Skip to main content

Advertisement

SpringerLink
Log in

Agronomic improvements through the genetic and physiological regulation of nitrogen uptake in wheat (Triticum aestivum L.)

  • Review Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

Nitrogen (N) uptake is the first step in nitrate assimilation, and efficient N uptake is essential for plant growth, especially for protein biosynthesis and photosynthetic activities. In cereals, improved N uptake is closely coupled with an increase in nitrogen use efficiency (NUE) and yield improvements. Because wheat (Triticum aestivum L.) is a leading crop worldwide, a better understanding of N uptake regulation in wheat is vital to improving NUE and developing sustainable agricultural systems. However, detailed information regarding the biological mechanisms that are responsible for the more efficient uptake of ambient N by wheat is limited. This review presents recent developments in the biological mechanisms of N uptake in wheat, including plant growth regulations, fundamental roles of root systems, interactions between N species, and genetic controls. Specifically, this paper provides a number of potential strategies that can be used to increase wheat N uptake. The information provided here may guide N fertilizer management during wheat production and further elucidate the plant regulatory mechanisms that are involved in N uptake, which can thereby increase wheat NUE.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abreu JP, De ME, Flores I, De Abreu FMG, Madeira MV (1993) Nitrogen uptake in relation to water availability in wheat. Plant Soil 154:89–96

    Article  Google Scholar 

  • Ahuja LR, Reddy VR, Saseendran SA, Yu Q (2008) Response of crops to limited water: understanding and modeling water stress effect on plant growth processes. ASA/CSSA/SSSA, Madison

    Google Scholar 

  • Albrizio R, Todorovic M, Matic T, Stellacci AM (2010) Comparing the interactive effects of water and nitrogen on durum wheat and barley grown in a Mediterranean environment. Field Crops Res 115:179–190

    Article  Google Scholar 

  • An DG, Su JY, Liu QY, Zhu YG, Tong YP, Li JM, Jing RL, Li B, Li ZS (2006) Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant Soil 284:73–84

    Article  CAS  Google Scholar 

  • Baresel JP, Zimmermann G, Reents HJ (2008) Effects of genotype and environment on N uptake and N partition in organically grown winter wheat (Triticum aestivum L.) in Germany. Euphytica 163:347–354

    Article  Google Scholar 

  • Barneix AJ (2007) Physiology and biochemistry of source-regulated protein accumulation in the wheat grain. J Plant Physiol 164:581–590

    Article  PubMed  CAS  Google Scholar 

  • Barrett-Lennard EG, Leighton PD, Buwalda F, Gibbs J, Armstrong W, Thomson CJ, Greenway H (1988) Effects of growing wheat in hypoxic nutrient solutions and of subsequent transfer to aerated solutions. I. growth and carbohydrate status of shoots and roots. Aust J Plant Physiol 15:585–598

    Article  CAS  Google Scholar 

  • Bingham IJ, Karley AJ, White PJ, Thomas WTB, Russell JR (2012) Analysis of improvements in nitrogen use efficiency associated with 75 years of spring barley breeding. Eur J Agron 42:49–58

    Article  Google Scholar 

  • Bradley DP, Morgan MA, O’Toole P (1989) Uptake and apparent utilization of urea and ammonium nitrate in wheat seedlings. Fertil Res 20:41–49

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Butterbach-bahl K, Dannenmann M (2011) Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate. Curr Opin Env Sus 3:389–395

    Article  Google Scholar 

  • Chandna R, Hakeem KR, Khan F, Ahmad A, Iqbal MV (2012) Variability of nitrogen uptake and assimilation among N-efficient and N-inefficient wheat (Triticum aestivum L.) genotypes. J Plant Interact 7:367–375

    Article  CAS  Google Scholar 

  • Chen C, Han G, He H, Westcott M (2011) Yield, protein, and remobilization of water soluble carbohydrate and nitrogen of three spring wheat cultivars as influenced by nitrogen input. Agron J 103:786–795

    Article  CAS  Google Scholar 

  • Collier MD, Fotelli MN, Nahm M, Kopriva S, Rennenberg H, Hanke DE (2003) Regulation of nitrogen uptake by Fagus sylvatica on a whole plant level—interactions between cytokinins and soluble N compounds. Plant Cell Environ 26:1549–1560

    Article  CAS  Google Scholar 

  • Coque M, Martin A, Veyrieras JB, Hirel B, Gallais A (2008) Genetic variation for N- remobilization and post silking N- uptake in a set of maize recombinant inbred lines. 3. QTL detection and coincidences. Theor Appl Genet 117:729–747

