Skip to main content
SpringerLink
Log in

A QTL with major effect on reducing leaf rust severity on the short arm of chromosome 1A of wheat detected across different genetic backgrounds and diverse environments

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

Abstract

Key message

Selection for QLr.cau - 1AS (a major QTL detected in wheat for reducing leaf rust severity) based on the DNA marker gpw2246 was as effective as selection for Lr34 based on cssfr5.

Abstract

Leaf rust is an important disease of wheat worldwide. Utilization of slow-rusting resistance constitutes a strategy to sustainably control this disease. The American wheat cultivar Luke exhibits slow leaf-rusting resistance at the adult plant stage. The objectives of this study were to detect and validate QTL for the resistance in Luke. Three winter wheat populations were used, namely, 149 recombinant inbred lines (RILs) derived from the cross Luke × Aquileja, 307 RILs from Luke × AQ24788-83, and 80 F2:3 families selected from Lingxing66 × KA298. Aquileja and Lingxing66 are highly susceptible to leaf rust. AQ24788-83 shows high (susceptible) infection type but contains the slow-rusting gene Lr34 as diagnosed by the gene-specific marker cssfr5. KA298, an F9 RIL selected from Luke × AQ24788-83, contains Lr34 and QLr.cau-1AS (a major QTL originated from Luke, this study). These wheats were evaluated for leaf rust in 12 field and greenhouse environments involving four locations and five seasons. Genotyping was done using simple sequence repeat (SSR) and diversity arrays technology markers. Of the detected QTLs, QLr.cau-1AS was significant consistently across all the genetic backgrounds, test environments, and likely a wide range of pathogen races. QLr.cau-1AS explained 22.3–55.2 % of leaf rust phenotypic variation, being comparable to Lr34 in effect size. A co-dominant SSR marker (gpw2246, http://wheat.pw.usda.gov/GG2/index.shtml) was identified to be tightly linked to QLr.cau-1AS. Selection based on gpw2246 for QLr.cau-1AS was as effective as the selection based on cssfr5 for Lr34. QLr.cau-1AS will be helpful for increasing the genetic diversity of slow leaf-rusting resistance in wheat breeding programs.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akbari M, Wenzl P, Caig V, Carling J, Xia L, Yang S, Uszynski G, Mohler V, Lehmensiek A, Kuchel H, Hayden MJ, Howes N, Sharp PJ, Vaughan P, Rathmell B, Huttner E, Kilian A (2006) Diversity array technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420

    Article  CAS  PubMed  Google Scholar 

  • Bassam BJ, Caetano-Anolles G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83

    Article  CAS  PubMed  Google Scholar 

  • Bjarko ME, Line RF (1988) Quantitative determination of the gene action of leaf rust resistance in four cultivars of wheat, Triticum aestivum. Phytopathology 78:451–456

    Article  Google Scholar 

  • Bolton M, Kolmer J, Garvin D (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575

    Article  PubMed  Google Scholar 

  • Buerstmayr M, Matiasch L, Mascher F, Vida G, Ittu M, Robert O, Holdgate S, Flath K, Neumayer A, Buerstmayr H (2014) Mapping of quantitative adult plant field resistance to leaf rust and stripe rust in two European winter wheat populations reveals co-location of three QTL conferring resistance to both rust pathogens. Theor Appl Genet 127:2011–2028

    Article  PubMed Central  PubMed  Google Scholar 

  • Caldwell RM (1968) Breeding for general and/or specific plant disease resistance. In: Findlay KW, Shepherd KW (eds) Proc 3th Int Wheat Genetics Symp. Australian Academy of Science, Canberra, pp 263–272

    Google Scholar 

  • Caldwell RM, Schafer JF, Compton LE, Patterson FL (1957) A mature plant type of wheat leaf-rust resistance of composite origin. Phytopathology 47:691–692

