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Overexpression of a glutamine synthetase gene affects growth and development in sorghum

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Abstract

Nitrogen is a primary macronutrient in plants, and nitrogen fertilizers play a critical role in crop production and yield. In this study, we investigated the effects of overexpressing a glutamine synthetase (GS) gene on nitrogen metabolism, and plant growth and development in sorghum (Sorghum bicolor L., Moench). GS catalyzes the ATP dependent reaction between ammonia and glutamate to produce glutamine. A 1,071 bp long coding sequence of a sorghum cytosolic GS gene (Gln1) under the control of the maize ubiquitin (Ubq) promoter was introduced into sorghum immature embryos by Agrobacterium-mediated transformation. Progeny of the transformants exhibited higher accumulation of the Gln1 transcripts and up to 2.2-fold higher GS activity compared to the non-transgenic controls. When grown under optimal nitrogen conditions, these Gln1 transgenic lines showed greater tillering and up to 2.1-fold increase in shoot vegetative biomass. Interestingly, even under greenhouse conditions, we observed a seasonal component to both these parameters and the grain yield. Our results, showing that the growth and development of sorghum Gln1 transformants are also affected by N availability and other environmental factors, suggest complexity of the relationship between GS activity and plant growth and development. A better understanding of other control points and the ability to manipulate these will be needed to utilize the transgenic technology to improve nitrogen use efficiency of crop plants.

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References

  • Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620

    Article  CAS  PubMed  Google Scholar 

  • Brauer EK, Rochon A, Bi YM, Bozzo GG, Rothstein SJ, Shelp BJ (2011) Reappraisal of nitrogen use efficiency in rice overexpressing glutamine synthetase1. Physiol Plant 141:361–372

    Article  CAS  PubMed  Google Scholar 

  • Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X (2009) Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Rep 28:527–537

    Article  CAS  PubMed  Google Scholar 

  • El Omari R, Rueda-Lopez M, Avila C, Crespillo R, Nhiri M, Canovas FM (2010) Ammonium tolerance and the regulation of two cytosolic glutamine synthetases in the roots of sorghum. Funct Plant Biol 37:55–63

    Article  Google Scholar 

  • Finnemann J, Schjoerring JK (2000) Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. Plant J 24:171–181

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Zhang H (2011) Nitrogen metabolism in plants in the post-genomic era. Annu Plant Rev 42:1–366

    Google Scholar 

  • Fu J, Sampalo R, Gallardo F, Canovas FM, Kirby EG (2003) Assembly of a cytosolic pine glutamine synthetase holoenzyme in leaves of transgenic poplar leads to enhanced vegetative growth in young plants. Plant Cell Environ 26:411–418

    Article  CAS  Google Scholar 

  • Fuentes SI, Allen AJ, Ortiz A, Hernandez 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 

  • Funayama K, Kojima S, Tabuchi-Kobayashi M, Sawa Y, Nakayama Y, Hayakawa T, Yamaya T (2013) Cytosolic glutamine synthetase 1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant Cell Physiol 54:934–943

    Article  CAS  PubMed  Google Scholar 

  • Gallardo F, Fu J, Cantón FR, García-Gutiérrez A, Cánovas FM, Kirby EG (1999) Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210:19–26

    Article  CAS  PubMed  Google Scholar 

  • Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605

    Article  CAS  PubMed  Google Scholar 

  • Habash DZ, Massiah AJ, Rong HL, Wallsgrove RM, Leigh RA (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138:83–89

    Article  CAS  Google Scholar 

  • Hirel B, Gadal P (1982) Glutamine synthetase isoforms in leaves of a C4 plant: Sorghum vulgare. Physiol Plant 54:69–74

    Article  CAS  Google Scholar 

  • Husted S, Hebbern CA, Mattsson M, Schjoerring JK (2000) A critical experimental evaluation of methods for determination of NH4+ in plant tissue, xylem sap and apoplastic fluid. Physiol Plant 109:167–179

