期刊论文详细信息
BMC Genomics
An integrated “omics” approach to the characterization of maize (Zea mays L.) mutants deficient in the expression of two genes encoding cytosolic glutamine synthetase
Bertrand Hirel2  Céline Dargel-Graffin2  Thérèse Tercé-Laforgue2  Isabelle Quilleré2  Thierry Balliau4  Benoît Valot4  Michel Zivy4  Nicolas Agier1  Gilles Clément2  Sandrine Imbaud3  Nardjis Amiour2 
[1] Centre National de la Recherche Sceintifique, Unité Mixte de Recherche 7238, Biologie Computationnelle et Quantitative, F-75006 Paris, France;Institut Jean-Pierre Bourgin, Institut National de la Recherche Agronomique (INRA), Centre de Versailles-Grignon, Unité Mixte de Recherche 1318 INRA-Agro-ParisTech, Equipe de Recherche Labellisée, Centre National de la Recherche Scientifique 3559, RD10, F-78026 Versailles, Cedex, France;Centre de Génétique Moléculaire, Unité Propre de Recherche 2167, Centre National de la Recherche Scientifique and, Gif/Orsay DNA MicroArray Platform (GODMAP), 1, avenue de la Terrasse, F-91198, Gif sur Yvette Paris, France;Platerforme d’Analyse Protéomique de Paris Sud-Ouest, Unité Mixte de Recherche de Génétique Végétale, Ferme du Moulon, F-91190, Gif/Yvette, Paris, France
关键词: Yield;    Transcriptome;    Proteome;    Nitrogen;    Mutant;    Metabolome;    Maize;    Grain filling;    Glutamine synthetase;    Assimilation;   
Others  :  1091776
DOI  :  10.1186/1471-2164-15-1005
 received in 2014-06-19, accepted in 2014-11-04,  发布年份 2014
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【 摘 要 】

Background

To identify the key elements controlling grain production in maize, it is essential to have an integrated view of the responses to alterations in the main steps of nitrogen assimilation by modification of gene expression. Two maize mutant lines (gln1.3 and gln1.4), deficient in two genes encoding cytosolic glutamine synthetase, a key enzyme involved in nitrogen assimilation, were previously characterized by a reduction of kernel size in the gln1.4 mutant and by a reduction of kernel number in the gln1.3 mutant. In this work, the differences in leaf gene transcripts, proteins and metabolite accumulation in gln1.3 and gln1.4 mutants were studied at two key stages of plant development, in order to identify putative candidate genes, proteins and metabolic pathways contributing on one hand to the control of plant development and on the other to grain production.

Results

The most interesting finding in this study is that a number of key plant processes were altered in the gln1.3 and gln1.4 mutants, including a number of major biological processes such as carbon metabolism and transport, cell wall metabolism, and several metabolic pathways and stress responsive and regulatory elements. We also found that the two mutants share common or specific characteristics across at least two or even three of the “omics” considered at the vegetative stage of plant development, or during the grain filling period.

Conclusions

This is the first comprehensive molecular and physiological characterization of two cytosolic glutamine synthetase maize mutants using a combined transcriptomic, proteomic and metabolomic approach. We find that the integration of the three “omics” procedures is not straight forward, since developmental and mutant-specific levels of regulation seem to occur from gene expression to metabolite accumulation. However, their potential use is discussed with a view to improving our understanding of nitrogen assimilation and partitioning and its impact on grain production.