    Google Scholar 

  • Chen WQ, Yan SB, Hu CC, Xie SX (1994) Physiological race and pathogenicity of Puccinia recondita f. sp. tritici in China during the period from 1990 to 1993. (In Chinese with English abstract). Acta Phytophylacica Sinica 21:289–294

    Google Scholar 

  • Chen J, Li GH, Du ZY, Quan W, Zhang HY, Che MZ, Wang Z, Zhong ZJ (2013) Mapping of QTL conferring resistance to sharp eyespot (Rhizoctonia cerealis) in bread wheat at the adult plant growth stage. Theor Appl Genet 126:2865–2878

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Bryan GJ, Collins AJ, Stephenson P, Gale MD (1995) Application of two microsatellite sequences in wheat storage proteins as molecular markers. Theor Appl Genet 90:247–252

    Article  CAS  PubMed  Google Scholar 

  • Dubin HJ, Torres E (1981) Causes and consequences of the 1976–1977 wheat leaf rust epidemic in Northwest Mexico. Annu Rev Phytopathol 19:41–49

    Article  Google Scholar 

  • Dyck PL, Samborski DJ (1982) The inheritance of resistance to Puccinia recondita in a group of common wheat cultivars. Can J Genet Cytol 24:273–283

    Article  Google Scholar 

  • Feuillet C, Schachermayr G, Keller B (1997) Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J 11:45–52

    Article  CAS  PubMed  Google Scholar 

  • Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B (2003) Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci USA 100:15253–15258

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Guo Q, Zhang ZJ, Xu YB, Li GH, Feng J, Zhou Y (2008) Quantitative trait loci for high-temperature adult-plant and slow-rusting resistance to Puccinia striiformis f. sp. tritici in wheat cultivars. Phytopathology 98:803–809

    Article  CAS  PubMed  Google Scholar 

  • Heath M (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Foessel SA, Lagudah ES, Huerta-Espino J, Hayden MJ, Bariana HS, Singh D, Singh RP (2011) New slow-rusting leaf rust and stripe rust resistance genes Lr67 and Yr46 in wheat are pleiotropic or closely linked. Theor Appl Genet 122:239–249

    Article  PubMed  Google Scholar 

  • Herrera-Foessel SA, Singh RP, Huerta-Espino J, Rosewarne GM, Periyannan SK, Viccars L, Calvo-Salazar V, Lan CX, Lagudah ES (2012) Lr68: a new gene conferring slow rusting resistance to leaf rust in wheat. Theor Appl Genet 124:1475–1486

    Article  CAS  PubMed  Google Scholar 

  • Hiebert CW, Thomas JB, McCallum BD, Humphreys DG, DePauw RM, Hayden MJ, Mago R, Schnippenkoetter W, Spielmeyer W (2010) An introgression on wheat chromosome 4DL in RL6077 (Thatcher × 6/PI 250413) confers adult plant resistance to stripe rust and leaf rust (Lr67). Theor Appl Genet 121:1083–1091

    Article  PubMed  Google Scholar 

  • Huang J, Zhao Z, Song F, Wang X, Xu H, Huang Y, An D, Li H (2012) Molecular detection of a gene effective against powdery mildew in the wheat cultivar Liangxing 66. Mol Breed 30:1737–1745

    Article  CAS  Google Scholar 

  • Ingala L, López M, Darino M, Pergolesi MF, Diéguez MJ, Sacco F (2012) Genetic analysis of leaf rust resistance genes and associated markers in the durable resistant wheat cultivar Sinvalocho MA. Theor Appl Genet 124:1305–1314

    Article  CAS  PubMed  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–473

    Article  CAS  PubMed  Google Scholar 

  • Khan M, Bukhari A, Dar Z, Rizvi S (2013) Status and strategies in breeding for rust resistance in wheat. Agric Sci 4:292–301

