı́n-Peña, A. J., Medina, J., Rioja, C., Burow, M., et al.

(2021). Arabidopsis thaliana transcription factors MYB28 and MYB29 shape

ammonium stress responses by regulating fe homeostasis. New Phytol. 229 (2),

1021–1035. doi: 10.1111/nph.16918

Gaudinier, A., Rodriguez-Medina, J., Zhang, L. F., Olson, A., Liseron-Monﬁls, C.,

Bagman, A. M., et al. (2018). Transcriptional regulation of nitrogen-associated

metabolism and growth. Nature 563 (7730), 259–264. doi: 10.1038/s41586-0180656-3

Di, D.-W., Sun, L., Wang, M., Wu, J., Kronzucker, H. J., Fang, S., et al. (2021).

WRKY46 promotes ammonium tolerance in arabidopsis by repressing NUDX9 and

indole-3-acetic acid-conjugating genes and by inhibiting ammonium efﬂux in the root

elongation zone. New Phytol. 232 (1), 190–207. doi: 10.1111/nph.17554

Frontiers in Plant Science

Hirose, N., Hayakawa, T., and Yamaya, T. (1997). Inducible accumulation of mRNA

for NADH-dependent glutamate synthase in rice roots in response to ammonium ions.

Plant Cell Physiol. 38 (11), 1295–1297. doi: 10.1093/oxfordjournals.pcp.a029120

frontiersin.org

Kojima et al.

10.3389/fpls.2023.1127006

transcription factors in Arabidopsis thaliana. Plant Cell Physiol. 51 (12), 2145–2151.

doi: 10.1093/jxb/erm066

Hirose, N., and Yamaya, T. (1999). Okadaic acid mimics nitrogen-stimulated

transcription of the NADH-glutamate synthase gene in rice cell cultures. Plant

Physiol. 121 (3), 805–812. doi: 10.1104/pp.121.3.805

Naito, S., Hirai, M. Y., Chino, M., and Komeda, Y. (1994). Expression of a soybean

(Glycine max [L.] merr.) seed storage protein gene in transgenic Arabidopsis thaliana

and its response to nutritional stress and to abscisic acid mutations. Plant Physiol. 104

(2), 497–503. doi: 10.1104/pp.104.2.497

Ishiyama, K., Hayakawa, T., and Yamaya, T. (1998). Expression of NADHdependent glutamate synthase protein in the epidermis and exodermis of rice roots

in response to the supply of ammonium ions. Planta 204 (3), 288–294. doi: 10.1007/

s004250050258

Niwa, Y., Hirano, T., Yoshimoto, K., Shimizu, M., and Kobayashi, H. (1999). Noninvasive quantitative detection and applications of non-toxic, S65T-type green

ﬂuorescent protein in living plants. Plant J. 18 (4), 455–463. doi: 10.1046/j.1365313X.1999.00464.x

Ishiyama, K., Inoue, E., Tabuchi, M., Yamaya, T., and Takahashi, H. (2004b).

Biochemical background and compartmentalized functions of cytosolic glutamine

synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol. 45

(11), 1640–1647. doi: 10.1093/pcp/pch190

Ohashi, M., Ishiyama, K., Kojima, S., Konishi, N., Sasaki, K., Miyao, M., et al. (2018).

Outgrowth of rice tillers requires availability of glutamine in the basal portions of

shoots. Rice 11 (31). doi: 10.1186/s12284-018-0225-2

Ishiyama, K., Inoue, E., Watanabe-Takahashi, A., Obara, M., Yamaya, T., and

Takahashi, H. (2004a). Kinetic properties and ammonium-dependent regulation of

cytosolic isoenzymes of glutamine synthetase in arabidopsis. J. Biol. Chem. 279 (16),

16598–16605. doi: 10.1074/jbc.M313710200

Sarasketa, A., Gonzá lez-Moro, M. B., Gonzá lez-Murua, C., and Marino, D. (2014).

Exploring ammonium tolerance in a large panel of arabidopsis thaliana natural

accessions. J. Exp. Bot. 65 (20), 6023–6033. doi: 10.1093/jxb/eru342

Ishiyama, K., Kojima, S., Takahashi, H., Hayakawa, T., and Yamaya, T. (2003). Cell

type distinct accumulations of mRNA and protein for NADH-dependent glutamate

synthase in rice roots in response to the supply of NH4+. Plant Physiol. Biochem. 41 (67), 643–647. doi: 10.1016/S0981-9428(03)00078-0

Sasaki, K., and Kojima, S. (2018). Identiﬁcation of genomic regions regulating

ammonium-dependent inhibition of primary root length in Arabidopsis thaliana. Soil

Sci. Plant Nutr. 64 (6), 746–751. doi: 10.1080/00380768.2018.1524268

Kan, C. C., Chung, T. Y., Juo, Y. A., and Hsieh, M. H. (2015). Glutamine rapidly

induces the expression of key transcription factor genes involved in nitrogen and stress

responses in rice roots. BMC Genomics 16 (1), 731. doi: 10.1186/s12864-015-1892-7

Shibata, M., Breuer, C., Kawamura, A., Clark, N. M., Rymen, B., Braidwood, L., et al.

