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Candidate genes and genome-wide association study of grain protein content and protein deviation in durum wheat

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Abstract

Main conclusion

Stable QTL for grain protein content co-migrating with nitrogen-related genes have been identified by the candidate genes and genome-wide association mapping approaches useful for marker-assisted selection.

Grain protein content (GPC) is one of the most important quality traits in wheat, defining the nutritional and end-use properties and rheological characteristics. Over the years, a number of breeding programs have been developed aimed to improving GPC, most of them having been prevented by the negative correlation with grain yield. To overcome this issue, a collection of durum wheat germplasm was evaluated for both GPC and grain protein deviation (GPD) in seven field trials. Fourteen candidate genes involved in several processes related to nitrogen metabolism were precisely located on two high-density consensus maps of common and durum wheat, and six of them were found to be highly associated with both traits. The wheat collection was genotyped using the 90 K iSelect array, and 11 stable quantitative trait loci (QTL) for GPC were detected in at least three environments and the mean across environments by the genome-wide association mapping. Interestingly, seven QTL were co-migrating with N-related candidate genes. Four QTL were found to be significantly associated to increases of GPD, indicating that selecting for GPC could not affect final grain yield per spike. The combined approaches of candidate genes and genome-wide association mapping led to a better understanding of the genetic relationships between grain storage proteins and grain yield per spike, and provided useful information for marker-assisted selection programs.

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Abbreviations

AlaAT:

Alanine aminotransferase

ASN:

Asparagine synthetase

CG:

Candidate gene

GDH:

Glutamate dehydrogenase

GOGAT:

Glutamate synthetase

GPC:

Grain protein content

GPD:

Grain protein deviation

GS:

Glutamine synthetase

GWAS:

Genome-wide association study

GY:

Grain yield

GYS:

Grain yield per spike

NIR:

Nitrite reductase

NR:

Nitrate reductase

NRT2:

Nitrate transporter

NUE:

Nitrogen use efficiency

PPDK:

Pyruvate orthophosphate dikinase

QTL:

Quantitative trait locus

References

  • Acreche MM, Slafer GA (2009) Grain weight, radiation interception and use efficiency as affected by sink-strength in Mediterranean wheats released from 1940 to 2005. Field Crops Res 110(2):98–105

    Article  Google Scholar 

  • Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119(3):507–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balyan HS, Gahlaut V, Kumar A, Jaiswal V, Dhariwal R, Tyagi S, Agarwal P, Kumari S, Gupta PK (2016) Nitrogen and phosphorus use efficiencies in wheat: physiology, phenotyping, genetics, and breeding. In: Janick J (ed) Plant breeding reviews, vol 40. Wiley, Hoboken, pp 167–234

    Chapter  Google Scholar 

  • Blanco A, Mangini G, Giancaspro A, Giove S, Colasuonno P, Simeone R, Gadaleta A (2012) Relationships between grain protein content and grain yield components through quantitative trait locus analyses in a recombinant inbred line population derived from two elite durum wheat cultivars. Mol Breed 30(1):79–92

    Article  CAS  Google Scholar 

  • Bogard M, Allard V, Brancourt-Hulmel M, Heumez E, Machet JM, Jeuffroy MH et al (2010) Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. J Exp Bot 61:4303–4312

    Article  CAS  PubMed  Google Scholar 

  • Bordes J, Ravel C, Jaubertie JP, Duperrier B, Gardet O, Heumez E, Balfourier F (2013) Genomic regions associated with the nitrogen limitation response revealed in a global wheat core collection. Theor Appl Genet 126(3):805–822

    Article  CAS  PubMed  Google Scholar 

  • Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder M, Weber W (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105(6–7):921–936

    Article  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46(3):1323–1330

    Article  Google Scholar 

  • Brevis JC, Dubcovsky J (2010) Effects of the chromosome region including the grain protein content locus Gpc-B1 on wheat grain and protein yield. Crop Sci 50:93–104