    Google Scholar 

  • Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34:435–455

    Article  CAS  PubMed  Google Scholar 

  • Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opin Plant Biol 8:441–449

    Article  PubMed  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Lagudah ES, Krattinger SG, Herrera-Foessel S, Singh RP, Huerta-Espino J, Spielmeyer W, Brown-Guedira G, Selter LL, Keller B (2009) Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor Appl Gent 119:889–898

    Article  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer pack-age for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Li ZF, Xia XC, He ZH, Li X, Zhang LJ, Wang HY, Meng QF, Yang WX, Li GQ, Liu DQ (2010) Seedling and slow rusting resistance to leaf rust in Chinese wheat cultivars. Plant Dis 94:45–53

    Article  CAS  Google Scholar 

  • Li ZF, Lan CX, He ZH, Singh RP, Rosewarne GM, Chen XM, Xia XC (2014) Overview and application of QTL for adult plant resistance to leaf rust and powdery mildew in wheat. Crop Sci 54:1907–1925

    Article  Google Scholar 

  • Line RF (2002) Stripe rust of wheat and barley in North America: a retrospective historical review. Annu Rev Phytopathol 2002(40):75–118

    Article  Google Scholar 

  • Long DL, Kolmer JA (1989) A North American system of nomenclature for Puccinia recondita f. sp. tritici. Phytopathology 79:525–529

    Article  Google Scholar 

  • Maccaferri M, Mantovani P, Tuberosa R, DeAmbrogio E, Giuliani S, Demontis A, Massi A, Sanguineti MC (2008) A major QTL for durable leaf rust resistance widely exploited in durum wheat breeding programs maps on the distal region of chromosome arm 7BL. Theor Appl Genet 117:1225–1240

    Article  CAS  PubMed  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    Article  CAS  PubMed  Google Scholar 

  • McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers WJ, Morris C, Appels R, Xia XC (2013) Catalogue of gene symbols for wheat: 2013 supplement. www.shigen.nig.ac.jp/wheat/komugi/genes/macgene/2013/GeneCatalogueIntroduction.pdf. Accessed 30 June 2014

  • Messmer MM, Seyfarth R, Keller M, Schachermayr G, Winzeler M, Zanetti S, Feuillet C, Keller B (2000) Genetic analysis of durable leaf rust resistance in winter wheat. Theor Appl Genet 100:419–431

    Article  CAS  Google Scholar 

  • Michelmore RW, Christopoulou M, Caldwell KS (2013) Impacts of resistance gene genetics, function, and evolution on a durable future. Annu Rev Phytopathol 51:291–319

    Article  CAS  PubMed  Google Scholar 

  • Milus EA, Line RF (1980a) Virulence of Puccinia recondita in the pacific Northwest. Plant Dis 64:78–80

    Article  Google Scholar 

  • Milus EA, Line RF (1980b) Characterization of resistance to leaf rust in Pacific Northwest wheats. Phytopathology 70:167–172

    Article  Google Scholar 

  • Milus EA, Line RF (1986) Number of genes controlling high temperature, adult-plant resistance to stripe rust in wheat. Phytopathology 76:93–96

    Article  Google Scholar 

  • Ohm HW, Shaner GE (1976) Three components of slow leaf-rusting at different growth stages in wheat. Phytopathology 66:1356–1360

    Article  Google Scholar 

  • Paillard S, Schnurbusch T, Winzeler M, Messmer M, Sourdille P, Abderhalden O, Keller B, Schachermayr G (2003) An integrative genetic linkage map of winter wheat (Triticum aestivum L.). Theor Appl Genet 107:1235–1242

    Article  CAS  PubMed  Google Scholar 

  • Park RF, McIntosh RA (1994) Adult plant resistances to Puccinia recondita f. sp. tritici in wheat. N Z J Crop Hortic Sci 22:151–158

    Article  Google Scholar 

  • Park RF, Mohler V, Nazari K, Singh D (2014) Characterization and mapping of gene Lr73 conferring seedling resistance to Puccinia triticina in common wheat. Theor Appl Genet 127:2041–2049

