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Fine mapping of shattering locus Br2 reveals a putative chromosomal inversion polymorphism between the two lineages of Aegilops tauschii

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Abstract

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This work laid the foundation for cloning of shattering gene Br2 and provided first line of evidence that two major Aegilops tauschii lineages are differentiated by an inversion polymorphism.

Abstract

Chromosome inversions often accompany population differentiation and capture local adaptation during speciation. Aegilops tauschii, the D-genome donor species of hexaploid wheat, consists of two genetically isolated lineages, L1 and L2, but little is known about the genetic mechanisms underlying the population differentiation in this diploid species. During fine mapping of the shattering gene Br2 using a large F2 population derived from a cross between TA1604 (an L1 accession) and AL8/78 (an L2 accession), we found contrasting patterns of crossover distribution in the Br2 interval and neighboring regions despite the high local gene synteny with Brachypodium distachyon and rice. Br2 was localized in a 0.08-cM interval, and 13 marker loci formed a block, where single-crossovers were completely suppressed, but double-crossovers were enriched with a recombination rate of ~11 cM/Mb. In contrast, in a neighboring region no double-crossover was recovered, but single-crossover rate reached 24 cM/Mb, which is much higher than the genome-wide average. This result suggests a putative inversion polymorphism between the parental lines in the Br2 region. Genotyping using the markers from the Br2 region divided a collection of 55 randomly sampled A. tauschii accessions into two major groups, and they are largely genetically isolated. The two groups correspond to the L1 and L2 lineages based on their geographic distribution patterns. This provides first evidence that inversions may underlie the evolution of A. tauschii lineages. The presence of inter-lineage inversions may complicate map-based cloning in A. tauschii and transfer of useful traits to wheat.

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Abbreviations

asl:

Above sea level

BP:

Before present

BAC:

Bacterial artificial chromosome

CAPS:

Cleaved amplified polymorphic sequence

cM:

Centimorgan

dCAPS:

Derived CAPS

indel:

Small insertion/deletion

MTP:

Minimal tiling path

RFLP:

Restriction fragment length polymorphism

SNP:

Single nucleotide polymorphism

UPGMA:

Unweighted pair group method with arithmetic means

UTR:

Untranslated region

References

  • Ayala D, Guerrero RF, Kirkpatrick M (2013) Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito. Evolution 67:946–958

    Article  PubMed  Google Scholar 

  • Dudnikov AJ (2011) Waxiness in Aegilops tauschii: its occurrence in natural habitats of the species. Cereal Res Commun 39:283–288

    Article  Google Scholar 

  • Dvorak J, Luo M-C, Yang Z-L, Zhang H-B (1998) The structure of Aegilops tauschii genepool and the evolution of hexaploid wheat. Theor Appl Genet 97:657–670

    Article  CAS  Google Scholar 

  • Eig A (1929) Monographisch-Kritische Uebersicht der Gatung Aegilops. Verlag des Repertoriums, Dahlem bei Berlin

    Google Scholar 

  • Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed Rev 24:1–44

    Google Scholar 

  • Guerrero RF, Rousset F, Kirkpatrick M (2012) Coalescent patterns for chromosomal inversions in divergent populations. Philos Trans R Soc Lond Ser B Biol Sci 367:430–438

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, pp 95–98

  • Hammer K (1980) Vorarbeiten zur monographischen Darstellung von Wildpflanzensortimenten: Aegilops L. Kulturpflanze 28:33–180

    Article  Google Scholar 

  • Harlan JR (1992) Crops and man, 2nd edn. Am Soc, Agronomy

    Google Scholar 

  • Huang L, Brooks S, Li W, Fellers J, Nelson JC, Gill B (2009) Evolution of new disease specificity at a simple resistance locus in a crop-weed complex: reconstitution of the Lr21 gene in wheat. Genetics 182:595–602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer K, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C, Quan Z, Liu G, Wang J, Consortium IWGS, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95

    Article  CAS  PubMed  Google Scholar 

  • Kimber G, Feldman M (1987) Wild wheat, an introduction. Columbia, MO

    Google Scholar 

  • Konishi S, Izawa T, Lin S, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312:1392–1396

    Article  CAS  PubMed  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Li W, Gill BS (2006) Multiple genetic pathways for seed shattering in the grasses. Funct Integr Genomics 6:300–309

    Article  CAS  PubMed  Google Scholar 

  • Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936–1939

    Article  CAS  PubMed  Google Scholar 

  • Li W, Huang L, Gill BS (2008) Recurrent deletions of puroindoline genes at the grain hardness locus in four independent lineages of polyploid wheat. Plant Physiol 146:200–212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li W, Zhu H, Challa GS, Zhang Z (2013) A non-additive interaction in a single locus causes a very short root phenotype in wheat. Theor Appl Genet 126:1189–1200

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Griffith ME, Li X, Zhu Z, Tan L, Fu Y, Zhang W, Wang X, Xie D, Sun C (2007) Origin of seed shattering in rice (Oryza sativa L.). Planta 226:11–20