【 授权许可】

   
2014 Amiour et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Hirel B, Le Gouis J, Ney B, Gallais A: The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 2007, 58:2369-2387.
  • [2]Good AG, Beatty PH: Fertilizing nature: a tragedy of excess in the commons. PLoS Biol 2011, 9:e1001124.
  • [3]Andrews M, Lea PJ: Our nitrogen footprint: the need for increased crop nitrogen use efficiency. Ann Appl Biol 2013, 163:165-169.
  • [4]Bertin P, Gallais A: Physiological and genetic basis of nitrogen use efficiency in maize.II. QTL detection and coincidences. Maydica 2001, 46:53-68.
  • [5]Gallais A, Hirel B: An approach of the genetics of nitrogen use efficiency in maize. J Exp Bot 2004, 55:295-306.
  • [6]Wang L, Zhong M, Li X, Yuan D, Xu Y, Liu H, He Y, Luoi L, Zhang Q: The QTL controlling amino acid content in grains of rice (Oryza sativa) are co-localized with the regions involved in the amino acid metabolism pathway. Mol Breed 2008, 21:127-137.
  • [7]Xie HL, Ji HQ, Liu Z, Tian GW, Wang CL, Hu YM, Tang JH: Genetic basis for nutritional content of stover in maize under low nitrogen conditions. Euphytica 2009, 165:485-493.
  • [8]Cai H, Chu Q, Gu R, Yuan L, Liu J, Zhang X, Chen F, Mi G, Zhang F: Identification of QTLs for plant height, ear height and grain yield in maize (Zea mays L.) in response to nitrogen and phosphorus supply. Plant Breed 2012, 131:502-510.
  • [9]Liu R, Zhang H, Zhao P, Zhang Z, Liang W, Tian Z, Zheng Y: Mining of candidate maize genes for nitrogen use efficiency by integrating gene expression and QTL data. Plant Mol Biol Rep 2012, 30:297-308.
  • [10]Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A: Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 2001, 125:1258-1270.
  • [11]Zhang N, Gibon Y, Gur A, Chen C, Lepak N, Höhne M, Zhang Z, Kroon D, Tschoep H, Stitt M, Buckler E: Fine quantitative trait loci mapping of carbon and nitrogen metabolism enzyme activities and seedling biomass in the maize IBM mapping population. Plant Physiol 2010, 154:1753-1765.
  • [12]Wen W, Li D, Li X, Gao Y, Li W, Li H, Liu J, Liu H, Chen W, Luo J, Yan J: Metabolome-based genome wide association study of maize kernel leads to novel biochemical insights. Nat Commun 2014, 5:3438. doi:10.1038/ncoms4438
  • [13]Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatou C, Balliau T, Valot B, Davanture M, Dubois F, Tercé-Laforgue T, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Quilleré I, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B: Two cytosolic glutamine synthetase isoforms of maize (Zea mays L.) are specifically involved in the control of grain production. Plant Cell 2006, 18:3252-3274.
  • [14]Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T, Sato T: Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J Exp Bot 2001, 52:1209-1217.
  • [15]Tabuchi M, Sugiyama T, Ishiyama K, Inoue E, Sato T, Takahashi H, Yamaya T: Severe reduction in growth and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase 1;1. Plant J 2005, 42:641-655.
  • [16]Hirel B, Martin Tercé-Laforgue T, Gonzalez-Moro MB, Estavillo JM: Physiology of maize I: A comprehensive and integrated view of nitrogen metabolism in a C4 plant. Physiol Plant 2005, 124:167-177.
  • [17]Fritz C, Palacios-Rojas NP, Feil R, Stitt M: Regulation of secondary metabolism by the carbon-nitrogen status of tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 2006, 46:533-548.
  • [18]Amiour N, Imbaud S, Clement G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quilleré I, Cañas RA, Tercé-laforgue T, Hirel B: The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 2012, 63:5017-5033.
  • [19]Loewus FA, Murthy PN: Myo-inositol metabolism in plants. Plant Sci 2000, 150:1-19.
  • [20]Stoop JMH, Williamson JD, Pharr DM: Mannitol metabolism in plants: a method for coping with stress. Trends Plant Sci 1996, 1:139-144.
  • [21]Taji T, Ohsumi C, Iuchi S, Deki M, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K: Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 2002, 29:417-426.
  • [22]Miret JA, Munné-Bosch S: Plant amino acid-derived vitamins: biosynthesis and function. Amino Acids 2013, 46:809-824.
  • [23]Li J, Copeland L: Role of malonate in chickpeas. Phytochemistry 2000, 54:585-589.
  • [24]Engqvist MKM, Khun A, Wienstroer J, Weber K, Jansen EEW, Jakobs C, Weber APM, Maurino VG: Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. J Biol Chem 2011, 286:11382-11390.
