Advertisement

Broadening the bread wheat D genome

  • Ghader MirzaghaderiEmail author
  • Annaliese S. Mason
Review Article

Key message

Although Ae. tauschii has been extensively utilised for wheat breeding, the D-genome-containing allopolyploids have largely remained unexploited. In this review, we discuss approaches that can be used to exploit the D genomes of the different Aegilops species for the improvement of bread wheat.

Abstract

The D genome of allohexaploid bread wheat (Triticum aestivum, 2n = AABBDD) is the least diverse of the three wheat genomes and is unarguably less diverse than that of diploid progenitor Aegilops tauschii (2n = DD). Useful genetic variation and phenotypic traits also exist within each of the wheat group species containing a copy of the D genome: allopolyploid Aegilops species Ae. cylindrica (2n = DcDcCcCc), Ae. crassa 4x (2n = D1D1XcrXcr), Ae. crassa 6x (2n = D1D1XcrXcrDcrDcr), Ae. ventricosa (2n = DvDvNvNv), Ae. vavilovii (2n = D1D1XcrXcrSvSv) and Ae. juvenalis (2n = D1D1XcrXcrUjUj). Although Ae. tauschii has been extensively utilised for wheat breeding, the D-genome-containing allopolyploids have largely remained unexploited. Some of these D genomes appear to be modified relative to the bread wheat and Ae. tauschii D genomes, and others present in the allopolyploids may also contain useful variation as a result of adaptation to an allopolyploid, multi-genome environment. We summarise the genetic relationships, karyotypic variation and phenotypic traits known to be present in each of the D genome species that could be of relevance for bread wheat improvement and discuss approaches that can be used to exploit the D genomes of the different Aegilops species for the improvement of bread wheat. Better understanding of factors controlling chromosome inheritance and recombination in wheat group interspecific hybrids, as well as effective utilisation of new and developing genetics and genomics technologies, have great potential to improve the agronomic potential of the bread wheat D genome.

Notes

Author Contribution statement

GM and ASM conceived and outlined the review; GM wrote the manuscript; and ASM revised the manuscript.

Funding

GM was supported by Iran National Science Foundation (INSF) Grant 95826690. ASM is funded by Emmy Noether DFG Grant MA6473/1-1.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, Pozniak CJ, Choulet F, Distelfeld A, Poland J (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191CrossRefPubMedGoogle Scholar
  2. Ardalani S, Mirzaghaderi G, Badakhshan H (2016) A Robertsonian translocation from Thinopyrum bessarabicum into bread wheat confers high iron and zinc contents. Plant Breed 135:286–290CrossRefGoogle Scholar
  3. Aziz A, Mahmood T, Mahmood Z, Shazadi K, Mujeeb-Kazi A, Rasheed AJCS (2018) Genotypic variation and genotype × environment interaction for yield-related traits in synthetic hexaploid wheats under a range of optimal and heat-stressed environments. Crop Sci 58:295–303CrossRefGoogle Scholar
  4. Badaeva ED, Friebe B, Gill BS (1996) Genome differentiation in Aegilops. 1. Distribution of highly repetitive DNA sequences on chromosomes of diploid species. Genome 39:293–306CrossRefPubMedGoogle Scholar
  5. Badaeva E, Amosova A, Muravenko O, Samatadze T, Chikida N, Zelenin A, Friebe B, Gill B (2002) Genome differentiation in Aegilops. 3. Evolution of the D-genome cluster. Plant Syst Evol 231:163–190CrossRefGoogle Scholar
  6. Badaeva E, Amosova A, Samatadze T, Zoshchuk S, Shostak N, Chikida N, Zelenin A, Raupp W, Friebe B, Gill B (2004) Genome differentiation in Aegilops. 4. Evolution of the U-genome cluster. Plant Syst Evol 246:45–76CrossRefGoogle Scholar
  7. Bayer PE, Ruperao P, Mason AS, Stiller J, Chan C-KK, Hayashi S, Long Y, Meng J, Sutton T, Visendi P, Varshney RK, Batley J, Edwards D (2015) High-resolution skim genotyping by sequencing reveals the distribution of crossovers and gene conversions in Cicer arietinum and Brassica napus. Theor Appl Genet 128:1039–1047CrossRefPubMedGoogle Scholar
  8. Bhatta M, Morgounov A, Belamkar V, Yorgancılar A, Baenziger PSJE (2018) Genome-wide association study reveals favorable alleles associated with common bunt resistance in synthetic hexaploid wheat. Euphytica 214:200CrossRefGoogle Scholar