    Article  PubMed  CAS  Google Scholar 

  • Deignan MT, Levis OAM (1988) The inhibition of ammonium uptake by nitrate in wheat. New Phytol 110:1–3

    Article  CAS  Google Scholar 

  • Delogu G, Cattivelli L, Pecchioni N, De Falcis D, Maggiore T, Stanca AM (1998) Uptake and agronomic efficiency of nitrogen in winter barley and winter wheat. Eur J Agron 9:11–20

    Article  Google Scholar 

  • Duan YH, Zhang YL, Ye LT, Fan XR, Xu GH, Shen QR (2007) Responses of rice cultivars with different nitrogen use efficiency to partial nitrate nutrition. Ann Bot 99:1153–1160

    Article  PubMed  CAS  Google Scholar 

  • Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J Cereal Sci 38:133–146

    Article  CAS  Google Scholar 

  • Ehdaie B, Merhaut DJ, Ahmadian S, Hoops AC, Khuong T, Layne AP, Waines JG (2010) Root system size influences water-nutrient uptake and nitrate leaching potential in wheat. J Agron Crop Sci 196:455–466

    Article  Google Scholar 

  • El-kereamy A, Guevara D, Bi YM, Chen X, Rothstein SJ (2011) Exploring the molecular and metabolic factors contributing to the adaptation of maize seedlings to nitrate limitation. Front Plant Sci 2:49

    Article  PubMed  CAS  Google Scholar 

  • Fageria NK, Baligar VC, Li YC (2008) The role of nutrient efficient plants in improving crop yields in the twenty first century. J Plant Nutr 31:1121–1157

    Article  CAS  Google Scholar 

  • Fang Y, Xu B, Turner NC, Li F (2010) Does root pruning increase yield and water-use efficiency of winter wheat? Crop Pasture Sci 61:899–910

    Google Scholar 

  • Feng FX, Huang GB, Chai Q, Yu AZ (2010) Tillage and straw management impacts on soil properties, root growth, and grain yield of winter wheat in Northwestern China. Crop Sci 50:1465–1473

    Google Scholar 

  • Fontaine JX, Ravel C, Pageau K, Heumez E, Dubois F, Hirel B, Le Gouis J (2009) A quantitative genetic study for elucidating the contribution of glutamine synthetase, glutamate dehydrogenase and other nitrogen-related physiological traits to the agronomic performance of common wheat. Theor Appl Genet 119:645–662

    Article  PubMed  CAS  Google Scholar 

  • Foulkes MJ, Hawkesford MJ, Barraclough PB, Holdsworth MJ, Kerr S, Kightley S, Shewry PR (2009) Identifying traits to improve the nitrogen economy of wheat: recent advances and future prospects. Field Crops Res 114:329–342

    Article  Google Scholar 

  • Gaju O, Allard V, Martre P, Snape JW, Heumez E, Le Gouis J, Moreau D, Bogard M, Griffiths S, Orford S, Hubbart S, Foulkes MJ (2011) Identification of traits to improve the nitrogen-use efficiency of wheat genotypes. Field Crops Res 123:139–152

    Article  Google Scholar 

  • Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Env 32:1272–1283

    Article  CAS  Google Scholar 

  • Garnica M, Houdusse F, Yvin JC, Garcia-Mina JM (2009) Nitrate modifies urea root uptake and assimilation in wheat seedlings. J Sci Food Agric 89:55–62

    Article  CAS  Google Scholar 

  • Garnica M, Houdusse F, Zamarreño AM, Garcia-Mina JM (2010) The signal effect of nitrate supply enhances active forms of cytokinins and indole acetic content and reduces abscisic acid in wheat plants grown with ammonium. J Plant Physiol 167:1264–1272

    Article  PubMed  CAS  Google Scholar 

  • Geleto T, Tanner DG, Mamo T, Gebeyehu G (1996) Response of rainfed bread and durum wheat to source, level and timing of nitrogen fertilizer on two Ethiopian Vertisols: II. N uptake, recovery and efficiency. Fertil Res 44:195–204

    Article  Google Scholar 

  • Girin T, El-Kafafi ES, Widiez T, Erban A, Hubberten HM, Kopka J, Hoefgen R, Gojon A, Lepetit M (2010) Identification of Arabidopsis mutants impaired in the systemic regulation of root nitrate uptake by the nitrogen status of the plant. Plant Physiol 153:1250–1260