  • [25]Olivier RA, Bedgar DL, Davin LB, Lewis NG: The arogenate dehydratase gene family: towards understanding differential regulation of carbon flux through phenylalanine into primary versus secondary metabolic pathways. Phytochemistry 2012, 82:22-37.
  • [26]Boerjan W, Ralph J, Baucher M: Lignin biosynthesis. Annu Rev Plant Biol 2003, 54:519-546.
  • [27]Seebauer JR, Moose SP, Fabbri BJ, Crossland LD, Below FE: Amino acid metabolism in maize ear shoots. Implications for assimilate preconditioning and nitrogen signalling. Plant Physiol 2004, 136:4326-4334.
  • [28]Hancock RD, Morris WL, Ducreux LJM, Morris JA, Usman M, Verrall SR, Fuller JF, Simpson GG, Zhang R, Hedley PE, Taylor MA: Physiological, biochemical and molecular response of the potato (Solanum tuberosum L.) plant to moderately elevated temperature. Plant Cell Environ 2014, 37:439-450.
  • [29]Below FE, Cazetta JO, Seebauer JR: Carbon/Nitogen interactions during ear and kernel development of maize. In Physiology and Modelling Kernel Set in Maize. Volume 29. Edited by Westgate ME, Boote KJ. Madison, WI: Crop Science Society of American and American Society of Agronomy; 2000::15-24.
  • [30]Seebauer JR, Singletary GW, Krumpelman M, Ruffo ML, Below FE: Relationship of source and sink in determining kernel composition in maize. J Exp Bot 2010, 61:511-519.
  • [31]Schnarrenberger C, Flechner A, Martin W: Enzymatic evidence for a complete oxidative pentose phosphate pathway in chloroplasts and an incomplete pathway in the cytosol of spinach leaves. Plant Physiol 1995, 108:609-614.
  • [32]Furbank RT, Taylor WC: Regulation of photosynthesis in C3 and C4 plants: a molecular approach. Plant Cell 1995, 7:797-807.
  • [33]Wang L, Li Y, Jacquot JP, Rouhier N, Xia B: Characterization of poplar GrxS14 in different structural forms. Protein Cell 2014. doi:10.1007/s13238-014-0042-3
  • [34]Dietz KJ, Jacob S, Oelze ML, Laxa M, Tognetti V, Nunes de Miranda SM, Baier M, Finkemeir I: The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 2011, 57:1697-1709.
  • [35]Gutu A, Nesbit AD, Alverson AJ, Palmer JD, Kehoe DM: Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression. Proc Natl Acad Sci U S A 2013, 110:16253-16258.
  • [36]Russel DA, Sachs MM: Differential expression and sequence analysis of the maize glyceraldehyde-3-phosphate dehydrogenase gene family. Plant Cell 1989, 1:793-803.
  • [37]Hussain SS, Ali M, Ahmad M, Siddique KHM: Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 2011, 29:300-311.
  • [38]Simons M, Saha R, Guillard L, Clément G, Armengaud P, Cañas R, Maranas CD, Lea PJ, Hirel B: Nitrogen use efficiency in maize (Zea mays L.): from “omics” studies to metabolic modelling. J Exp Bot 2014, 65:5657-5671.
  • [39]Bahrman N, Le Gouis J, Negroni L, Amilhat L, Leroy P, Lainé AL, Jaminon O: Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen regimes. Proteomics 2004, 4:709-719.
  • [40]Prinsi B, Negri AS, Pesaresi P, Cocucci M, Espen L: Evaluation of protein pattern changes in roots and leaves of Zea mays plants in response to nitrate availability by two-dimensional gel electrophoresis analysis. BMC Plant Biol 2009, 9:113. BioMed Central Full Text
  • [41]MØller ALB, Pedas P, Andersen B, Svensson B, Schoerring JK, Finnie C: Responses of barley root and shoot proteomes to long-term nitrogen deficiency, short term nitrogen starvation and ammonium. Plant Cell Environ 2011, 34:2024-2037.
  • [42]Tovar-Méndez A, Miernyk JA, Randall DD: Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 2003, 270:1043-1049.
  • [43]Vincent R, Fraisier V, Chaillou S, Limami MA, Deléens E, Phillipson B, Douat C, Boutin JP, Hirel B: 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 1997, 201:424-433.
  • [44]Sato Y, Antonio B, Namiki N, Motoyama R, Sugimoto K, Takehisa H, Minmi H, Kamatsuki K, Kusababa M, Hirochika H, Nagamura Y: Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol 2011, 11:10. BioMed Central Full Text
  • [45]Shen Y, Venu RC, Nobuta K, Wu X, Notibala V, Demirci C, Meyers BC, Wang GL, Ji G, Li QQ: Transcriptome dynamics through alternative polyadenylation in developmental environmental responses in plants revealed by deep sequencing. Genome 2011, 21:1478-1486.
  • [46]Hoppe A: What mRNA abundances can tell us about metabolism. Metabolites 2012, 2:614-631.
  • [47]Fernie AR, Stitt M: On the discordance of metabolomics with proteomics and transcriptomics: coping with increasing complexity in logic, chemistry and network interaction. Plant Physiol 2012, 158:1139-1145.