  9. Bordbar F, Rahiminejad MR, Saeidi H, Blattner FR (2011) Phylogeny and genetic diversity of D-genome species of Aegilops and Triticum (Triticeae, Poaceae) from Iran based on microsatellites, ITS, and trnL-F. Plant Syst Evol 291:117–131CrossRefGoogle Scholar
  10. Burridge AJ, Winfield MO, Allen AM, Wilkinson PA, Barker GLA, Coghill J, Waterfall C, Edwards KJ (2017) High-Density SNP Genotyping Array for Hexaploid Wheat and Its Relatives. In: Bhalla PL, Singh MB (eds) Wheat Biotechnology: Methods and Protocols. Springer New York, New York, pp 293–306CrossRefGoogle Scholar
  11. Chao S, Dubcovsky J, Dvorak J, Luo M-C, Baenziger SP, Matnyazov R, Clark DR, Talbert LE, Anderson JA, Dreisigacker S, Glover K, Chen J, Campbell K, Bruckner PL, Rudd JC, Haley S, Carver BF, Perry S, Sorrells ME, Akhunov ED (2010) Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L.). BMC Genom 11:727CrossRefGoogle Scholar
  12. Chapman JA, Mascher M, Buluc A, Barry K, Georganas E, Session A, Strnadova V, Jenkins J, Sehgal S, Oliker L, Schmutz J, Yelick KA, Scholz U, Waugh R, Poland JA, Muehlbauer GJ, Stein N, Rokhsar DS (2015) A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol 16:26CrossRefPubMedPubMedCentralGoogle Scholar
  13. Charmet G (2011) Wheat domestication: lessons for the future. CR Biol 334:212–220CrossRefGoogle Scholar
  14. Chen X, Min D, Yasir TA, Hu Y-G (2012) Genetic diversity, population structure and linkage disequilibrium in elite Chinese winter wheat investigated with SSR markers. PLoS ONE 7:e44510CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cifuentes M, Benavente E (2009) Complete characterization of wheat–alien metaphase I pairing in interspecific hybrids between durum wheat (Triticum turgidum L.) and jointed goatgrass (Aegilops cylindrica Host). Theor Appl Genet 118:1609–1616CrossRefPubMedGoogle Scholar
  16. Colasuonno P, Gadaleta A, Giancaspro A, Nigro D, Giove S, Incerti O, Mangini G, Signorile A, Simeone R, Blanco A (2014) Development of a high-density SNP-based linkage map and detection of yellow pigment content QTLs in durum wheat. Mol Breeding 34:1563–1578CrossRefGoogle Scholar
  17. Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078CrossRefPubMedGoogle Scholar
  18. Cox T, Hatchett J (1994) Hessian fly-resistance gene H26 transferred from Triticum tauschii to common wheat. Crop Sci 34:958–960CrossRefGoogle Scholar
  19. Cox T, Raupp W, Gill B (1994) Leaf rust-resistance genes Lr41, Lr42, and Lr43 transferred from Triticum tauschii to common wheat. Crop Sci 34:339–343CrossRefGoogle Scholar
  20. Cox T, Sears R, Bequette R (1995) Use of winter wheat x Triticum tauschii backcross populations for germplasm evaluation. Theor Appl Genet 90:571–577CrossRefPubMedGoogle Scholar
  21. Cox TS, Wu J, Wang S, Cai J, Zhong Q, Fu B (2017) Comparing two approaches for introgression of germplasm from Aegilops tauschii into common wheat. Crop J 5:355–362CrossRefGoogle Scholar
  22. Cruz CD, Peterson GL, Bockus WW, Kankanala P, Dubcovsky J, Jordan KW, Akhunov E, Chumley F, Baldelomar FD, Valent B (2016) The 2NS translocation from Aegilops ventricosa confers resistance to the Triticum pathotype of Magnaporthe oryzae. Crop Sci 56:990–1000CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cuadrado A, Schwarzacher T, Jouve N (2000) Identification of different chromatin classes in wheat using in situ hybridization with simple sequence repeat oligonucleotides. Theor Appl Genet 101:711–717CrossRefGoogle Scholar
  24. Danilova TV, Akhunova AR, Akhunov ED, Friebe B, Gill BS (2017) Major structural genomic alterations can be associated with hybrid speciation in Aegilops markgrafii (Triticeae). Plant J 92:317–330CrossRefPubMedGoogle Scholar
  25. Del Blanco I, Rajaram S, Kronstad W (2001) Agronomic potential of synthetic hexaploid wheat-derived populations. Crop Sci 41:670–676CrossRefGoogle Scholar
  26. Dosba F, Doussinault G, Tanguy A-M, Jouault H (1981) Les lignées d’addition blé-Aegilops ventricosa. I.-Étude du comportement vis-à-vis du piétinverse des différentes lignées obtenues. Agronomie 1:503–511CrossRefGoogle Scholar
  27. Dvorak J, Zhang H-B (1990) Variation in repeated nucleotide sequences sheds light on the phylogeny of the wheat B and G genomes. Proc Natl Acad Sci 87:9640–9644CrossRefPubMedGoogle Scholar
  28. Endo T (1990) Gametocidal chromosomes and their induction of chromosome mutations in wheat. Jpn J Genet 65:135–152CrossRefGoogle Scholar