    Article  CAS  PubMed  Google Scholar 

  • Peterson RF, Campbell AB, Hannah AE (1948) A diagrammatic scale for estimating rust intensity of leaves and stems of cereals. Can J Res 26:496–500

    Article  Google Scholar 

  • Qayoum A, Line RF (1985) High-temperature, adult plant resistance to stripe rust of wheat. Phytopathology 75:121–1125

    Article  Google Scholar 

  • Quan W, Hou GL, Chen J, Du ZY, Lin F, Guo Y, Liu S, Zhang ZJ (2013) Mapping of QTL lengthening the latent period of Puccinia striiformis in winter wheat at the tillering growth stage. Eur J Plant Pathol 136:715–727

    Article  CAS  Google Scholar 

  • Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B (2012) Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnol J 10:477–487

    Article  CAS  PubMed  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal M (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed Central  PubMed  Google Scholar 

  • Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat: Concepts and methods of disease management. CIMMYT, Mexico

    Google Scholar 

  • Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5:69–76

    Article  CAS  PubMed  Google Scholar 

  • Schachermayr G, Feuillet C, Keller B (1997) Molecular markers for the detection of the wheat leaf rust resistance gene Lr10 in diverse genetic backgrounds. Mol Breed 3:65–74

    Article  CAS  Google Scholar 

  • Schnurbusch T, Paillard S, Schori A, Messmer M, Schachermayr G, Winzeler M, Keller B (2004) Dissection of quantitative and durable leaf rust resistance in Swiss winter wheat reveals a major resistance QTL in the Lr34 chromosomal region. Theor Appl Genet 108:477–484

    Article  CAS  PubMed  Google Scholar 

  • Singh RP (1992) Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathology 82:835–838

    Article  Google Scholar 

  • Singh RP, Gupta AK (1992) Expression of wheat leaf rust resistance gene Lr34 in seedlings and adult plants. Plant Dis 76:489–491

    Article  Google Scholar 

  • Singh RP, Mujeeb-Kazi A, Huerta-Espino J (1998) Lr46: a gene conferring slow-rusting resistance to leaf rust in wheat. Phytopathology 88:890–894

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Chen WQ, He ZH (1999) Leaf rust resistance of spring, facultative, and winter wheat cultivars from China. Plant Dis 83:644–651

    Article  Google Scholar 

  • Singh D, Simmonds J, Park RF, Bariana HS, Snape JW (2009) Inheritance and QTL mapping of leaf rust resistance in the European winter wheat cultivar ‘Beaver’. Euphytica 169:253–261

    Article  Google Scholar 

  • Singh A, Knox RE, DePauw RM, Singh AK, Cuthbert RD, Campbell HL, Shorter S, Bhavani S (2014) Stripe rust and leaf rust resistance QTL mapping, epistatic interactions, and co-localization with stem rust resistance loci in spring wheat evaluated over three continents. Theor Appl Genet 127:2465–2477

    Article  CAS  PubMed  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  CAS  PubMed  Google Scholar 

  • Sourdille P, Singh S, Cadalen T, Brown-Guedira GL, Gay G, Qi L, Gill BS, Dufour P, Murigneux A, Bernard M (2004) Microsatellite-based deletion bin system for the establishment of genetic-physical map relationships in wheat (Triticum aestivum L.). Funct Integr Genomics 4:12–25

    Article  CAS  PubMed  Google Scholar 

  • Spielmeyer W, McIntosh RA, Kolmer J, Lagudah ES (2005) Powdery mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust cosegregate at a locus on the short arm of chromosome 7D of wheat. Theor Appl Genet 111:731–735

    Article  CAS  PubMed  Google Scholar 

  • Suenaga K, Singh RP, Huerta-Espino J, William HM (2003) Microsatellite markers for genes Lr34/Yr18 and other quantitative trait loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology 93:881–890