    Article  CAS  Google Scholar 

  • Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435

    Article  CAS  PubMed  Google Scholar 

  • Clarke JM, McCaig TN, DePauw RM, Knox RE, Clarke FR, Fernandez MR, Ames NP (2005) Strongfield durum wheat. Can J Plant Sci 85:651–654

    Article  Google Scholar 

  • Colasuonno P, Lozito ML, Marcotuli I, Nigro D, Giancaspro A, Mangini G et al (2017) The carotenoid biosynthetic and catabolic genes in wheat and their association with yellow pigments. BMC Genomics 18:122. https://doi.org/10.1186/s12864-016-3395-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147(2):469–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curci PL, Bergès H, Marande W, Maccaferri M, Tuberosa R, Sonnante G (2018) Asparagine synthetase genes (AsnS1 and AsnS2) in durum wheat: structural analysis and expression under nitrogen stress. Euphytica 214(2):36. https://doi.org/10.1007/s10681-017-2105-z

    Article  CAS  Google Scholar 

  • Cuthbert JL, Somers DJ, Brûlé-Babel AL, Brown PD, Crow GH (2008) Molecular mapping of quantitative trait loci for yield and yield components in spring wheat (Triticum aestivum L.). Theor Appl Genet 117:595–608

    Article  CAS  PubMed  Google Scholar 

  • Donnelly P (2008) Progress and challenges in genome-wide association studies in humans. Nature 456:728–731

    Article  CAS  PubMed  Google Scholar 

  • Gadaleta A, Nigro D, Giancaspro A, Blanco A (2011) The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct Integr Genomics 11:665–670

    Article  CAS  PubMed  Google Scholar 

  • Gadaleta A, Nigro D, Marcotuli I, Giancaspro A, Giove SL, Blanco A (2014) Isolation and characterization of cytosolic glutamine synthetase (GSe) genes and association with grain protein content in durum wheat. Crop Pasture Sci 65:38–45

    Article  CAS  Google Scholar 

  • Gao R, Curtis TY, Powers SJ, Xu H, Huang J, Halford NG (2016) Food safety: structure and expression of the asparagine synthetase gene family of wheat. J Cereal Sci 68:122–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Giancaspro A, Giove SL, Zito D, Blanco A, Gadaleta A (2016) Mapping QTLs for Fusarium head blight resistance in an interspecific wheat population. Front Plant Sci 7:1381. https://doi.org/10.3389/fpls.2016.01381

    Article  PubMed  PubMed Central  Google Scholar 

  • Good AG, Johnson SJ, De Pauw M, Carroll RT, Savidov N, Vidmar J, Stroeher V (2007) Engineering nitrogen use efficiency with alanine aminotransferase. Botany 85(3):252–262

    CAS  Google Scholar 

  • Groos C, Robert N, Bervas E, Charmet G (2003) Genetic analysis of grain protein content, grain yield and thousand-kernel weight in bread wheat. Theor Appl Genet 106:1032–1040

    Article  CAS  PubMed  Google Scholar 

  • Gu R, Duan F, An X, Zhang F, von Wiren N, Yuan L (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515–1524

    Article  CAS  PubMed  Google Scholar 

  • Gupta PK, Kulwal PL, Jaiswal V (2014) Association mapping in crop plants: opportunities and challenges. Adv Genet 85:109–147

    Article  CAS  PubMed  Google Scholar 

  • Habash DZ, Bernard S, Schondelmaier J, Weyen J, Quarrie SA (2007) The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theor Appl Genet 114:403–419

    Article  CAS  PubMed  Google Scholar 

  • Hu M, Zhao X, Liu Q, Hong X, Zhang W, Zhang Y, Tong Y (2018) Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol J 16(11):1858–1867

    Article  CAS  PubMed  PubMed Central  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 

  • Kotur Z, Mackenzie N, Ramesh S, Tyerman SD, Kaiser BN, Glass AD (2012) Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol 194(3):724–731