    Article  CAS  Google Scholar 

  • Katayama H, Mori M, Kawamura Y, Tanaka T, Mori M, Hasegawa H (2009) Production and characterization of transgenic rice plants carrying a high-affinity nitrate transporter gene (OsNRT2.1). Breed Sci 59:237–243

    Article  CAS  Google Scholar 

  • Kebrom TH, Spielmeyer W, Finnegan EJ (2013) Grasses provide new insights into regulation of shoot branching. Trends Plant Sci 18:41–48

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Campbell L, Rathore K (2011) Rapid recovery- and characterization of transformants following Agrobacterium-mediated T-DNA transfer to sorghum. Plant Cell Tissue Organ Cult 104:137–146

    Article  CAS  Google Scholar 

  • Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce-Laforgue T, Quillere I, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1025

    Article  CAS  PubMed  Google Scholar 

  • Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53:979–987

    Article  CAS  PubMed  Google Scholar 

  • Migge A, Carrayol E, Hirel B, Becker TW (2000) Leaf-specific overexpression of plastidic glutamine synthetase stimulates the growth of transgenic tobacco seedlings. Planta 210:252–260

    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  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Neal D, Joy KW (1973) Glutamine synthetase of pea leaves. I. Purification, stabilization, and pH optima. Arch Biochem Biophys 159:113–122

    Article  PubMed  Google Scholar 

  • Ortega JL, Moguel-Esponda S, Potenza C, Conklin CF, Quintana A, Sengupta-Gopalan C (2006) The 3′ untranslated region of a soybean cytosolic glutamine synthetase (GS1) affects transcript stability and protein accumulation in transgenic alfalfa. Plant J 45:832–846

    Article  CAS  PubMed  Google Scholar 

  • Ortega J, Wilson O, Sengupta-Gopalan C (2012) The 5′ untranslated region of the soybean cytosolic glutamine synthetase β1 gene contains prokaryotic translation initiation signals and acts as a translational enhancer in plants. Mol Genet Genomics 287:881–893

    Article  CAS  PubMed  Google Scholar 

  • Palanichelvam K, Oger P, Clough SJ, Cha C, Bent AF, Farrand SK (2000) A second T-region of the soybean-supervirulent chrysopine-type Ti plasmid pTiChry5, and construction of a fully disarmed vir helper plasmid. Mol Plant Microbe Interact 13:1081–1091

    Article  CAS  PubMed  Google Scholar 

  • Palle SR, Campbell LM, Pandeya D, Puckhaber L, Tollack LK, Marcel S, Sundaram S, Stipanovic RD, Wedegaertner TC, Hinze L, Rathore KS (2013) RNAi-mediated ultra-low gossypol cottonseed trait: performance of transgenic lines under field conditions. Plant Biotechnol J 11:296–304

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW, Irwin N, Janssen KA (2001) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are thankful to Dr. James Balthrop (Office of the Texas State Chemist, TAMU) for his help with seed protein analyses and to Ms. Virginia Johnson (Protein Chemistry Laboratory, TAMU) for her help with amino acid analyses. J. U. would like to thank the Ministerio de Economía y Finanzas de Panamá, Secretaría Nacional de Ciencia, Tecnología e Innovación, and Instituto para la Formación y Aprovechamiento de Recursos Humanos for the scholarship provided during the course of her Ph.D.

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Authors and Affiliations

  1. Institute for Plant Genomics and Biotechnology, Texas A&M University, College Station, TX, 77843-2123, USA

    Jazmina Urriola & Keerti S. Rathore

  2. Department of Soil and Crop Sciences, Texas A&M University, College Station, TX, 77843-2474, USA

    Keerti S. Rathore

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  1. Jazmina Urriola
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  2. Keerti S. Rathore
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Correspondence to Keerti S. Rathore.

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Urriola, J., Rathore, K.S. Overexpression of a glutamine synthetase gene affects growth and development in sorghum. Transgenic Res 24, 397–407 (2015). https://doi.org/10.1007/s11248-014-9852-6

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  • DOI: https://doi.org/10.1007/s11248-014-9852-6

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