    Article  CAS  PubMed  Google Scholar 

  • Tsilo TJ, Kolmer JA, Anderson JA (2014) Molecular mapping and improvement of leaf rust resistance in wheat breeding lines. Phytopathology 104:865–870

    PubMed  Google Scholar 

  • Van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017

    Article  PubMed Central  PubMed  Google Scholar 

  • Wan JJ, Meng QF, Yang WX, Wen XL, Liu DQ (2010) Study on virulence of Puccininia triticina on wheat in Shandong province. (In Chinese with English abstract). J Anhui Agri Sci 38:16929–16930

    Google Scholar 

  • Wang S, Basten JC, Zeng ZB (2010) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm. Accessed 27 Dec 2014

  • Wenzl P, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • William HM, Hoisington D, Singh RP, Gonzalez-de-Leon D (1997) Detection of quantitative trait loci associated with leaf rust resistance in bread wheat. Genome 40:253–260

    Article  CAS  PubMed  Google Scholar 

  • William HM, Singh RP, Huerta-Espino J, Palacios G, Suenaga K (2006) Characterization of genetic loci conferring adult plant resistance to leaf rust and stripe rust in spring wheat. Genome 49:977–990

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Bai G, Carver BF, Shaner GE, Hunger RM (2005) Molecular characterization of slow leaf-rusting resistance in wheat. Crop Sci 45:758–765

    Article  CAS  Google Scholar 

  • Zhang ZJ (1995) Evidence of durable resistance in nine Chinese landraces and one Italian cultivar of Triticum aestivum to Puccinia striiformis. Eur J Plant Pathol 101:405–409

    Article  Google Scholar 

  • Zhou HX, Xia XC, He ZH, Li X, Wang CF, Li ZF, Liu DQ (2013) Molecular mapping of leaf rust resistance gene LrNJ97 in Chinese wheat line Neijiang 977671. Theor Appl Genet 126:2141–2147

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Ren Y, Lillemo M, Yao ZJ, Zhang PP, Xia XC, He ZH, Li ZF, Liu DQ (2014) QTL mapping of adult-plant resistance to leaf rust in a RIL population derived from a cross of wheat cultivars Shanghai 3/Catbird and Naxos. Theor Appl Genet 127:1873–1883

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully thank Professors W. Q. Chen and W. X. Yang for their supports with the purification of P. triticina race and some wheat lines. This study was supported by the National Natural Science Foundation of China (30871612), the National Basic Research Program of China (2013CB127700), and the Special Fund for Agro-scientific Research in the Public Interest (201203014).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This research complies with the current laws of P. R. China.

Author information

Author notes

  1. Ziyi Du

    Present address: Plant Protection Institute, Inner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot, 010031, People’s Republic of China

Authors and Affiliations

  1. Department of Plant Pathology, China Agricultural University, Beijing, 100193, People’s Republic of China

    Ziyi Du, Mingzhe Che, Jiang Chen, Yan Guo, Zhen Wang, Junda Ren, Huyan Zhang & Zhongjun Zhang

  2. Department of Mathematics, China Agricultural University, Beijing, 100083, People’s Republic of China

    Guohui Li

  3. Center for Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, People’s Republic of China

    Wei Quan

Authors
  1. Ziyi Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mingzhe Che
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guohui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei Quan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yan Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junda Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huyan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhongjun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongjun Zhang.

Additional information

Communicated by T. Miedaner.

M. Che and G. Li contributed equally to this paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 37 kb)

Supplementary material 2 (DOC 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Du, Z., Che, M., Li, G. et al. A QTL with major effect on reducing leaf rust severity on the short arm of chromosome 1A of wheat detected across different genetic backgrounds and diverse environments. Theor Appl Genet 128, 1579–1594 (2015). https://doi.org/10.1007/s00122-015-2533-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-015-2533-x

Keywords

Search

Navigation