  29. Endo T, Gill B (1996) The deletion stocks of common wheat. J Hered 87:295–307CrossRefGoogle Scholar
  30. Fakhri Z, Mirzaghaderi G, Ahmadian S, Mason AS (2016) Unreduced gamete formation in wheat × Aegilops spp. hybrids is genotype specific and prevented by shared homologous subgenomes. Plant Cell Rep 35:1143–1154CrossRefPubMedGoogle Scholar
  31. Farooq S, Niazi ML, Iqbal N, Shah T (1989) Salt tolerance potential of wild resources of the tribe Triticeae. Plant Soil 119:255–260CrossRefGoogle Scholar
  32. Farooq S, Iqbal N, Asghar M, Shah T (1992) Intergeneric hybridization for wheat improvement. 6: Production of salt tolerant germplasm through crossing wheat (Triticum aestivum L.) with Aegilops cylindrica and its significance in practical agriculture. 93:095276. CIMMYTGoogle Scholar
  33. Feldman M, Levy AA, Fahima T, Korol A (2012) Genomic asymmetry in allopolyploid plants: wheat as a model. J Exp Bot 63:5045–5059CrossRefPubMedGoogle Scholar
  34. Friebe B, Zhang P, Linc G, Gill B (2005) Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogenet Genome Res 109:293–297CrossRefPubMedGoogle Scholar
  35. Gao FM, Liu JD, Yang L, Wu XX, Xiao YG, Xia XC, He ZH (2016) Genome-wide linkage mapping of QTL for physiological traits in a Chinese wheat population using the 90K SNP array. Euphytica 209:789–804CrossRefGoogle Scholar
  36. Gao LF, Zhao GY, Huang DW, Jia JZ (2017) Candidate loci involved in domestication and improvement detected by a published 90K wheat SNP array. Sci Rep 7:44530CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ghaffary SMT, Faris JD, Friesen TL, Visser RG, van der Lee TA, Robert O, Kema GHJT, Genetics A (2012) New broad-spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat. Theor Appl Genet 124:125–142CrossRefGoogle Scholar
  38. Gill BS, Raupp W (1987) Direct genetic transfers from Aegilops squarrosa L. to hexaploid wheat. Crop Sci 27:445–450CrossRefGoogle Scholar
  39. Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966–971CrossRefPubMedGoogle Scholar
  40. Heun M, Schäfer-Pregl R, Klawan D, Castagna R, Accerbi M, Borghi B, Salamini F (1997) Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278:1312–1314CrossRefGoogle Scholar
  41. Hussien T, Bowden R, Gill B, Cox T, Marshall D (1997) Performance of four new leaf rust resistance genes transferred to common wheat from Aegilops tauschii and Triticum monococcum. Plant Dis 81:582–586CrossRefGoogle Scholar
  42. Imtiaz M, Ogbonnaya FC, Oman J, van Ginkel M (2008) Characterization of quantitative trait loci controlling genetic variation for preharvest sprouting in synthetic backcross-derived wheat lines. Genetics 178:1725–1736CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jacobsen E, Schouten HJ (2007) Cisgenesis strongly improves introgression breeding and induced translocation breeding of plants. Trends Biotechnol 25:219–223CrossRefPubMedGoogle Scholar
  44. Jahier J, Tanguy A, Dedryver F, Rivoal R, Khatkar S, Bariana H (2001) The Aegilops ventricosa segment on chromosome 2AS of the wheat cultivar ‘VPM1’ carries the cereal cyst nematode resistance gene Cre5. Plant Breed 120:125–128CrossRefGoogle Scholar
  45. 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 KF, 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, International Wheat Genome Sequencing C, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95CrossRefPubMedGoogle Scholar
  46. Joukhadar R, El-Bouhssini M, Jighly A, Ogbonnaya FC (2013) Genome-wide association mapping for five major pest resistances in wheat. Mol Breeding 32:943–960CrossRefGoogle Scholar
  47. Kiani R, Arzani A, Habibi F (2015) Physiology of salinity tolerance in Aegilops cylindrica. Acta Physiol Plant 37:1–10CrossRefGoogle Scholar
  48. Kihara H (1925) Weitere Untersuchungen über die pentaploiden Triticum-Bastarde. I Jpn J Bot 2:299–305Google Scholar
  49. Kihara H, Yamashita H, Tanaka M (1959) Genomes of 6x species of Aegilops. Wheat Inform Serv 8:3–5Google Scholar
  50. Kimber G, Zhao Y (1983) The D genome of the Triticeae. Can J Genet Cytol 25:581–589CrossRefGoogle Scholar
  51. King J, Grewal S, Cy Yang, Hubbart S, Scholefield D, Ashling S, Edwards KJ, Allen AM, Burridge A, Bloor C (2017) A step change in the transfer of interspecific variation into wheat from Amblyopyrum muticum. Plant Biotechnol J 15:217–226CrossRefPubMedGoogle Scholar
