Skip to main content
Log in

Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

A quantitative trait locus (QTL) associated with the protein content of cytosolic glutamine synthetase (GS1; EC 6.3.1.2) in senescing leaves, panicle number, and panicle weight was characterized in rice (Oryza sativa L.). A near-isogenic line (NIL), C-22, developed by marker-assisted selection was grown under different nitrogen levels in the greenhouse and in a paddy field. Chromosome 2 of C-22 had an approximately 50-cM segment substituted from the Kasalath (indica) chromosome in a Koshihikari (japonica) genetic background. C-22 showed a 12–37% lower content of GS1 protein in leaf blades than Koshihikari, which was in good agreement with a QTL region positively affected by the japonica chromosome. At an early vegetative stage, C-22 had more active tillers than Koshihikari in the greenhouse. At the reproductive stage, both panicle number and total panicle weight of C-22 were significantly higher than those of Koshihikari, particularly when the plants were grown under a low-nitrogen condition. These traits of C-22 were further confirmed in a paddy field. Thus, tiller development was positively affected by the Kasalath chromosome at an early vegetative stage, which resulted in an increased panicle number and panicle weight at the mature stage in C-22. These data indicate that the target QTL (Pnn1; panicle number 1) is important in the development of tillers and panicles in rice. Linkage analyses for panicle number and ratio of developing tiller formation in the second axil (RDT) revealed that Pnn1 was delimited at the 6.7-cM region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahn S, Tanksley SD (1993) Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci USA 90:7980–7984

    CAS  PubMed  Google Scholar 

  • Avila C, Suárez MF, Gómez-Maldonado J, Cánovas FM (2001) Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development. Plant J 25:93–102

    Article  CAS  PubMed  Google Scholar 

  • Bourque JE (1995) Antisense strategies for genetic manipulations in plants. Plant Sci 105:125–149

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brugière M, Doubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, Hirel B (1999) Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell 11:1995–2011

    Article  PubMed  Google Scholar 

  • Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  CAS  PubMed  Google Scholar 

  • Dubois F, Brugière N, Sangwan RS, Hirel B (1996) Localization of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ- and cell-specific patterns of protein synthesis and gene expression. Plant Mol Biol 31:803–817

    CAS  PubMed  Google Scholar 

  • Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Google Scholar 

  • Fuentes SI, Allen DJ, Ortiz-Lopez A, Hernández G (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52:1071–1081

    Article  CAS  PubMed  Google Scholar 

  • Goto S, Akagawa T, Kojima S, Hayakawa T, Yamaya T (1998) Organization and structure of NADH-dependent glutamate synthase gene from rice plants. Biochim Biophys Acta 1387:298–308

    CAS  PubMed  Google Scholar 

  • Hayakawa T, Yamaya T, Mae T, Ojima K (1993) Changes in the content of two glutamate synthase proteins in spikelets of rice (Oryza sativa) plants during ripening. Plant Physiol 101:1257–1262

    CAS  PubMed  Google Scholar 

  • Hayashi H, Chino M (1990) Chemical composition of phloem sap from the upper most internode of the rice plant. Plant Cell Physiol 31:247–251

    CAS  Google Scholar 

  • Hirel B, Bertin P, Quilleré I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125:1258–1270

    Article  CAS  PubMed  Google Scholar 

  • Ireland R, Lea P (1999) The enzymes of glutamine glutamate asparagine and aspartate metabolism. In: Singh B (ed) Plant amino acids: biochemistry and biotechnology. Marcel Dekker, New York, pp 49–109

    Google Scholar 

  • Kamachi K, Yamaya T, Mae T, Ojima K (1991) A role for glutamine synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol 96:411–417

    CAS  Google Scholar 

  • Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci USA 100:11765–11770

    Article  CAS  PubMed  Google Scholar 

  • Lea P, Robinson S, Stewart G (1990) The enzymology and metabolism of glutamine glutamate and asparagine. In: Miflin P, Lea P (eds) The biochemistry of plants, vol 16. Academic, San Diego, pp 121–157

  • Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621

    Article  CAS  PubMed  Google Scholar 

  • Limami AM, Rouillon C, Glebarec G, Gallais A, Hirel B (2002) Genetic and physiological analysis of germination efficiency in maize in relation to nitrogen metabolism reveals the importance of cytosolic glutamine synthetase. Plant Physiol 130:1860–1870

    Article  CAS  PubMed  Google Scholar 

  • Lin HX, Yamamoto T, Sasaki T, Yano M (2000) Characterization and detection of epistatic interactions of 3 QTLs Hd1 Hd2 and Hd3 controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101:1021–1028

    Article  CAS  Google Scholar 

  • Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96:997–1003

    Article  CAS  Google Scholar 

  • Loudet O, Chaillou S, Merigout P, Talbotec J, Daniel-Vedele F (2003) Quantitative trait loci analysis of nitrogen use efficiency in Arabidopsis. Plant Physiol 131:345–358

    Article  CAS  PubMed  Google Scholar 

  • Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization photosynthesis and yield potential. Plant Soil 196:201–210

    Article  CAS  Google Scholar 

  • Mae T, Ohira K (1981) The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22:1067–1074

    CAS  Google Scholar 

  • Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-15-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant Cell Physiol 25:429–437

    CAS  Google Scholar 

  • Makino A, Mae T, Ohira K (1988) Differences between wheat and rice in the enzymatic properties of ribulose-15-bisphosphate carboxylase/oxygenase and relationship to photosynthetic gas exchange. Planta 174:30–38

    CAS  Google Scholar 

  • Mickelson S, See D, Meyer FD, Garner JP, Foster CR, Blake TK, Fischer AM (2003) Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves. J Exp Bot 54:801–812

    Article  CAS  PubMed  Google Scholar 

  • Nelson JC (1997) qgene: software of marker-based genomic analysis and breeding. Mol Breed 3:239–245

    Article  CAS  Google Scholar 

  • Nesbitt TC, Tanksley SD (2001) fw2.2 directly affects the size of developing tomato fruit with secondary effects on fruit number and photosynthate distribution. Plant Physiol 127:575–583

    Article  CAS  PubMed  Google Scholar 

  • Obara M, Sato T, Yamaya T (2000) High content of cytosolic glutamine synthetase does no accompany a high activity of the enzyme in rice (Oryza sativa) leaves of indica cultivars. Physiol Plant 108:11–18

    Article  CAS  Google Scholar 

  • Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T, Sato T (2001) Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J Exp Bot 52:1209–1217

    Article  CAS  PubMed  Google Scholar 

  • Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM (2002) Overexpression of cytosolic glutamine synthetase: relation to nitrogen light and photorespiration. Plant Physiol 129:1170–1180

    Article  CAS  PubMed  Google Scholar 

  • Ortega JL, Temple SJ, Sengupta-Gopalan C (2001) Constitutive overexpression of cytosolic glutamine synthetase (GS1) gene in transgenic alfalfa demonstrates that GS1 may be regulated at the level of RNA stability and protein turnover. Plant Physiol 126:109–121

    Article  CAS  PubMed  Google Scholar 

  • Rauh BL, Basten C, Buckler ES IV (2002) Quantitative trait loci analysis of growth response to varying nitrogen sources in Arabidopsis thaliana. Theor Appl Genet 104:743–750

    Article  CAS  PubMed  Google Scholar 

  • Sakurai N, Hayakawa T, Nakamura T, Yamaya T (1996) Changes in the cellular localization of cytosolic glutamine synthetase protein in vascular bundles of rice at various stages of development. Planta 200:306–311

    Article  CAS  Google Scholar 

  • Sechley K, Yamaya T, Oaks A (1992) Compartmentation of nitrogen assimilation in higher plants. Int Rev Cytol 134:85–163

    CAS  Google Scholar 

  • Stam M, de Bruin R, van Blokland R, van der Hoorn RAL, Mol JMM, Kooter JM (2000) Distinct features of post-transcriptional gene silencing by antisense transgenes in single copy and inverted T-DNA repeat loci. Plant J 21:27–42

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi M, Umetsu T, Hongo Y, Hayakawa T, Yamaya T (2004) Localization of cytosolic glutamine synthetase isozymes in rice. Plant Cell Physiol 45[Suppl]:s97