    Article  CAS  PubMed  Google Scholar 

  • Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122

    Article  CAS  PubMed  Google Scholar 

  • Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Daniel-Vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation pattern towards N starvation. Plant Physiol 157(3):1255–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Jain S, Elias EM, Ibrahim M, Sharma LK (2018) An overview of QTL identification and marker-assisted selection for grain protein content in wheat. In: Sengar RS, Singh A (eds) Eco-friendly agro-biological techniques for enhancing crop productivity. Springer, Singapore, pp 245–274

    Chapter  Google Scholar 

  • Laidò G, Marone D, Russo MA, Colecchia SA, Mastrangelo AM, De Vita P et al (2014) Linkage disequilibrium and genome-wide association mapping in tetraploid wheat (Triticum turgidum L.). PLoS One 9(4):e95211. https://doi.org/10.1371/journal.pone.0095211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lea PJ, Azevedo RA (2007) Nitrogen use efficiency. 2. Amino acid metabolism. Ann Appl Biol 15(3):269–275

    Article  CAS  Google Scholar 

  • Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2. 1: AtNRT2. 2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143(1):425–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipka AE, Gore MA, Magallanes-Lundback M, Mesberg A, Lin H, Tiede T, DellaPenna D (2013) Genome-wide association study and pathway level analysis of tocochromanol levels in maize grain. G3-Genes Genom Genet 3(8):1287–1299

    Google Scholar 

  • Lu Y, Luo F, Yang M, Li X, Lian X (2011) Suppression of glutamate synthase genes significantly affects carbon and nitrogen metabolism in rice (Oryza sativa L.). Sci China Life Sci 54:651–663

    Article  CAS  PubMed  Google Scholar 

  • Maccaferri M, Cane MA, Sanguineti MC, Salvi S, Colalongo MC, Massi A, Fahima T (2014) A consensus framework map of durum wheat (Triticum durum Desf.) suitable for linkage disequilibrium analysis and genome-wide association mapping. BMC Genomics 15(1):873. https://doi.org/10.1186/1471-2164-15-873

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahjourimajd S, Taylor J, Rengel Z, Khabaz-Saberi H, Kuchel H, Okamoto M, Langridge P (2016) The genetic control of grain protein content under variable nitrogen supply in an Australian wheat mapping population. PLoS One 11(7):e0159371. https://doi.org/10.1371/journal.pone.0159371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mangini G, Gadaleta A, Colasuonno P, Marcotuli I, Signorile AM, Simeone R et al (2018) Genetic dissection of the relationships between grain yield components by genome-wide association mapping in a collection of tetraploid wheats. PLoS One 13(1):e0190162. https://doi.org/10.1371/journal.phone.0190162

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcotuli I, Houston K, Waugh R, Fincher GB, Burton RA, Blanco A, Gadaleta A (2015) Genome wide association mapping for arabinoxylan content in a collection of tetraploid wheats. PLoS One 10(7):e0132787. https://doi.org/10.1371/journal.pone.0132787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcotuli I, Colasuonno P, Blanco A, Gadaleta A (2018) Expression analysis of cellulose synthase-like genes in durum wheat. Sci Rep 8:15675. https://doi.org/10.1038/s41598-018-34013-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marjoram P, Zubair A, Nuzhdin SV (2014) Post-GWAS: where next? More samples, more SNPs or more biology? Heredity 112(1):79–88

    Article  CAS  PubMed  Google Scholar 

  • Monaghan JM, Snape JW, Chojecki AJS, Kettlewell PS (2001) The use of grain protein deviation for identifying wheat cultivars with high grain protein concentration and yield. Euphytica 122(2):309–317