(2018). GTL1 and DF1 regulate root hair growth through transcriptional repression of

ROOT HAIR DEFECTIVE 6-LIKE 4 in Arabidopsis. Development 145 (3).

doi: 10.1242/dev.159707

Kojima, S. (2018). The possible interaction of ammonium and auxin polar transport

on root system architectures in the two ecotypes of Arabidopsis thaliana. Soil Sci.Plant

Nutri. 64 (5), 616–622.

Shibata, M., Favero, D. S., Takebayashi, R., Takebayashi, A., Kawamura, A., Rymen,

B., et al. (2022). Trihelix transcription factors GTL1 and DF1 prevent aberrant root hair

formation in an excess nutrient condition. New Phytol. 235 (4), 1426–1441.

doi: 10.1111/nph.18255

Kojima, S., Ishiyama, K., Beier, M. P., and Hayakawa, T. (2020). “Ammonium

assimilation and metabolism in rice,” in Progress in botany, vol. 82 . Eds. F. M. Cá novas,

U. Lüttge, M.-C. Risueño and H. Pretzsch (Cham: Springer International Publishing),

211–231. doi: 10.1007/124_2020_40

Subudhi, P. K., Garcia, R. S., Coronejo, S., and Tapia, R. (2020). Comparative

transcriptomics of rice genotypes with contrasting responses to nitrogen stress reveals

genes inﬂuencing nitrogen uptake through the regulation of root architecture. Int. J.

Mol. Sci. 21 (16). doi: 10.3390/ijms21165759

Kojima, S., Konishi, N., Beier, M. P., Ishiyama, K., Maru, I., Hayakawa, T., et al.

(2014). NADH-dependent glutamate synthase participated in ammonium assimilation

in Arabidopsis root. Plant Signal. Behav. 9 (8), e29402. doi: 10.4161/psb.29402

Tabuchi, M., Abiko, T., and Yamaya, T. (2007). Assimilation of ammonium ions and

reutilization of nitrogen in rice (Oryza sativa l.). J. Exp. Bot. 58 (9), 2319–2327.

doi: 10.1093/jxb/erm016

Konishi, N., Ishiyama, K., Beier, M. P., Inoue, E., Kanno, K., Yamaya, T., et al. (2017).

Contribution of two glutamine synthetase isozymes to ammonium assimilation in

arabidopsis roots. J. Exp. Bot. 68 (3), 613–625. doi: 10.1093/jxb/erw454

Tamura, W., Hidaka, Y., Tabuchi, M., Kojima, S., Hayakawa, T., Sato, T., et al.

(2010). Reverse genetics approach to characterize a function of NADH-glutamate

synthase1 in rice plants. Amino Acids 39 (4), 1003–1012. doi: 10.1007/s00726-0100531-5

Konishi, N., Ishiyama, K., Matsuoka, K., Maru, I., Hayakawa, T., Yamaya, T., et al.

(2014). NADH-dependent glutamate synthase plays a crucial role in assimilating

ammonium in the arabidopsis root. Physiol. Plantar 152 (1), 138–151. doi: 10.1111/

ppl.12177

Valvekens, D., Vanmontagu, M., and Vanlijsebettens, M. (1988). Agrobacterium

tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using

kanamycin selection. Proc. Natl. Acad. Sci. U.S.A. 85 (15), 5536–5540. doi: 10.1073/

pnas.85.15.55

Konishi, N., Saito, M., Imagawa, F., Kanno, K., Yamaya, T., and Kojima, S. (2018).

Cytosolic glutamine synthetase isozymes play redundant roles in ammonium

assimilation under low-ammonium conditions in roots of Arabidopsis thaliana.

Plant Cell Physiol. 59 (3), 601–613. doi: 10.1093/pcp/pcy014

Vega-Mas, I., Cukier, C., Coleto, I., Gonzá lez-Murua, C., Limami, A. M., Gonzá lezMoro, M. B., et al. (2019). Isotopic labelling reveals the efﬁcient adaptation of wheat

root TCA cycle ﬂux modes to match carbon demand under ammonium nutrition. Sci.

Rep. 9 (1). doi: 10.1038/s41598-019-45393-8

Konishi, M., and Yanagisawa, S. (2010). Identiﬁcation of a nitrate-responsive ciselement in the arabidopsis NIR1 promoter deﬁnes the presence of multiple cisregulatory elements for nitrogen response. Plant J. 63 (2), 269–282. doi: 10.1111/

j.1365-313X.2010.04239.x

Lea, P. J., and Miﬂin, B. J. (1974). Alternative route for nitrogen assimilation in

higher plants. Nature 251 (5476), 614–616. doi: 10.1038/251614a0

Wang, R., Guan, P., Chen, M., Xing, X., Zhang, Y., and Crawford, N. M. (2010).