  52. Knight E, Binnie A, Draeger T, Moscou M, Rey M-D, Sucher J, Mehra S, King I, Moore G (2015) Mapping the ‘breaker’ element of the gametocidal locus proximal to a block of sub-telomeric heterochromatin on the long arm of chromosome 4Ssh of Aegilops sharonensis. Theor Appl Genet 128:1049–1059CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kunert A, Naz AA, Dedeck O, Pillen K, Leon J (2007) AB-QTL analysis in winter wheat: I. Synthetic hexaploid wheat (T. turgidum ssp. dicoccoides x T. tauschii) as a source of favourable alleles for milling and baking quality traits. Theor Appl Genet 115:683–695CrossRefPubMedGoogle Scholar
  54. Lagudah ES, Macritchie F, Halloran GM (1987) The influence of high-molecular-weight subunits of glutenin from Triticum tauschii on flour quality of synthetic hexaploid wheat. J Cereal Sci 5:129–138CrossRefGoogle Scholar
  55. Lang T, Li G, Wang H, Yu Z, Chen Q, Yang E, Fu S, Tang Z, Yang Z (2018) Physical location of tandem repeats in the wheat genome and application for chromosome identification. Planta.  https://doi.org/10.1007/s00425-018-3033-4
  56. Leach LJ, Belfield EJ, Jiang CF, Brown C, Mithani A, Harberd NP (2014) Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat. BMC Genom 15:276CrossRefGoogle Scholar
  57. Leonard JM, Watson CJ, Carter AH, Hansen JL, Zemetra RS, Santra DK, Campbell KG, Riera-Lizarazu OJT, Genetics A (2008) Identification of a candidate gene for the wheat endopeptidase Ep-D1 locus and two other STS markers linked to the eyespot resistance gene Pch1. Theor Appl Genet 116:261–270CrossRefPubMedGoogle Scholar
  58. Li LF, Liu B, Olsen KM, Wendel JF (2015) A re-evaluation of the homoploid hybrid origin of Aegilops tauschii, the donor of the wheat D-subgenome. New Phytol 208:4–8CrossRefPubMedGoogle Scholar
  59. Limin A, Fowler D (1981) Cold hardiness of some relatives of hexaploid wheat. Can J Bot 59:572–573CrossRefGoogle Scholar
  60. Linc G, Gaál E, Molnár I, Icsó D, Badaeva E, Molnár-Láng M (2017) Molecular cytogenetic (FISH) and genome analysis of diploid wheatgrasses and their phylogenetic relationship. PLoS ONE 12:e0173623CrossRefPubMedPubMedCentralGoogle Scholar
  61. Ling HQ, Zhao SC, Liu DC, Wang JY, Sun H, Zhang C, Fan HJ, Li D, Dong LL, Tao Y, Gao C, Wu HL, Li YW, Cui Y, Guo XS, Zheng SS, Wang B, Yu K, Liang QS, Yang WL, Lou XY, Chen J, Feng MJ, Jian JB, Zhang XF, Luo GB, Jiang Y, Liu JJ, Wang ZB, Sha YH, Zhang BR, Wu HJ, Tang DZ, Shen QH, Xue PY, Zou SH, Wang XJ, Liu X, Wang FM, Yang YP, An XL, Dong ZY, Zhang KP, Zhang XQ, Luo MC, Dvorak J, Tong YP, Wang J, Yang HM, Li ZS, Wang DW, Zhang AM, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90CrossRefPubMedGoogle Scholar
  62. Lopes M, Dreisigacker S, Pena R, Sukumaran S, Reynolds MP (2015) Genetic characterization of the wheat association mapping initiative (WAMI) panel for dissection of complex traits in spring wheat. Theor Appl Genet 128:453CrossRefPubMedGoogle Scholar
  63. Lukaszewski AJ (1997) Further manipulation by centric misdivision of the 1RS. 1BL translocation in wheat. Euphytica 94:257–261CrossRefGoogle Scholar
  64. Luo MC, Gu YQ, You FM, Deal KR, Ma YQ, Hu YQ, Huo NX, Wang Y, Wang JR, Chen SY, Jorgensen CM, Zhang Y, McGuire PE, Pasternak S, Stein JC, Ware D, Kramer M, McCombie WR, Kianian SF, Martis MM, Mayer KFX, Sehgal SK, Li WL, Gill BS, Bevan MW, Simkova H, Dolezel J, Song WN, Lazo GR, 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 Natl Acad Sci USA 110:7940–7945CrossRefPubMedGoogle Scholar
  65. Maccaferri M, Ricci A, Salvi S, Milner SG, Noli E, Martelli PL, Casadio R, Akhunov E, Scalabrin S, Vendramin V, Ammar K, Blanco A, Desiderio F, Distelfeld A, Dubcovsky J, Fahima T, Faris J, Korol A, Massi A, Mastrangelo AM, Morgante M, Pozniak C, N’Diaye A, Xu S, Tuberosa R (2015) A high-density, SNP-based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotechnol J 13:648–663CrossRefPubMedGoogle Scholar
  66. Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Consortium TIWGS, Jakobsen KS, Wulff BBH, Steuernagel B, Mayer KFX, Olsen O-A (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345:1250092CrossRefPubMedGoogle Scholar
  67. Mason AS, Batley J (2015) Creating new interspecific hybrid and polyploid crops. Trends Biotechnol 33:436–441CrossRefPubMedGoogle Scholar