    Article  CAS  Google Scholar 

  • Nigro D, Gu YQ, Huo N, Marcotuli I, Blanco A, Gadaleta A, Anderson OD (2013) Structural analysis of the wheat genes encoding NADH-dependent glutamine-2-oxoglutarate amidotransferases genes and correlation with grain protein content. PLoS One 8:e73751. https://doi.org/10.1371/journal.pone.0073751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nigro D, Blanco A, Anderson OD, Gadaleta A (2014) Characterization of ferredoxin-dependent glutamine-oxoglutarate amidotransferase (Fd-GOGAT) genes and their relationship with grain protein content QTL in wheat. PLoS One 9:e103869. https://doi.org/10.1371/journal.pone.0103869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nigro D, Fortunato S, Giove SL, Paradiso A, Gu YQ, Blanco A, de Pinto MC, Gadaleta A (2016) Glutamine synthetase in durum wheat: genotypic variation and relationship with grain protein content. Front Plant Sci 7:971. https://doi.org/10.3389/fpls.2016.00971

    Article  PubMed  PubMed Central  Google Scholar 

  • Nigro D, Fortunato S, Giove SL, Mangini G, Yacoubi I, Simeone R, BlancoA Gadaleta A (2017a) Allelic variants of glutamine synthetase and glutamate synthase genes in a collection of durum wheat and association with grain protein content. Diversity 9(4):52. https://doi.org/10.3390/d9040052

    Article  CAS  Google Scholar 

  • Nigro D, Laddomada B, Mita G, Blanco E, Colasuonno P, Simeone R, Gadaleta A, Pasqualone A, Blanco A (2017b) Genome-wide association mapping of phenolic acids in tetraploid wheats. J Cereal Sci 75:25–34

    Article  CAS  Google Scholar 

  • Oury FX, Berard P, Brancourt-Hulmel M, Depatureaux C, Doussignault G, Galic N, Giraud A, Heumez E, Lecompte C, Pluchard P, Rolland B, Rousset M, Trottet M (2003) Yield and grain protein concentration in bread wheat: a review and a study of multi-annual data from a French breeding program. J Genet Breed 57:59–68

    Google Scholar 

  • Quraishi UM, Abrouk M, Murat F, Pont C, Foucrier S et al (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756

    Article  CAS  PubMed  Google Scholar 

  • Quraishi UM, Pont C, Ain QU, Flores R, Burlot L, Alaux M, Salse J (2017) Combined genomic and genetic data integration of major agronomical traits in bread wheat (Triticum aestivum L.). Front Plant Sci 8:1843. https://doi.org/10.3389/fpls.2017.01843

    Article  PubMed  PubMed Central  Google Scholar 

  • Rapp M, Lein V, Lacoudre F, Lafferty J, Müller E, Vida G, Leiser WL (2018) Simultaneous improvement of grain yield and protein content in durum wheat by different phenotypic indices and genomic selection. Theor Appl Genet 131(6):1315–1329

    Article  CAS  PubMed  Google Scholar 

  • Salse J, Quraishi UM, Pont C, Murat F, Le Gouis J, Lafarge S (2013) Grain filling of a plant through the modulation of NADH-glutamate synthase. Patent Application No. 13/576,610

  • Sears RG (1998) Improving grain protein concentration and grain yield in USA hard winter wheat. In: Fowler DB, Geddes WE, Johnston AM, Preston KR (eds) Wheat protein production and marketing. In: Proceedings of Wheat Symposium, Saskatoon, Printcrafters Inc., Winnipeg, Canada, pp 63–67

  • Sharp PJ, Kreis M, Shewry PR, Gale MD (1988) Location of β-amylase sequences in wheat and its relatives. Theor Appl Genet 75:286–290

    Article  CAS  Google Scholar 

  • Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732

    Article  CAS  PubMed  Google Scholar 

  • Simmonds NW (1995) The relation between yield and protein in cereal grain. J Sci Food Agric 67:309–315

    Article  CAS  Google Scholar 

  • Simons M, Saha R, Guillard L, Clément G, Armengaud P, Cañas R, Maranas CD, Lea PJ, Hirel B (2014) Nitrogen use efficiency in maize (Zea mays L.): from omics studies to metabolic modelling. J Exp Bot 65:5657–5671