    Article  PubMed  CAS  Google Scholar 

  • Gooding MJ, Addisu M, Uppal RK, Snape JW, Jones HE (2012) Effect of wheat dwarfing genes on nitrogen-use efficiency. J Agr Sci 150:3–22

    Article  CAS  Google Scholar 

  • Górny AG, Banaszak Z, Ługowska B, Ratajczak D (2011) Inheritance of the efficiency of nitrogen uptake and utilization in winter wheat (Triticum aestivum L.) under diverse nutrition levels. Euphytica 177:191–206

    Article  Google Scholar 

  • Hackett C (1972) A method of applying nutrients locally to roots under controlled conditions and some morphological effects of locally applied nitrate on the branching of wheat roots. Aust J Biol Sci 25:1169–1180

    CAS  Google Scholar 

  • Hamid A, Ahmad M (1993) Priming effects of 15N-labelled ammonium nitrate on uptake of soil N by wheat (Triticum aestivum L.) under field conditions. Biol Fertil Soils 15:297–300

    Article  CAS  Google Scholar 

  • Herrera JM, Stamp P, Liedgens M (2007) Interannual variability in root growth of spring wheat (Triticum aestivum L.) at low and high nitrogen supply. Europ J Agron 26:317–326

    Article  Google Scholar 

  • Hirel B, Le Gouis J, Ney B, Gallais A (2007) 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 58:2369–2387

    Article  PubMed  CAS  Google Scholar 

  • Itoh H, Hayashi S, Nakajima T, Hayashi T, Yoshida H, Yamazaki K, Komatsu T (2009) Effects of soil Type, vertical root distribution and precipitation on grain yield of winter wheat. Plant Prod Sci 12:503–513

    Article  Google Scholar 

  • Jenkinson DS, Fox RH, Rayner JH (1985) Interactions between fertilizer nitrogen and soil nitrogen—the so-called “priming” effect. J Soil Sci 36:425–444

    Article  CAS  Google Scholar 

  • Karley AJ, Valentine TA, Squire GR (2011) Dwarf alleles differentially affect barley root traits influencing nitrogen acquisition under low nutrient supply. J Exp Bot 62:3917–3927

    Article  PubMed  CAS  Google Scholar 

  • Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399–1409

    Article  PubMed  CAS  Google Scholar 

  • Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J (2007) In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crops Res 102:22–32

    Article  Google Scholar 

  • King J, Gay A, Sylvester-Bradley R, Bingham I, Foulkes J, Gregory P, Robinson D (2003) Modelling cereal root systems for water and nitrogen capture: towards and economic optimum. Ann Bot 91:383–390

    Article  PubMed  CAS  Google Scholar 

  • Kristensen HL, Thorup-Kristensen K (2004) Root growth and nitrate uptake of three different catch crops in deep soil layers. Soil Sci Soc Am J 68:529–537

    Article  CAS  Google Scholar 

  • Kuhlmann H, Barraclough PB (1987) Comparison between the seminal and nodal root systems of winter wheat in their activity for N and K uptake. Z Pflanz Bodenkd 150:24–30

    Article  Google Scholar 

  • Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A (1999) Molecular and functional regulation of two NO3 − uptake systems by N and C status of Arabidopsis plants. Plant J 18:509–519

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Zhao XQ, He X, Zhao GY, Li B, Liu DC, Zhang AM, Zhang XY, Tong YP, Li ZS (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytol 189:449–458

    Article  PubMed  CAS  Google Scholar 

  • Liao MT, Fillery IRP, Palta JA (2004) Early vigorous growth is a major factor influencing nitrogen uptake in wheat. Funct Plant Biol 31:121–129

    Article  CAS  Google Scholar 

  • Liao MT, Palta JA, Fillery IRP (2006) Root characteristics of vigorous wheat improve early nitrogen uptake. Aust J Agric Res 57:1097–1107

    Article  Google Scholar 

  • Lilley JM, Kirkegaard JA (2011) Benefits of increased soil exploration by wheat roots. Field Crops Res 122:118–130

    Article  Google Scholar 

  • Liu J, Liu H, Huang SM, Yang XY, Wang BR, Li XY, Ma YB (2010) Nitrogen efficiency in long-term wheat-maize cropping systems under diverse field sites in China. Field Crops Res 118:145–151

    Article  Google Scholar 

  • López-Bellido RJ, Shepherd CE, Barraclough PB (2004) Predicting post-anthesis N requirements of bread wheat with a Minolta SPAD meter. Eur J Agron 20:313–320