  68. McNeil D, Lagudah ES, Hohmann U, Appels R (1994) Amplification of DNA sequences in wheat and its relatives: the Dgas44 and R350 families of repetitive sequences. Genome 37:320–327CrossRefPubMedGoogle Scholar
  69. Meimberg H, Rice KJ, Milan NF, Njoku CC, McKay JK (2009) Multiple origins promote the ecological amplitude of allopolyploid Aegilops (Poaceae). Am J Bot 96:1262–1273CrossRefPubMedGoogle Scholar
  70. Mena M, Doussinault G, Lopez-Braña I, Aguaded S, García-Olmedo F, Delibes A (1992) Eyespot resistance gene Pch-1 in H-93 wheat lines. Evidence of linkage to markers of chromosome group 7 and resolution from the endopeptidase locus Ep-D1b. Theor Appl Genet 83:1044–1047CrossRefPubMedGoogle Scholar
  71. Middleton CP, Senerchia N, Stein N, Akhunov ED, Keller B, Wicker T, Kilian B (2014) Sequencing of chloroplast genomes from wheat, barley, rye and their relatives provides a detailed Insight into the evolution of the Triticeae tribe. PLoS ONE 9:e85761CrossRefPubMedPubMedCentralGoogle Scholar
  72. Miranda L, Murphy J, Marshall D, Cowger C, Leath S (2007) Chromosomal location of Pm35, a novel Aegilops tauschii derived powdery mildew resistance gene introgressed into common wheat (Triticum aestivum L.). Theor Appl Genet 114:1451–1456CrossRefPubMedGoogle Scholar
  73. Mirzaghaderi G, Houben A, Badaeva ED (2014) Molecular-cytogenetic analysis of Aegilops triuncialis and identification of its chromosomes in the background of wheat. Mol Cytogenet 7:91CrossRefPubMedPubMedCentralGoogle Scholar
  74. Molnár-Láng M (2015) The Crossability of Wheat with Rye and Other Related Species. In: Molnár-Láng M, Ceoloni C, Doležel J (eds) Alien Introgression in Wheat: Cytogenetics, Molecular Biology, and Genomics. Springer International Publishing, Cham, pp 103–120Google Scholar
  75. Morrison LA, Crémieux LC, Mallory-Smith CA (2002) Infestations of jointed goatgrass (Aegilops cylindrica) and its hybrids with wheat in Oregon wheat fields. Weed Sci 50:737–747CrossRefGoogle Scholar
  76. Mujeeb-Kazi A, Rosas V, Roldan S (1996) Conservation of the genetic variation of Triticum tauschii (Coss.) Schmalh. (Aegilops squarrosa auct. non L.) in synthetic hexaploid wheats (T. turgidum L. s. lat. x T. tauschii; 2n = 6x = 42, AABBDD) and its potential utilization for wheat improvement. Genet Resour Crop Evol 43:129–134CrossRefGoogle Scholar
  77. Mujeeb-Kazi A, Fuentes-Davila G, Villareal R, Cortes A, Roasas V, Delgado R (2001) Registration of 10 synthetic hexaploid wheat and six bread wheat germplasms resistant to karnal bunt. Crop Sci 41:1652CrossRefGoogle Scholar
  78. Mujeeb-Kazi A, Gul A, Farooq M, Rizwan S, Ahmad I (2008) Rebirth of synthetic hexaploids with global implications for wheat improvement. Crop Pasture Sci 59:391–398CrossRefGoogle Scholar
  79. Mukai Y (1996) Multicolor fluorescence in situ hybridization: a new tool for genome analysis. In: Jauhar PP (ed) Methods of Genome Analysis in Plants. CRC Press, Boca Raton, Fla., pp 181–192Google Scholar
  80. Mulki MA, Jighly A, Ye G, Emebiri LC, Moody D, Ansari O, Ogbonnaya FC (2013) Association mapping for soilborne pathogen resistance in synthetic hexaploid wheat. Mol Breeding 31:299–311CrossRefGoogle Scholar
  81. Murai K, Tsunewaki K (1993) Photoperiod-sensitive cytoplasmic male sterility in wheat with Aegilops crassa cytoplasm. Euphytica 67:41–48CrossRefGoogle Scholar
  82. Murai K, Ohta H, Kurushima M, Ishikawa N (2016) Photoperiod-sensitive cytoplasmic male sterile elite lines for hybrid wheat breeding, showing high cross-pollination fertility under long-day conditions. Euphytica 212:313–322CrossRefGoogle Scholar
  83. Nakai Y (1982) D genome donors for Aegilops crassa (DDMcrMcr, DDD2D2McrMcr) and Ae. vavilovii (DDMcrMcrSpSp) deduced from esterase analysis by isoelectric focusing. Jpn J Genet 57:349–360CrossRefGoogle Scholar
  84. Naranjo T, Benavente E (2015) The Mode and Regulation of Chromosome Pairing in Wheat-Alien Hybrids (Ph Genes, an Updated View). In: Molnár-Láng M, Ceoloni C, Doležel J (eds) Alien Introgression in Wheat: Cytogenetics, Molecular Biology, and Genomics. Springer International Publishing, Cham, pp 133–162Google Scholar
  85. Ogbonnaya FC, Halloran GM, Lagudah ES (2005) D genome of wheat—60 years on from Kihara, Sears and McFadden. In: Tsunewaki K (ed) Frontiers of wheat bioscience. Kihara memorial foundation for the advancement of life sciences, Yokohama, pp 205–220Google Scholar
