Asparagine synthetase1, but not asparagine synthetase2, is responsible for the biosynthesis of asparagine following the supply of ammonium to rice roots

Plant and Cell Physiology

Volumn 56, Issue 4, 2015, Pages 769-778

  Ohashi, Miwa ^a   Ishiyama, Keiki ^a   Kojima, Soichi ^a   Konishi, Noriyuki ^a   Nakano, Kentaro ^b   Kanno, Keiichi ^a   Hayakawa, Toshihiko ^a   Yamaya, Tomoyuki ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b Cambridge Technology Partners Co Ltd   (Japan)

Author keywords

Ammonium assimilation; Asparagine synthetase; Cytosolic glutamine synthetase; Knockout mutant; NADH glutamate synthase; Rice root

Indexed keywords

AMMONIUM DERIVATIVE; ASPARAGINE; ASPARTATE AMMONIA LIGASE; CARBON; MESSENGER RNA; NITROGEN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; MERISTEM; METABOLISM; MOLECULAR GENETICS; MUTATION; ORYZA; PHENOTYPE; PLANT GENE; PLANT ROOT; REAL TIME POLYMERASE CHAIN REACTION; SEEDLING; SHOOT;

AMINO ACID SEQUENCE; AMMONIUM COMPOUNDS; ASPARAGINE; ASPARTATE-AMMONIA LIGASE; CARBON; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; GENES, PLANT; MERISTEM; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN; ORYZA; PHENOTYPE; PLANT PROTEINS; PLANT ROOTS; PLANT SHOOTS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEEDLINGS;

EID: 84942109958     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv005     Document Type: Article

References (49)