    Article  CAS  PubMed  Google Scholar 

  • Lin Z, Li X, Shannon LM, Yeh CT, Wang ML, Bai G, Peng Z, Li J, Trick HN, Clemente TE, Doebley J, Schnable PS, Tuinstra MR, Tesso TT, White F, Yu J (2012) Parallel domestication of the Shattering1 genes in cereals. Nature Genet 13:720–724

    Article  Google Scholar 

  • Lincoln S, Lander ES (1992) Systematic detection of errors in genetic linkage data. Genomics 14:604–610

    Article  CAS  PubMed  Google Scholar 

  • Lowry DB, Willis JH (2010) A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol 8:e1000500

    Article  PubMed Central  PubMed  Google Scholar 

  • Lubbers L, Gill KS, Cox TS, Gill BS (1991) Variation of molecular markers among geographically diverse accessions of Triticum tauschii. Genome 34:354–361

    Article  Google Scholar 

  • Luo MC, Gu YQ, You FM, Deal KR, Ma Y, Hu Y, Huo N, Wang Y, Wang J, Chen S, Jorgensen CM, Zhang Y, McGuire P, Pasternak S, Stein J, Ware D, Kramer M, McCombie WR, Kianian SF, Martis MM, Mayer KF, Sehgal SK, Li W, Gill BS, Bevan MW, Simková H, Dolezel J, Weining S, Lazo G, Anderson OD, Dvorak J (2013) A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat D-genome progenitor. Proc Nat Acad Sci USA 110:7940–7945

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McGaugh SE, Noor MA (2012) Genomic impacts of chromosomal inversions in parapatric Drosophila species. Philos Trans R Soc Lond Ser B Biol Sci 367:422–429

    Article  Google Scholar 

  • Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Mol Ecol 19:999–1013

    Article  PubMed  Google Scholar 

  • Nalam VJ, Vales MI, Watson CJ, Kianian SF, Riera-Lizarazu O (2006) Map-based analysis of genes affecting the brittle rachis character in tetraploid wheat (Triticum turgidum L.). Theor Appl Genet 112:373–381

    Article  CAS  PubMed  Google Scholar 

  • Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392

    Article  CAS  PubMed  Google Scholar 

  • Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, Mago R, McIntosh R, Dodds P, Dvorak J, Lagudah E (2013) The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341:786–788

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, La RCM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma X-F, Gustafson JP, Miftahudin, Wennerlind EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi D-W, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 10,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the near east. Nat Rev Genet 3:429–441

    CAS  PubMed  Google Scholar 

  • Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotech 31:686–688

    Article  CAS  Google Scholar 

  • Sohail Q, Shehzad T, Kilian A, Eltayeb AE, Tanaka H, Tsujimoto H (2012) Development of diversity array technology (DArT) markers for assessment of population structure and diversity in Aegilops tauschii. Breed Sci 62:38–45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thiel T, Kota R, Grosse I, Stein N, Graner A (2004) SNP2CAPS: a SNP and INDEL analysis tool for CAPS marker development. Nucleic Acids Res 32:e5

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang J, Luo MC, Chen Z, You FM, Wei Y, Zheng Y, Dvorak J (2013) Aegilops tauschii single nucleotide polymorphisms shed light on the origins of wheat D-genome genetic diversity and pinpoint the geographic origin of hexaploid wheat. New Phytol 198:925–937

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Fujii Y, Kato N, Ban T, Martinek P (2006) Microsatellite mapping of the genes for brittle rachis on homoeologous group 3 chromosomes in tetraploid and hexaploid wheats. J Appl Genet 47:93–98

    Article  PubMed  Google Scholar 

  • Weng Y, Li W, Devkota RN, Rudd JC (2005) Microsatellite markers associated with two Aegilops tauschii-derived greenbug resistance loci in wheat. Theor Appl Genet 110:462–469

    Article  CAS  PubMed  Google Scholar 

  • Yildirim A, Jones SS, Murray TD, Cox TS, Line RF (1995) Resistance to stripe rust and eyespot disease of wheat in Triticum tauschii. Plant Dis 79:1230–1236

    Article  Google Scholar 

  • You FM, Huo N, Deal KR, Gu YQ, Luo MC, McGuire PE, Dvorak J, Anderson OD (2011) Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genom 12:59

    Article  CAS  Google Scholar 

  • Zhou Y, Lu D, Li C, Luo J, Zhu BF, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B, Han B (2012) Genetic control of seed shattering in rice by the APETALA2 transcription factor shattering abortion1. Plant Cell 24:1034–1048

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Jan Dvorak for supplying the BAC clones and the seeds of A. tauschii accession AL8/78. This project was supported by USDA Hatch program through South Dakota Agricultural Experiment Station (WL) and NSF WGRC I/UCRC Award Number 1338897 (BSG).

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The authors declare that they have no conflict of interest.

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Correspondence to Wanlong Li.

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Communicated by M. J. Sillanpaa.

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Zhang, Z., Zhu, H., Gill, B.S. et al. Fine mapping of shattering locus Br2 reveals a putative chromosomal inversion polymorphism between the two lineages of Aegilops tauschii . Theor Appl Genet 128, 745–755 (2015). https://doi.org/10.1007/s00122-015-2469-1

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