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Copy number variation of chromosome 5A and its association with Q gene expression, morphological aberrations, and agronomic performance of winter wheat cultivars

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Our investigations combine chromosome 5A copy number variation associated with relative 5A Q gene expression and morphological and agronomic data to characterize the occurrence of speltoid plants in winter wheat cultivars.

Abstract

The occurrence of speltoid aberrants in wheat breeding is a serious problem that may result in rejection of a candidate cultivar during licensing. The spear-shaped, hard threshing spike is caused by copy number reduction of the domestication gene Q, located on the long arm of wheat chromosome 5A. As a member of the APETALA2-like transcription factor family, the 5AQ gene is involved in flower development and pleiotropically controls other agronomic traits. In this report, a characterization of instability of chromosome 5A is given and effects due to the loss of the Q gene and other genes are discussed. Based on pyrosequencing, we correctly predicted the 5AQ copy number for 392 of 402 tested offspring plants (97.5 %) originating from single speltoid plants of eleven wheat cultivars. The findings indicate that the resulting speltoid plants were either reduced in chromosome 5A copy number or possessed a partial deletion of the distal end of chromosome arm 5AL. 5AQ specific real-time PCR analysis revealed varying transcription levels among cultivars. During early spike development, the relative transcription of the 5AQ gene was always lower in speltoids than in normal square headed wheat plants, most likely leading to the occurrence of the characteristic speltoid spike phenotype. The parallel analysis of 18 agronomic traits revealed pleiotropic effects governed by genes located on 5A. Our results demonstrate that through pyrosequencing one can identify aneuploidy or deletions within chromosome 5A to select against the occurrence of speltoid plants in wheat seedlings.

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References

  • Asakura N, Mori N, Nakamura C, Ohtsuka I (2009) Genotyping of the Q locus in wheat by a simple PCR-RFLP method. Gen Genet Sys 84:233–237

    Article  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Bayliss MW, Riley R (1972) Analysis of temperature-dependent asynapsis in Triticum aestivum. Genet Res 20:193–200

    Article  Google Scholar 

  • Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186:54–62

    Article  PubMed  CAS  Google Scholar 

  • Carrera J, Rodrigo G, Jaramillo A, Elena SF (2009) Reverse-engineering the Arabidopsis thaliana transcriptional network under changing environmental conditions. Gen Biol 10:R96

    Article  Google Scholar 

  • Chen XM (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581–585

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  PubMed  CAS  Google Scholar 

  • Díaz A, Zikhali M, Turner AS, Isaac P, Laurie DA (2012) Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS One 7(3):e33234

    Article  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.4, Available from http://www.geneious.com/

  • Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307

    Article  CAS  Google Scholar 

  • EU CPVO. European Union (2008) Protocol for distinctness, uniformity and stability tests, Triticum aestivum L.: wheat. EU Community Plant Variety Office, p 40

    Google Scholar 

  • Faris JD, Gill BS (2002) Genomic targeting and high-resolution mapping of the domestication gene Q in wheat. Genome 45:706–718

    Article  PubMed  CAS  Google Scholar 

  • Förster S, Schumann E, Weber WE, Pillen K (2012) Discrimination of alleles and copy numbers at the Q locus in hexaploid wheat using quantitative pyrosequencing. Euphytica 186:207–218

    Article  Google Scholar 

  • Friebe B, Zhang P, Linc G, Gill BS (2005) Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogene Gen Res 109:293–297

    Article  CAS  Google Scholar 

  • Gil-Humanes J, Piston F, Martin A, Barro F (2009) Comparative genomic analysis and expression of the APETALA2-like genes from barley, wheat, and barley-wheat amphiploids. BMC Plant Biol 9:66

    Article  PubMed  Google Scholar 

  • Greer E, Martin AC, Pendle A, Colas I, Jones AME, Moore G, Shaw P (2012) The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24:152–162

    Article  PubMed  CAS  Google Scholar 

  • Hanemann A, Schweizer GF, Cossu R, Wicker T, Röder MS (2009) Fine mapping, physical mapping and development of diagnostic markers for the Rrs2 scald resistance gene in barley. Theor Appl Genet 119:1507–1522

    Article  PubMed  CAS  Google Scholar 

  • Huskins CL (1946) Fatuoid, speltoid and related mutations of oats and wheat. Bot Rev 12:457–514