  86. Okamoto Y, Nguyen AT, Yoshioka M, Iehisa JCM, Takumi S (2013) Identification of quantitative trait loci controlling grain size and shape in the D genome of synthetic hexaploid wheat lines. Breed Sci 63:423–429CrossRefPubMedPubMedCentralGoogle Scholar
  87. Olson EL, Rouse MN, Pumphrey MO, Bowden RL, Gill BS, Poland JA (2013) Simultaneous transfer, introgression, and genomic localization of genes for resistance to stem rust race TTKSK (Ug99) from Aegilops tauschii to wheat. Theor Appl Genet 126:1179–1188CrossRefPubMedGoogle Scholar
  88. Padmanaban S, Sutherland MW, Knight NL, Martin A (2017a) Genome inheritance in populations derived from hexaploid/tetraploid and tetraploid/hexaploid wheat crosses. Mol Breeding 37:48CrossRefGoogle Scholar
  89. Padmanaban S, Zhang P, Hare RA, Sutherland MW, Martin A (2017b) Pentaploid wheat hybrids: applications, characterisation, and challenges. Front Plant Sci 8:358CrossRefPubMedPubMedCentralGoogle Scholar
  90. Padmanaban S, Zhang P, Sutherland MW, Knight NL, Martin A (2018) A cytological and molecular analysis of D-genome chromosome retention following F2–F6 generations of hexaploid × tetraploid wheat crosses. Crop Pasture Sci 69:121–130CrossRefGoogle Scholar
  91. Pedersen C, Langridge P (1997) Identification of the entire chromosome complement of bread wheat by two-colour FISH. Genome 40:589–593CrossRefPubMedGoogle Scholar
  92. Prażak R (2001) Cross direction for successful production of F1 hybrids between Triticum and Aegilops species. Plant Breed Seed Sci 45:83–86Google Scholar
  93. Qi L, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosome Res 15:3–19CrossRefPubMedGoogle Scholar
  94. Rasheed A, Xia X, Ogbonnaya F, Mahmood T, Zhang Z, Mujeeb-Kazi A, He Z (2014) Genome-wide association for grain morphology in synthetic hexaploid wheats using digital imaging analysis. BMC Plant Biol 14:128CrossRefPubMedPubMedCentralGoogle Scholar
  95. Raupp W, Amri A, Hatchett J, Gill B, Wilson D, Cox T (1993) Chromosomal location of hessian fly–resistance Genes H22, H23, and H24 derived from Triticum tauschii in the D genome of wheat. J Hered 84:142–145CrossRefGoogle Scholar
  96. Raupp WJ, Sukhwinder-Singh Brown-Guedira GL, Gill BS (2001) Cytogenetic and molecular mapping of the leaf rust resistance gene Lr39 in wheat. Theor Appl Genet 102:347–352CrossRefGoogle Scholar
  97. Rayburn AL, Gill BS (1986) Isolation of a D-genome specific repeated DNA sequence from Aegilops squarrosa. Plant Mol Biol Report 4:102–109CrossRefGoogle Scholar
  98. Rayburn AL, Gill BS (1987) Molecular analysis of the D-genome of the Triticeae. Theor Appl Genet 73:385–388CrossRefPubMedGoogle Scholar
  99. Riehl S, Zeidi M, Conard NJ (2013) Emergence of agriculture in the foothills of the Zagros Mountains of Iran. Science 341:65–67CrossRefPubMedGoogle Scholar
  100. Riley R, Chapman V (1958) Genetic control of cytologically diploid behavior of hexaploid wheat. Nature 182:713–715CrossRefGoogle Scholar
  101. Riley R, Chapman V, Johnson R (1968) The incorporation of alien disease resistance in wheat by genetic interference with the regulation of meiotic chromosome synapsis. Genet Res Camb 12:199–219CrossRefGoogle Scholar
  102. Ruperao P, Chan CKK, Azam S, Karafiatova M, Hayashi S, Cizkova J, Saxena RK, Simkova H, Song C, Vrana J, Chitikineni A, Visendi P, Gaur PM, Millan T, Singh KB, Taran B, Wang J, Batley J, Dolezel J, Varshney RK, Edwards D (2014) A chromosomal genomics approach to assess and validate the desi and kabuli draft chickpea genome assemblies. Plant Biotechnol J 12:778–786CrossRefPubMedGoogle Scholar
  103. Saluja M, Kaur S, Bansal U, Bhardwaj SC, Chhuneja P (2018) Molecular mapping of linked leaf rust resistance and non-glaucousness gene introgressed from Aegilops tauschii Coss. in hexaploid wheat Triticum aestivum L. Plant Genet Resour Charact Util 16:82–88CrossRefGoogle Scholar
  104. Schneider A, Molnár I, Molnár-Láng M (2008) Utilisation of Aegilops (goatgrass) species to widen the genetic diversity of cultivated wheat. Euphytica 163:1–19CrossRefGoogle Scholar
  105. Sears E (1956) The transfer of leaf-rust resistance from Aegilops umbellulata to wheat. Brookhaven Symp Biol 9:1–22Google Scholar