1. Boehlein, S.K., Walworth, E.S., Richards, N.G. and Schuster, S.M. (1997a) Mutagenesis and chemical rescue indicate residues involved in betaaspartyl-AMP formation by Escherichia coli asparagine synthetase B. J. Biol. Chem. 1272: 12384-12392.
2. Boehlein, S.K., Walworth, E.S. and Schuster, S.M. (1997b) Identification of cysteine-523 in the aspartate binding site of Escherichia coli asparagine synthetase B. Biochemistry 36: 10168-10177.
3. Chevalier, C., Bourgeois, E., Just, D. and Raymond, P. (1996) Metabolic regulation of asparagine synthetase gene expression in maize (Zea mays L.) root tips. Plant J. 9: 1-11.
4. +-dependent asparaginase, NSE1, is crucial for plant growth and seed production in Lotus japonicas. Plant Cell Physiol. 54: 107-118.
5. Davies, K.M. and King, C.A. (1993) Isolation and characterization of a cDNA clone for a harvest-induced asparagine synthetase from Asparagus officinalis L. Plant Physiol. 102: 1337-1340.
6. Fukumorita, T. and Chino, M. (1982) Sugar, amino-acid, and inorganic contents in rice phloem sap. Plant Cell Physiol. 23: 273-283.
7. 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: 934-943.
8. Gaufichon, L., Masclaux-Daubresse, C., Tcherkez, G., Reisdorf-Cren, M., Sakakibara, Y., Hase, T. et al. (2013) Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant Cell Environ. 36: 328-324.
9. Gaufichon, L., Reisdorf-Cren, M., Rothstein, S.J., Chardon, F. and Suzukia, A. (2010) Biological functions of asparagine synthetase in plants. Plant Sci. 179: 141-153.
10. Gu, T., Duan, F., An, X., Zhang, F., von Wirén, N. and Yuan, L. (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol. 54: 1515-1524.
11. Hayashi, H. and Chino, M. (1990) Chemical composition of phloem sap from the upper most internode of the rice plant. Plant Cell Physiol. 31: 247-251.
12. Herrera-Rodríguez, M.B., Carrasco-Ballesteros, S., Maldonado, J.M., Pineda, M., Aguilar, M. and Pérez-Vicente, R. (2002) Three genes showing distinct regulatory patterns encode the asparagine synthetase of sunflower (Helianthus annuus). New Phytol. 155: 33-45.
13. Herrera-Rodríguez, M.B., Maldonado, J.M. and Pérez-Vicente, R. (2004) Light and metabolic regulation of HAS1, HAS1.1 and HAS2, three asparagine synthetase genes in Helianthus annuus. Plant Physiol. Biochem. 42: 511-518.
14. Herrera-Rodríguez, M.B., Maldonado, J.M. and Pérez-Vicente, R. (2006) Role of asparagine and asparagine synthetase genes in sunflower (Helianthus annuus) germination and natural senescence. J. Plant Physiol. 163: 1061-1070.
15. Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H. and Kanda, M. (1996) Retrotransposon of rice involved in mutations induced by tissue culture. Proc. Natl Acad. Sci. USA 93: 7783-7788.
16. 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: 1295-1297.
17. Ireland, R.J. and Lea, P.J. (1999) The enzymes of glutamine, glutamate, asparagine and aspartate metabolisms. In Plant Amino Acids. Biochemistry and Biotechnology. Edited by Singh, B.K. pp. 49-109. Marcel Dekker Inc., New York.
18. Ishiyama, K., Inoue, E., Tabuchi, M., Yamaya, T. and Takahashi, H. (2004) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol. 45: 1640-1647.
19. Ishiyama, K., Kojima, S., Takahashi, H., Hayakawa, T. and Yamaya, T. (2003) Cell type distinct accumulations of mRNA and protein for NADHdependent glutamate synthase in rice roots in response to the supply of NH4 +. Plant Physiol. Biochem. 41: 643-647.
20. Kamachi, K., Yamaya, T., Hayakawa, T., Mae, T. and Ojima, K. (1992) Vascular bundle-specific localization of cytosolic glutamine synthetase in rice leaves. Plant Physiol. 99: 1481-1486.
21. Kamada-Nobusada, T., Makita, N., Kojima, M. and Sakakibara, H. (2013) Nitrogen-dependent regulation of de novo cytokinin biosynthesis in rice: The role of glutamine metabolism as an additional signal. Plant Cell Physiol. 54: 1881-1893.
22. Kawachi, T., Sueyoshi, K., Nakajima, A., Yamagata, H., Sugimoto, T. and Oji, Y. (2002) Expression of asparagine synthetase in rice (Oryza sativa) roots in response to nitrogen. Physiol. Plant. 114: 41-46.
23. 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. Plant. 152: 138-151.
24. Lam, H.M., Hsieh, M.H. and Coruzzi, G.M. (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J. 16: 345-353.
25. Lam, H.M., Peng, S.S. and Coruzzi, G.M. (1994) Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol. 106: 1347-1357.
26. Larsen, T.M., Boehlein, S.K., Schuster, S.M., Richards, N.G., Thoden, J.B., Holden, H.M. et al. (1999) Three-dimensional structure of Escherichia coli asparagine synthetase B: A short journey from substrate to product. Biochemistry 38: 16146-16157.
27. Lea, P.J., Sodek, L., Parry, M.A.J., Shewry, P.R. and Halford, N.G. (2007) Asparagine in plants. Ann. Appl. Biol. 150: 1-26.
28. Luo, L., Li, W., Miura, K., Ashikari, M. and Kyozuka, J. (2012) Control of tiller growth of rice by OsSPL14 and strigolactones, which work in two independent pathways. Plant Cell Physiol. 53: 1793-1801.
29. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K. et al. (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion in retrotransposon-rich regions of the genome. Plant Cell 15: 1771-1780.
30. Morita, S., Lux, A., Enstone, D.E., Peterson, C.A. and Abe, J. (1996) Reexamination of rice seminal root ontogeny using fluorescence microscopy. Jpn. J. Crop Sci. 65: 37-38.
31. Nakano, K., Suzuki, T., Hayakawa, T. and Yamaya, T. (2000) Organ cellular localization of asparagine synthetase in rice plants. Plant Cell Physiol. 41: 874-880.
32. Ohashi, M., Ishiyama, K., Kusano, M., Fukushima, A., Kojima, S., Hanada, A. et al. (2015) Lack of cytosolic glutamine synthetase1;2 in vascular tisses of axillary buds caused severe reduction in their outgrowth and disorder of metabolic balance in rice seedlings. Plant J. 81: 347-356.
33. Oliveira, I.C. and Coruzzi, G.M. (1999) Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis. Plant Physiol. 121: 301-310.
34. + uptake in roots of Arabidopsis thaliana: Evidence for regulation by root glutamine levels. Plant J. 19: 143-152.
35. Sakai, H., Lee, S.S., Tanaka, T., Numa, H., Kim, J., Kawahara, Y. et al. (2013) Rice annotation project database (RAP-DB): An integrative and interactive database for rice genomics. Plant Cell Physiol. 54: E6.
36. Sakakibara, H., Takei, K. and Hirose, N. (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 11: 440-448.
37. Sakurai, N., Hayakawa, T., Nakamura, T. and Yamaya, T. (1996) Changes in the cellular localization of cytosolic glutamine synthetase protein in vascular bundles of rice leaves at various stages of development. Planta 200: 306-311.
38. Sonoda, Y., Ikeda, A., Saiki, S., von Wirén, N., Yamaya, T. and Yamaguchi, J. (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1;1-1;3) in rice. Plant Cell Physiol. 44: 726-734.
39. 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: 2319-2327.
40. Tabuchi, M., Sugiyama, K., Ishiyama, K., Inoue, E., Sato, T., Takahashi, H. et al. (2005) Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant J. 42: 641-651.
41. Tamura, W., Hidaka, Y., Tabuchi, M., Kojima, S., Hayakawa, T., Sato, T. et al. (2010) Reverse genetic approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids 39: 1003-1012.
42. Tamura, W., Kojima, S., Toyokawa, A., Watanabe, H., Tabuchi-Kobayashi, M., Hayakawa, T. et al. (2011) Disruption of a novel NADH-glutamate synthase2 gene caused marked reduction in spikelet number of rice. Front. Plant Sci. 2: 57.
43. Tsai, F.Y. and Coruzzi, G.M. (1990) Dark-induced and organ-specific expression of two asparagine synthetase genes in Pisum sativum. EMBO J. 9: 323-332.
44. Tsai, F.Y. and Coruzzi, G.M. (1991) Light represses transcription of asparagine synthetase genes in photosynthetic and nonphotosynthetic organs of plants. Mol. Cell Biol. 11: 4966-4972.
45. Urquhart, A.A. and Joy, K.W. (1981) Use of phloem exudate technique in the study of amino acid transport in pea plants. Plant Physiol. 68: 750-754.
46. Vincentz, M., Moureaux, T., Leydecker, M.T., Vaucheret, H. and Caboche, M. (1993) Regulation of nitrate and nitrite reductase expression in Nicotiana plumbaginifolia leaves by nitrogen and carbon metabolites. Plant J. 3: 315-324.
47. 2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and their diurnal patterns in Arabidopsis thaliana: possible relationships with respiratory rates. Plant Cell Physiol. 55: 341-357.
48. Wong, H.K., Chan, H.K., Coruzzi, G.M. and Lam, H.M. (2004) Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis. Plant Physiol. 134: 332-338.
49. 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: 5519-5525.