    Article  Google Scholar 

  • Jantasuriyarat C, Vales MI, Watson CJW, Riera-Lizarazu O (2004) Identification and mapping of genetic loci affecting the free-threshing habit and spike compactness in wheat (Triticum aestivum L.). Theor Appl Genet 108:261–273

    Article  PubMed  CAS  Google Scholar 

  • Jofuku KD, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225

    PubMed  CAS  Google Scholar 

  • Kato K, Miura H, Sawada S (1999) QTL mapping of genes controlling ear emergence time and plant height on chromosome 5A of wheat. Theor Appl Genet 98:472–477

    Article  CAS  Google Scholar 

  • Kato K, Miura H, Sawada S (2000) Mapping QTLs controlling grain yield and its components on chromosome 5A of wheat. Theor Appl Genet 101:1114–1121

    Article  CAS  Google Scholar 

  • Kato K, Sonokawa R, Miura H, Sawada S (2003) Dwarfing effect associated with the threshability gene Q on wheat chromosome 5A. Plant Breed 122:489–492

    Article  CAS  Google Scholar 

  • Kerber ER, Dyck PL (1969) Inheritance in hexaploid wheat of leaf rust resistance and other characters derived from Aegilops squarrosa. Can J Genet Cytol 11:639–647

    Google Scholar 

  • Kerber ER, Rowland GG (1974) Origin of free threshing character in hexaploid wheat. Can J Genet Cytol 16:145–154

    Google Scholar 

  • MacKey J (1954) Neutron and X-ray experiments in wheat and a revision of the speltoid problem. Hereditas 40:65–180

    Google Scholar 

  • Matthies IE, Sharma S, Weise S, Röder MS (2012) Sequence variation in the barley genes encoding sucrose synthase I and sucrose phosphate synthase II, and its association with variation in grain traits and malting quality. Euphytica 184:73–83

    Article  CAS  Google Scholar 

  • Mestiri I, Chagué V, Tanguy AM, Huneau C, Huteau V, Belcram H, Coriton O, Chalhoub B, Jahier J (2010) Newly synthesized wheat allohexaploids display progenitor-dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol 186:86–101

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu M (1963) Dosage effect of spelta gene Q of hexaploid wheat. Genetics 48:469–482

    PubMed  CAS  Google Scholar 

  • Ning SZ, Chen QJ, Yuan ZW, Zhang LQ, Yan ZH, Zheng YL, Liu DC (2009) Characterization of WAP2 gene in Aegilops tauschii and comparison with homoeologous loci in wheat. J Sys Evol 47:543–551

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute (2008) The SAS enterprise guide for windows, release 4.2. SAS Institute, Cary

    Google Scholar 

  • Sears ER (1952) Misdivision of univalents in common wheat. Chromosoma 4:535–550

    Article  PubMed  CAS  Google Scholar 

  • Sears ER (1954) The aneuploids of common wheat. MO Agr Exp Sta Res Bull 572:1–59

    Google Scholar 

  • Simons KJ, Fellers JP, Trick HN, Zhang ZC, Tai YS, Gill BS, Faris JD (2006) Molecular characterization of the major wheat domestication gene Q. Genetics 172:547–555

    Article  PubMed  CAS  Google Scholar 

  • Singh MP (1969) Some radiation induced changes at ‘Q’ locus in bread wheat (Triticum aestivum L.). Caryologia 22:119–126

    Google Scholar 

  • Singh RJ (2003) Plant cytogenetics. CRC Press, Boca Raton

    Google Scholar 

  • Singh D, Rajlakshmy C (1994) Breeding behaviour of monosomics in hexaploid wheat. Wheat Info Serv 78:18–20

    Google Scholar 

  • Snape JW, Law CN, Parker BB, Worland AJ (1985) Genetical analysis of chromosome 5A of wheat and its influence on important agronomic characters. Theor Appl Genet 71:518–526

    Article  PubMed  CAS  Google Scholar 

  • Söderbäck E, Zackrisson AL, Lindblom B, Alderborn A (2005) Determination of CYP2D6 gene copy number by pyrosequencing. Clin Chem 51:522–531