Multiple regulatory elements in the arabidopsis NIA1 promoter act synergistically to

form a nitrate enhancer. Plant Physiol. 154 (1), 423–432. doi: 10.1104/pp.110.162586

Liang, T., Yuan, Z., Fu, L., Zhu, M., Luo, X., Xu, W., et al. (2021). Integrative

transcriptomic and proteomic analysis reveals an alternative molecular network of

glutamine synthetase 2 corresponding to nitrogen deﬁciency in rice (Oryza sativa l.).

Int. J. Mol. Sci. 22 (14). doi: 10.3390/ijms22147674

Xu, Y., Wang, Y., Du, J., Pei, S., Guo, S., Hao, R., et al. (2022). A DE1 BINDING

FACTOR 1–GLABRA2 module regulates rhamnogalacturonan I biosynthesis in

arabidopsis seed coat mucilage. Plant Cell 34 (4), 1396–1414. doi: 10.1093/plcell/

koac011

Liseron-Monﬁls, C., Bi, Y. M., Downs, G. S., Wu, W., Signorelli, T., Lu, G., et al.

(2013). Nitrogen transporter and assimilation genes exhibit developmental stageselective expression in maize (Zea mays l.) associated with distinct cis-acting

promoter motifs. Plant Signal. Behav. 8 (10). doi: 10.4161/psb.26056

Yabuki, Y., Ohashi, M., Imagawa, F., Ishiyama, K., Beier, M. P., Konishi, N., et al.

(2017). A temporal and spatial contribution of asparaginase to asparagine catabolism

during development of rice grains. Rice 10, 1–10. doi: 10.1186/s12284-017-0143-8

Yamaya, T., and Kusano, M. (2014). Evidence supporting distinct functions of three

cytosolic glutamine synthetases and two NADH-glutamate synthases in rice. J. Exp.

Bot. 65 (19), 5519–5525. doi: 10.1093/jxb/eru103

Marschner, H. (1995). Mineral nutrition of higher plants (London: Academic Press).

Maruyama-Nakashita, A., Nakamura, Y., Watanabe-Takahashi, A., Inoue, E.,

Yamaya, T., and Takahashi, H. (2005). Identiﬁcation of a novel cis-acting element

conferring sulfur deﬁciency response in arabidopsis roots. Plant J. 42 (3), 305–314.

doi: 10.1111/j.1365-313X.2005.02363.x

Yang, S.-y., Hao, D.-l., Song, Z.-z., Yang, G.-z., Wang, L., and Su, Y.-h. (2015). RNASeq analysis of differentially expressed genes in rice under varied nitrogen supplies.

Gene 555 (2), 305–317. doi: 10.1016/j.gene.2014.11.021

Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T., and Takahashi, H. (2004). A

novel regulatory pathway of sulfate uptake in Arabidopsis roots: Implication of CRE1/

WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 38 (5), 779–789.

doi: 10.1111/j.1365-313X.2004.02079.x

Yasuda, T., Konishi, N., and Kojima, S. (2017). Ammonium uptake capacity and

response of cytosolic glutamine synthetase 1;2 to ammonium supply are key factors for

the adaptation of ammonium nutrition in arabidopsis thaliana. Soil Sci. Plant Nutr. 63

(6), 553–560. doi: 10.1080/00380768.2017.1395292

Miller, A. J., Fan, X. R., Orsel, M., Smith, S. J., and Wells, D. M. (2007). Nitrate

transport and signalling. J. Exp. Bot. 58 (9), 2297–2306. doi: 10.1093/jxb/erm066

Zhou, T., Hua, Y., Yue, C., Huang, J., and Zhang, Z. (2021). Physiologic,

metabolomic, and genomic investigations reveal distinct glutamine and mannose

metabolism responses to ammonium toxicity in allotetraploid rapeseed genotypes.

Plant Sci. 310, 110963. doi: 10.1016/j.plantsci.2021.110963

Mitsuda, N., Ikeda, M., Takada, S., Takiguchi, Y., Kondou, Y., Yoshizumi, T., et al.

(2010). Efﬁcient yeast one-/two-hybrid screening using a library composed only of

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Coregulation of glutamine synthetase1;2 (GLN1;2) and NADH-dependent glutamate synthase (GLT1) gene expression in Arabidopsis roots in response to ammonium supply

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Coregulation of glutamine synthetase1;2 (GLN1;2) and NADH-dependent glutamate synthase (GLT1) gene expression in Arabidopsis roots in response to ammonium supply

概要

この論文で使われている画像

関連論文

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