    Article  Google Scholar 

  • López-Bellido L, López-Bellido RJ, Redondo R (2005) Nitrogen efficiency in wheat under rainfed Mediterranean conditions as affected by split nitrogen application. Field Crops Res 94:86–97

    Article  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13

    PubMed  CAS  Google Scholar 

  • Mattas KK, Uppal RS, Singh RP (2011) Effect of varieties and nitrogen management on the growth, yield and nitrogen uptake of durum wheat. Res J Agric Sci 2:376–380

    Google Scholar 

  • Mladenov N, Hristov N, Kondic-Spika A, Djuric V, Jevtic R, Mladenov V (2011) Breeding progress in grain yield of winter wheat cultivars grown at different nitrogen levels in semiarid conditions. Breeding Sci 61:260–268

    Article  CAS  Google Scholar 

  • Muñoz-Romero V, Benítez-Vega J, López-Bellido RJ, Fontán JM, López-Bellido L (2010) Effect of tillage system on the root growth of spring wheat. Plant Soil 326:97–107

    Article  Google Scholar 

  • Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I, Tillard P, Zhuo D, Glass ADM, Touraine B (2003) Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol Biol 52:689–703

    Article  PubMed  CAS  Google Scholar 

  • Olesen JE, Berntsen J, Hansen EM, Petersen BM, Petersen J (2002) Crop nitrogen demand and canopy area expansion in winter wheat during vegetative growth. Eur J Agron 16:279–294

    Article  Google Scholar 

  • Orsel M, Chopin F, Leleu O, Smith SJ, Krapp A, Daniel-Vedele F, Miller AJ (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis physiology and protein–protein interaction. Plant Physiol 142:1304–1317

    Article  PubMed  CAS  Google Scholar 

  • Palta JA, Fillery IRP, Rebetzke GJ (2007) Restricted-tillering wheat does not lead to greater investment in roots and early nitrogen uptake. Field Crops Res 104:52–59

    Article  Google Scholar 

  • Pan J, Zhu Y, Jiang D, Dai TB, Li YX, Cao WX (2006) Modeling plant nitrogen uptake and grain nitrogen accumulation in wheat. Field Crops Res 97:322–336

    Article  Google Scholar 

  • Riga A, Fisher V, Van Praag HJ (1980) Fate of fertilizer nitrogen applied to winter wheat as Na15NO3 and (15NH4)2SO4 studied in microplots through a four course rotation: influence of fertilizer splitting on soil and fertilizer nitrogen. Soil Sci 130:88–99

    Article  CAS  Google Scholar 

  • Sadras VO, Rodriguez D (2010) Modelling the nitrogen-driven trade-off between nitrogen utilisation efficiency and water use efficiency of wheat in eastern Australia. Field Crops Res 118:297–305

    Article  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  PubMed  CAS  Google Scholar 

  • Salvagiotti F, Castellarín JM, Miralles DJ, Pedrol HM (2009) Sulfur fertilization improves nitrogen use efficiency in wheat by increasing nitrogen uptake. Field Crops Res 113:170–177

    Article  Google Scholar 

  • Shah SA, Shah SM, Mohammad W, Shafi M, Nawaz H (2009) N uptake and yield of wheat as influenced by integrated use of organic and mineral nitrogen. Int J Plant Prod 3:45–56

    CAS  Google Scholar 

  • Sharma BD, Kar S, Cheema SS (1990) Yield, water use and nitrogen uptake for different water and N levels in winter wheat. Fertil Res 22:119–127

    Article  Google Scholar 

  • Singh VP, Arora A (2001) Intraspecific variation in nitrogen uptake and nitrogen utilization efficiency in wheat (Triticum aestivum L.). J Agron Crop Sci 186:239–244

    Article  Google Scholar 

  • Smith CJ, Whitfield DM (1990) Nitrogen accumulation and redistribution of late applications of l5N labelled fertilizer by wheat. Field Crops Res 24:211–226

    Article  Google Scholar 

  • Sorgonà A, Cacco G (2002) Linking the physiological parameters of nitrate uptake with root morphology and topology in wheat (Triticum durum) and citrus (Citrus volkameriana) rootstock. Can J Bot 80:494–503

    Article  Google Scholar 

  • Sorgonà A, Lupini A, Mercati F, Di Dio L, Sunseri F, Abenavoli MR (2011) Nitrate uptake along the maize primary root: an integrated physiological and molecular approach. Plant Cell Environ 34:1127–1140