    Article  PubMed  Google Scholar 

  • Sood S, Kuraparthy V, Bai G, Gill BS (2009) The major threshability genes soft glume (sog) and tenacious glume (Tg), of diploid and polyploid wheat, trace their origin to independent mutations at non-orthologous loci. Theor Appl Genet 119:341–351

    Article  PubMed  Google Scholar 

  • Sourdille P, Cadalen T, Gay G, Gill B, Bernard M (2002) Molecular and physical mapping of genes affecting awning in wheat. Plant Breed 121:320–324

    Article  CAS  Google Scholar 

  • Tai YS (2007) The potential wheat signaling pathways in response to abiotic stress. Amer J Plant Physiol 2:295–302

    Article  CAS  Google Scholar 

  • Theissen G, Saedler H (1999) The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev Genet 25:181–193

    PubMed  CAS  Google Scholar 

  • Unrau J, Smith WE, McGinnis RC (1950) Spike density, speltoidy, and compactoidy in hexaploid wheat. Can J Res C 28:273–276

    Article  Google Scholar 

  • Vega JM, Feldman M (1998) Effect of the pairing gene Ph1 on centromere misdivision in common wheat. Genetics 148:1285–1294

    PubMed  CAS  Google Scholar 

  • Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22:2156–2170

    Article  PubMed  CAS  Google Scholar 

  • Yoon HY, Kim SK, Kim YW, Kang HW, Lee SC, Ryu KH, Shon HS, Kim WJ, Kim YJ (2012) Combined hyper methylation of APC and GSTP1 as a molecular marker for prostate cancer: quantitative pyrosequencing analysis. J Biomol Screen 17:987–992

    Article  PubMed  Google Scholar 

  • Zhang Z (2008) Genomic analysis of Q domestication alleles and genes for susceptibility to Stagonospora nodorum in wheat, Dissertation Chapter III. NORTH DAKOTA STATE UNIVERSITY, US, pp 40–60

    Google Scholar 

  • Zhang LY, Liu DC, Guo XL, Yang WL, Sun JZ, Wang DW, Zhang AM (2010) Genomic distribution of quantitative trait loci for yield and yield-related traits in common wheat. J Integr Plant Biol 52:996–1007

    Article  PubMed  Google Scholar 

  • Zhang Z, Belcram H, Gornicki P, Charles M, Just J, Huneau C, Magdelenat G, Couloux A, Samain S, Gill BS, Rasmussen JB, Barbe V, Faris JD, Chalhoub B (2011) Duplication and partitioning in evolution and function of homologous Q loci governing domestication characters in polyploid wheat. PNAS 108:18737–18742

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F, Jiang J, von Wettstein D, Liu B (2013) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. PNAS 110:3447–3452

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge Ms. Roswitha Ende for excellent technical assistance. Also, we thank Dr. Justin D. Faris and Dr. Andreas Börner for providing seeds of the CS fndel-143 deletion and CS nulli-tetrasomic lines, respectively. We are grateful to the Federal Plant Variety Office, Hannover, Germany, and the German breeding companies KWS Lochow GmbH, Bergen, Pflanzenzucht Dr. H.c.R. Carsten, Bad Schwartau, and Dr. Hermann Strube, Söllingen, for providing speltoid bread wheat material. This research was financially supported by the Federal Ministry of Economics and Technology, Berlin (BMWi, Code Number KF 2104501MD8) and the “FAZIT-STIFTUNG Gemeinnützige Verlagsgesellschaft mbH”, Frankfurt am Main. The research project was administrated by the “Arbeitsgemeinschaft industrieller Forschungsvereinigungen e.V.”, Köln (AiF) and the “Gemeinschaft zur Förderung der privaten deutschen Pflanzenzüchtung e.V.”, Bonn (GFP).

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We certify that there is no conflict of interest with any financial organization. Further, we strictly followed ethical standards when conducting the reported research.

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Correspondence to Sebastian Förster.

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Communicated by A. E. Melchinger.

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Förster, S., Schumann, E., Baumann, M. et al. Copy number variation of chromosome 5A and its association with Q gene expression, morphological aberrations, and agronomic performance of winter wheat cultivars. Theor Appl Genet 126, 3049–3063 (2013). https://doi.org/10.1007/s00122-013-2192-8

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