    Article  CAS  PubMed  Google Scholar 

  • Suprayogi Y, Pozniak CJ, Clarke FR, Clarke JM, Knox RE, Singh AK (2009) Identification and validation of quantitative trait loci for grain protein concentration in adapted Canadian durum wheat populations. Theor Appl Genet 119(3):437–448

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi M, Abiko T, Yamaya T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice. J Exp Bot 58:2319–2327

    Article  CAS  PubMed  Google Scholar 

  • Taulemesse F, Le Gouis J, Gouache D, Gibon Y, Allard V (2015) Post-flowering nitrate uptake in wheat is controlled by N status at flowering, with a putative major role of root nitrate transporter NRT2.1. PLoS One 10(3):e0120291. https://doi.org/10.1371/journal.pone.0120291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor L, Nunes-Nesi A, Parsley K, Leiss A, Leach G, Coates S, Hibberd JM (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J 62(4):641–652

    Article  CAS  PubMed  Google Scholar 

  • Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19:656–663

    Article  CAS  PubMed  Google Scholar 

  • Thorwarth P, Piepho HP, Zhao Y, Ebmeyer E, Schacht J, Schachschneider R, Kazman E, Reif JC, Wurschum T, Friedrich C, Longin CFH (2018) Higher grain yield and higher grain protein deviation underline the potential of hybrid wheat for a sustainable agriculture. Plant Breed 137(3):326–337

    Article  CAS  Google Scholar 

  • Tian H, Fu J, Drijber RA, Gao Y (2015) Expression patterns of five genes involved in nitrogen metabolism in two winter wheat (Triticum aestivum L.) genotypes with high and low nitrogen utilization efficiencies. J Cereal Sci 61:48–54

    Article  CAS  Google Scholar 

  • Uauy C, Brevis JC, Dubcovsky J (2006) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57:2785–2794

    Article  CAS  PubMed  Google Scholar 

  • Wang LIN, Cui FA, Wang J, Jun LI, Ding A, Zhao C, Wang H (2012) Conditional QTL mapping of protein content in wheat with respect to grain yield and its components. Thai J Genet 91(3):303–312

    Article  Google Scholar 

  • Wang SW, Forrest D, Allen K, Chao A, Huang SBE, Maccaferri M et al (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12(6):787–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weng J, Xie C, Hao Z, Wang J, Liu C, Li M, Li X (2011) Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS One 6(12):e29229. https://doi.org/10.1371/journal.pone.0029229

    Article  CAS  PubMed  PubMed Central  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 

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

    Article  CAS  PubMed  Google Scholar 

  • Zanetti S, Winzeler M, Feuillet C, Keller B, Messmer M (2001) Genetic analysis of bread–making quality in wheat and spelt. Plant Breed 120:13–19

    Article  CAS  Google Scholar 

  • Zeng DD, Qin R, Li M et al (2017) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Mol Genet Genomics 292(2):385–395

    Article  CAS  PubMed  Google Scholar 

  • Zhao XQ, Nie XL, Xiao XG (2013) Over-expression of a tobacco nitrate reductase gene in wheat (Triticum aestivum L.) increases seed protein content and weight without augmenting nitrogen supplying. PloS One 8(9):74678. https://doi.org/10.1371/journal.pone.0074678

    Article  CAS  Google Scholar 

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Acknowledgements

The research project was supported by grants from Ministero dell’Istruzione, dell’Università e della Ricerca, project ‘ISCOCEM’, and from Regione Puglia “Programma regionale a sostegno della specializzazione intelligente e della sostenibilità sociale ed ambientale-FutureInResearch”.

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Nigro, D., Gadaleta, A., Mangini, G. et al. Candidate genes and genome-wide association study of grain protein content and protein deviation in durum wheat. Planta 249, 1157–1175 (2019). https://doi.org/10.1007/s00425-018-03075-1

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