  106. Sehgal S, Kaur S, Gupta S, Sharma A, Kaur R, Bains N (2011) A direct hybridization approach to gene transfer from Aegilops tauschii Coss. to Triticum aestivum L. Plant Breed 130:98–100CrossRefGoogle Scholar
  107. Sharma HC, Gill BS (1983) Current status of wide hybridization in wheat. Euphytica 32:17–31CrossRefGoogle Scholar
  108. Singh RP, Nelson JC, Sorrells ME (2000) Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci 40:1148–1155CrossRefGoogle Scholar
  109. Singh S, Franks C, Huang L, Brown-Guedira G, Marshall D, Gill B, Fritz A (2004) Lr41, Lr39, and a leaf rust resistance gene from Aegilops cylindrica may be allelic and are located on wheat chromosome 2DS. Theor Appl Genet 108:586–591CrossRefPubMedGoogle Scholar
  110. Sutka J (1994) Genetic control of frost tolerance in wheat (Triticum aestivum L.). Euphytica 77:277–282CrossRefGoogle Scholar
  111. Tan C-T, Yu H, Yang Y, Xu X, Chen M, Rudd JC, Xue Q, Ibrahim AMH, Garza L, Wang S, Sorrells ME, Liu S (2017) Development and validation of KASP markers for the greenbug resistance gene Gb7 and the Hessian fly resistance gene H32 in wheat. Theor Appl Genet 130:1867–1884CrossRefPubMedGoogle Scholar
  112. Tang Y-l, Yang W-y, Tian J-c, Li J, Chen F (2008) Effect of HMW-GS 6 + 8 and 1.5 + 10 from synthetic hexaploid wheat on wheat quality traits. Agric Sci China 7:1161–1171CrossRefGoogle Scholar
  113. The T (1973) Chromosome location of genes conditioning stem rust resistance transferred from diploid to hexaploid wheat. Nat New Biol 241:256CrossRefPubMedGoogle Scholar
  114. Tiwari VK, Wang S, Sehgal S, Vrána J, Friebe B, Kubaláková M, Chhuneja P, Doležel J, Akhunov E, Kalia B (2014) SNP discovery for mapping alien introgressions in wheat. BMC Genom 15:273CrossRefGoogle Scholar
  115. van Slageren MW (1994) Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae), vol 94-7. Wageningen Agricultural University Papers, Wageningen, The NetherlandsGoogle Scholar
  116. Vikas V, Sivasamy M, Kumar J, Jayaprakash P, Kumar S, Parimalan R, Kumar A, Srinivasan K, Radhamani J, Jacob SR (2014) Stem and leaf rust resistance in wild relatives of wheat with D genome (Aegilops spp.). Genet Resour Crop Evol 61:861–874CrossRefGoogle Scholar
  117. Voss-Fels K, Snowdon RJ (2015) Understanding and utilizing crop genome diversity via high-resolution genotyping. Plant Biotechnol J 14:1086–1094CrossRefPubMedGoogle Scholar
  118. Voss-Fels K, Frisch M, Qian L, Kontowski S, Friedt W, Gottwald S, Snowdon RJ (2015) Subgenomic diversity patterns caused by directional selection in bread wheat gene pools. Plant Genome 8:1–13CrossRefGoogle Scholar
  119. Wang T, Xu SS, Harris MO, Hu J, Liu L, Cai X (2006) Genetic characterization and molecular mapping of Hessian fly resistance genes derived from Aegilops tauschii in synthetic wheat. Theor Appl Genet 113:611–618CrossRefPubMedGoogle Scholar
  120. 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 198:925–937CrossRefPubMedGoogle Scholar
  121. Wang SC, Wong DB, Forrest K, Allen A, Chao SM, Huang BE, Maccaferri M, Salvi S, Milner SG, Cattivelli L, Mastrangelo AM, Whan A, Stephen S, Barker G, Wieseke R, Plieske J, Lillemo M, Mather D, Appels R, Dolferus R, Brown-Guedira G, Korol A, Akhunova AR, Feuillet C, Salse J, Morgante M, Pozniak C, Luo MC, Dvorak J, Morell M, Dubcovsky J, Ganal M, Tuberosa R, Lawley C, Mikoulitch I, Cavanagh C, Edwards KJ, Hayden M, Akhunov E, Sequencing IWG (2014) Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol J 12:787–796CrossRefPubMedPubMedCentralGoogle Scholar
  122. Wang XT, Zhang HK, Li YL, Zhang ZB, Li LF, Liu B (2016) Transcriptome asymmetry in synthetic and natural allotetraploid wheats, revealed by RNA-sequencing. New Phytol 209:1264–1277CrossRefPubMedGoogle Scholar
  123. Wang Y, Han Q, He F, Bao Y, Ming D, Wang H (2017) Characterization of a Triticum aestivum-Aegilops germplasm line presenting reduced plant height and early maturation. Crop J 5:185–194CrossRefGoogle Scholar
  124. Wendel JF, Lisch D, Hu G, Mason AS (2018) The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Curr Opin Genet Dev 49:1–7CrossRefPubMedGoogle Scholar
  125. Williamson VM, Thomas V, Ferris H, Dubcovsky J (2013) An Aegilops ventricosa translocation confers resistance against root-knot nematodes to common wheat. Crop Sci 53:1412CrossRefPubMedPubMedCentralGoogle Scholar