    Google Scholar 

  • Takahashi N (1984) Differentiation of ecotypes in Oryza sativa L. In: Tunoda S, Takahashi N (eds) Biology of rice. Scientific, Tokyo, pp 31–67

    Google Scholar 

  • Takahashi Y, Shomura A, Sasaki T, Yano M (2001) Hd6, a rice quantitative trait locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proc Natl Acad Sci USA 98:7922–7927

    Article  CAS  PubMed  Google Scholar 

  • Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–223

    Article  CAS  PubMed  Google Scholar 

  • Temple SJ, Bagga S, Sengupta-Goplan C (1998) Down-regulation of specific members of the glutamine synthetase gene family in alfalfa by antisense RNA technology. Plant Mol Biol 37:535–547

    Article  CAS  PubMed  Google Scholar 

  • Tobin AK, Yamaya T (2001) Cellular compartmentation of ammonium assimilation in rice and barely. J Exp Bot 52:591–604

    Article  CAS  PubMed  Google Scholar 

  • Ukai Y, Ohsama U, Saito A, Hayashi T (1995) mapl: a package of DNA polymorphism linkage maps and analysis of QTL. Breed Sci 45:139–142

    Google Scholar 

  • Vincent R, Fraisier V, Chaillou S, Limami MA, Deleens E, Phillipson B, Douat C, Boutin JP, Hirel B (1997) Overexpression of a soybean gene encoding cytosolic glutamine synthetase in shoots of transgenic Lotus corniculatus L. plants triggers changes in ammonium assimilation and plant development. Planta 201:424–433

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Woo Y, Kim CS, Larkins BA (2001) Quantitative trait locus for mapping of loci influencing elongation factor 1α content in maize endosperm. Plant Physiol 125:1271–1282

    Article  CAS  PubMed  Google Scholar 

  • Yamaya T, Hayakawa T, Tanasawa K, Kamachi K, Mae T, Ojima K (1992) Tissue distribution of glutamate synthase and glutamine synthetase in rice leaves. Plant Physiol 100:1427–1432

    CAS  Google Scholar 

  • Yamaya T, Tanno H, Hirose N, Watanabe S, Hayakawa T (1995) A supply of nitrogen causes increase in the level of NADH-dependent glutamate synthase protein and in the activity of the enzyme in roots of rice seedling. Plant Cell Physiol 36:1197–1204

    CAS  Google Scholar 

  • Yamaya T, Obara M, Hayakawa T, Sato T (1997) Comparison of contents for cytosolic-glutamine synthetase and NADH-dependent glutamate synthase proteins in leaves of japonica indica and javanica rice plants. Soil Sci Plant Nutr 43:1107–1112

    CAS  Google Scholar 

  • Yamaya T, Obara M, Nakajima H, Sasaki S, Hayakawa T, Sato T (2002) Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. J Exp Bot 53:917–925

    Article  CAS  PubMed  Google Scholar 

  • Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monnna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1 a major photoperiod sensitivity quantitative trait locus in rice is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S (1981) Fundamentals of rice crop science. The International Rice Research Institute, Manila

    Google Scholar 

  • Zhuang JY, Lin HX, Lu J, Qian HR, Hittalmani S, Huang N, Zheng KL (1997) Analysis of QTL×environment interaction for yield components and plant height in rice. Theor Appl Genet 9:799–808

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported in part by a program of CREST of JST (Japan Science Technology), in part by Grants-in-Aid (Nos. 10556075, 12460029, 13460144, 14360035, 14654160, and 15380003) for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and in part by Rice Genome Project 1016 (IP6001) and Genome Resource Project GE1004, Ministry of Agriculture, Forestry and Fisheries of Japan. M.O was supported by a Research Fellowship of the Japan Society for the Promotion of Science for Young Scientists.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tadashi Sato.

Additional information

Communicated by D.J. Mackill

Rights and permissions

Reprints and permissions

About this article

Cite this article

Obara, M., Sato, T., Sasaki, S. et al. Identification and characterization of a QTL on chromosome 2 for cytosolic glutamine synthetase content and panicle number in rice. Theor Appl Genet 110, 1–11 (2004). https://doi.org/10.1007/s00122-004-1828-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1828-0

Keywords

Navigation