    Article  PubMed  Google Scholar 

  • Sticksel E, Maidl FX, Retzer F, Fischbeck G (1999) Nitrogen uptake and utilization in winter wheat under different fertilization regimes, with particular reference to main stems and tillers. J Agron Crop Sci 183:47–52

    Article  CAS  Google Scholar 

  • Suprayogi Y, Clarke JM, Bueckert R, Clarke FR, Pozniak CJ (2011) Nitrogen remobilization and post-anthesis nitrogen uptake in relation to elevated grain protein concentration in durum wheat. Can J Plant Sci 91:273–282

    Article  CAS  Google Scholar 

  • Tottman DR (1987) The decimal code for the growth stages of cereals, with illustrations. Ann Appl Biol 110:441–445

    Article  Google Scholar 

  • Vidal I, Longeri L, Hétier JM (1999) Nitrogen uptake and chlorophyll meter measurements in spring wheat. Nutr Cycl Agroecosys 55:1–6

    Article  Google Scholar 

  • Wang X, Wu P, Xia M, Wu Z, Chen Q, Liu F (2002) Identification of genes enriched in rice roots of the local nitrate treatment and their expression patterns in split-root treatment. Gene 297:93–102

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Li FR, Zhao L, Zhang EH, Shi SL, Zhao WZ, Song WX, Vance MM (2010) Effects of irrigation and nitrogen application rates on nitrate nitrogen distribution and fertilizer nitrogen loss, wheat yield and nitrogen uptake on a recently reclaimed sandy farmland. Plant Soil 337:325–339

    Article  CAS  Google Scholar 

  • Wang RF, An DG, Hu CS, Li LH, Zhang YM, Jia YG, Tong YP (2011) Relationship between nitrogen uptake and use efficiency of winter wheat grown in the North China Plain. Crop Pasture Sci 62:504–514

    Article  Google Scholar 

  • Weligama C, Sale PWG, Conyers MK, Liu DL, Tang C (2010) Nitrate leaching stimulates subsurface root growth of wheat and increases rhizosphere alkalisation in a highly acidic soil. Plant Soil 328:119–132

    Article  CAS  Google Scholar 

  • Whu L, McGechan MB, Watson CA, Baddeley JA (2005) Developing existing plant root system architecture models to meet future agricultural challenges. Adv Agron 85:181–219

    Article  Google Scholar 

  • Yin LP, Li P, Wen B, Taylor D, Berry JO (2007) Characterization and expression of a high-affinity nitrate system transporter gene (TaNRT2.1) from wheat roots, and its evolutionary relationship to other NTR2 genes. Plant Sci 172:621–631

    Article  CAS  Google Scholar 

  • Zhao SP, Zhao XQ, Li SM, Shi WM (2006) Optimization and application of real-time PCR method for detecting the expression levels of nitrogen assimilation-related genes in rice. Russ J Plant Physiol 53:560–569

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Shandong and National Earmarked Fund for Modern Agro-industry Technology Research System (CARS-3-1-21) and the Special Fund for Agro-scientific Research on Public Causes, MOA of China (201303109-7, 201203079, 200903007-03). The authors would like to thank Dr J.P. Baresel (Plant Science, Technical University Munich, Alte Akademie 12, Freising 85354, Germany) for kindly providing the Fig. 1 source.

Author information

Authors and Affiliations

  1. Crop Research Institute, Shandong Academy of Agricultural Sciences, 202 Gongyebei Road, Jinan, 250100, China

    Lingan Kong, Fahong Wang & Jisheng Si

  2. Departamento de Ciencias y Recursos Agrícolas y Forestales, University of Córdoba, Campus de Rabanales, Edificio C-4 “Celestino Mutis”, Ctra. Madrid km 396, 14071, Córdoba, Spain

    Luis López-bellido & Jisheng Si

  3. CIPAV-Roullier Group, Poligono Arazuri-Orcoyen, C/C No. 32., 31160 Orcoyen, Navarre, Spain

    Jose Maria Garcia-mina & Jisheng Si

Authors
  1. Lingan Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fahong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis López-bellido
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jose Maria Garcia-mina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jisheng Si
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lingan Kong.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kong, L., Wang, F., López-bellido, L. et al. Agronomic improvements through the genetic and physiological regulation of nitrogen uptake in wheat (Triticum aestivum L.). Plant Biotechnol Rep 7, 129–139 (2013). https://doi.org/10.1007/s11816-013-0275-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-013-0275-2

Keywords

Search

Navigation