  • [48]Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D: Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 2012, 19:463-476.
  • [49]Li XP, Björkman O, Shih C, Crossman AR, Rosenquist M, Jansson S, Niyogi KK: A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 2010, 403:391-395.
  • [50]Takahashi S, Badger M: Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 2011, 16:53-60.
  • [51]Senger B, Auxilien S, Englisch , Cramer F, Fasiolo F: The modified wobble base inosine in yeast tRNA is a positive determinant for aminoacylation by isoleucyl-tRNA synthetase. Biochemistry 1997, 36:8269-8275.
  • [52]Taniguchi T, Miyaushi K, Nakane D, Miyata M, Muto A, Nishimura S, Suzuki T: Decoding system for the UAU codon tRNAIle with the UAU anticodon in Mycoplasma mobile. Nucleic Acids Res 2013, 41:2621-2631.
  • [53]Slewinski TL: Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant 2011, 4:641-662.
  • [54]Gupta S, Gallavotti G, Stryker GA, Schmidt RJ, Lal SK: A novel class of Helitron-related transposable element in maize contain portions of multiple pseudogenes. Plant Mol Biol 2005, 57:115-127.
  • [55]Schuler MA, Werck-Reichart D: Functional genomics of P450s. Annu Rev Plant Biol 2003, 54:629-667.
  • [56]Broyart C, Fontaine J-X, Molinié R, Cailleu D, Tercé-Laforgue T, Dubois F, Hirel B, Mesnard F: Metabolic profiling of maize mutants deficient for two glutamine synthetase isoenzymes using 1H-NMR-based metabolomics. Phytochem Anal 2010, 21:102-109.
  • [57]Cañas RA, Quilleré I, Lea PJ, Hirel B: Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotechnol J 2010, 8:966-978.
  • [58]Shen H, Mazarei M, Hisano H, Escamilla-Trevino L, Fu C, Pu Y, Rudis MR, Tang Y, Xiao X, Jackson L, Li G, Hernandez T, Chen F, Ragauskas AJ, Neal Stewart C Jr, Wang ZY, Dixon RA: A genomic approach to deciphering lignin biosynthesis in switchgrass. Plant Cell 2013, 25:4342-4361.
  • [59]Minic Z: Physiological role of plant glycoside hydrolases. Planta 2008, 227:723-740.
  • [60]Kasprzewska A: Plant chitinase-regulation and function. Cell Mol Biol Lett 2003, 8:809-824.
  • [61]Zhao Y, Dong W, Zhang N, Ai X, Wang M, Huang Z, Xiao L, Xia G: A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signalling. Plant Physiol 2013, 164:1068-1076.
  • [62]Maris C, Dominguez C, Allain FHT: The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 2005, 272:2118-2131.
  • [63]Fontaine JX, Tercé-Laforgue T, Armengaud P, Clément G, Renou JP, Pelletier S, Catterou M, Azzopardi M, Gibon Y, Lea PJ, Hirel B, Bubois F: Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell 2012, 24:4044-4065.
  • [64]Andrews M, Raven JA, Lea PJ: Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann Appl Biol 2013, 163:174-199.
  • [65]Dauwe R, Moreel K, Goemine G, Gielen , Rohde A, Van Beeumen J, Ralph J, Boudet AM, Kopka J, Rochange SF, Halpin C, Messens E, Boerjan W: Molecular phenotyping of lignin-modified tobacco reveals associated changes in cell-wall metabolism, primary metabolism, stress metabolism and photorespiration. Plant J 2007, 52:263-285.
  • [66]Hirai M, Yano M, Goodenove DB, Kanaya S, Kimura T, Awazuhara M, Fujiwara T, Saito : Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2004, 101:10205-12010.
  • [67]Kant SK, Bi YM, Rothstein S: Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 2011, 62:1400-1509.
  • [68]Gutiérrez RA: Systems biology for enhanced plant nitrogen nutrition. Science 2012, 336:1673-1675.
  • [69]Kruger NJ, Ratcliffe RG: Pathways and fluxes: exploring the plant metabolic network. J Exp Bot 2012, 63:2243-2246.
  • [70]Ruppin E, Papin JA, de Figueiredo LF, Schuster S: Metabolic reconstruction, constraint-based analysis and game theory to probe genome-scale metabolic networks. Curr Opin Biotechnol 2010, 21:502-510.
  • [71]Coïc Y, Lesaint C: Comment assurer une bonne nutrition en eau et en ions minéraux en horticulture. Horticulture Française 1971, 8:11-14.
  • [72]Verwoerd TC, Dekker BNM, Hoekema A: A small-scale procedure for the rapid isolation of plants RNAs. Nucleic Acids Res 1989, 17:2362.
  • [73]Méchin V, Thévenot C, Le G, Prioul JL, Damerval C: Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 2007, 143:1203-1219.
  • [74]Fiehn O: Metabolite profiling in Arabidopsis. In Methods in Molecular Biology. 2nd edition. Edited by Salinas J, Sanchez-Serrano JJ. Totowa NJ: Humana Press; 2006:439-447.
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