  126. Winfield MO, Allen AM, Burridge AJ, Barker GLA, Benbow HR, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, King J, West C, Griffiths S, King I, Bentley AR, Edwards KJ (2016) High-density SNP genotyping array for hexaploid wheat and its secondary and tertiary gene pool. Plant Biotechnol J 14:1195–1206CrossRefPubMedGoogle Scholar
  127. Xu S, Dong Y (1992) Fertility and meiotic mechanisms of hybrids between chromosome autoduplication tetraploid wheats and Aegilops species. Genome 35:379–384CrossRefGoogle Scholar
  128. Yan L, Liang F, Xu H, Zhang X, Zhai H, Sun Q, Ni Z (2017) Identification of QTL for grain size and shape on the D genome of natural and synthetic allohexaploid wheats with near-identical AABB genomes. Front Plant Sci 8:1705CrossRefPubMedPubMedCentralGoogle Scholar
  129. Yang W, Liu D, Li J, Zhang L, Wei H, Hu X, Zheng Y, He Z, Zou Y (2009) Synthetic hexaploid wheat and its utilization for wheat genetic improvement in China. J Genet Genomics 36:539–546CrossRefPubMedGoogle Scholar
  130. Yang C, Zhao L, Zhang H, Yang Z, Wang H, Wen S, Zhang C, Rustgi S, von Wettstein D, Liu B (2014) Evolution of physiological responses to salt stress in hexaploid wheat. Proc Natl Acad Sci USA 111:11882–11887CrossRefPubMedGoogle Scholar
  131. Zegeye H, Rasheed A, Makdis F, Badebo A, Ogbonnaya FC (2014) Genome-wide association mapping for seedling and adult plant resistance to stripe rust in synthetic hexaploid wheat. PLoS ONE 9:e105593CrossRefPubMedPubMedCentralGoogle Scholar
  132. Zemetra R, Hansen J, Mallory-Smith C (1998) Potential for gene transfer between wheat (Triticum aestivum) and jointed goatgrass (Aegilops cylindrica). Weed Sci 46:313–317Google Scholar
  133. Zhang H-B, Dvořák J (1992) The genome origin and evolution of hexaploid Triticum crassum and Triticum syriacum determined from variation in repeated nucleotide sequences. Genome 35:806–814CrossRefGoogle Scholar
  134. Zhang P, Li W, Friebe B, Gill BS (2004) Simultaneous painting of three genomes in hexaploid wheat by BAC-FISH. Genome 47:979–987CrossRefPubMedGoogle Scholar
  135. Zhang YM, Liu ZS, Khan A, Lin Q, Han Y, Mu P, Liu YG, Zhang HS, Li LY, Meng XH, Ni ZF, Xin MM (2016) Expression partitioning of homeologs and tandem duplications contribute to salt tolerance in wheat (Triticum aestivum L.). Sci Rep 6:21476CrossRefPubMedPubMedCentralGoogle Scholar
  136. Zhang P, Dundas IS, Xu SS, Friebe B, McIntosh RA, Raupp WJ (2017) Chromosome engineering techniques for targeted introgression of rust resistance from wild wheat relatives. In: Wheat rust diseases. Springer, pp 163–172Google Scholar
  137. Zhang R, Singh RP, Lillemo M, He X, Randhawa MS, Huerta-Espino J, Singh PK, Li Z, Lan C (2018) Two main stripe rust resistance genes identified in synthetic-derived wheat line Soru#1. Phytopathology.  https://doi.org/10.1094/phyto-1004-1018-0141-r CrossRefPubMedGoogle Scholar
  138. Zhao YH, Kimber G (1984) New hybrids with D-genome wheat relatives. Genetics 106:509–515PubMedPubMedCentralGoogle Scholar
  139. Zhou S, Zhang J, Che Y, Liu W, Lu Y, Yang X, Li X, Jia J, Liu X, Li L (2017) Construction of Agropyron Gaertn. genetic linkage maps using a wheat 660K SNP array reveals a homoeologous relationship with the wheat genome. Plant Biotechnol J 16:818–827CrossRefPubMedPubMedCentralGoogle Scholar
  140. Zhu Y, Saraike T, Yamamoto Y, Hagita H, Takumi S, Murai K (2008) orf260cra, a novel mitochondrial gene, is associated with the homeotic transformation of stamens into pistil-like structures (pistillody) in alloplasmic wheat. Plant Cell Physiol 49:1723–1733CrossRefPubMedGoogle Scholar
  141. Zimin AV, Puiu D, Hall R, Kingan S, Salzberg SL (2017) The first near-complete assembly of the hexaploid bread wheat genome, Triticum aestivum. BioRxiv.  https://doi.org/10.1101/159111:159111 CrossRefGoogle Scholar
  142. Zou J, Semagn K, Iqbal M, N’Diaye A, Chen H, Asif M, Navabi A, Perez-Lara E, Pozniak C, Yang RC, Randhawa H, Spaner D (2017) Mapping QTLs controlling agronomic traits in the ‘Attila’ x ‘CDC Go’ spring wheat population under organic management using 90K SNP array. Crop Sci 57:365–377CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Agronomy and Plant Breeding, Faculty of AgricultureUniversity of KurdistanSanandajIran
  2. 2.Department of Plant BreedingJustus Liebig University, IFZ Research Centre for Biosystems, Land Use and NutritionGiessenGermany

Personalised recommendations