Abstract
The introduction of Reduced height (Rht)-B1b and Rht-D1b into bread wheat (Triticum aestivum) varieties was a key component of the ‘green revolution’ and today these alleles are the primary sources of semi-dwarfism in wheat. The Rht-1 loci encode DELLA proteins, which are transcription factors that affect plant growth and stress tolerance. In bread wheat, Rht-D1b and Rht-B1b influence resistance to the disease Fusarium Head Blight. To identify Rht-1 variants, locus specific primers were developed and used to sequence the entire open reading frame (ORF) and 1.7 kb of the 5′ and 0.5 kb of the 3′ flanking regions of Rht-A1 (Rht-A1+f), Rht-B1 (Rht-B1+f), and Rht-D1 (Rht-D1+f) in bread wheat (36 sequences from each genome) and tetraploid and diploid wheat (TDW) (one to three sequences from each genome). Among the bread wheat accessions, the Rht-A1+f and Rht-D1+f sequences contained relatively low genetic diversity and few haplotypes relative to the Rht-B1+f sequences. The TDW accessions were relatively rich in genetic diversity and contained the majority of the polymorphic sites. Novel polymorphisms, relative to ‘Chinese Spring’, discovered among the accessions include 160 and 197 bp insertions 5′ of Rht-B1 and a frameshift in the Rht-B1 ORF. Quantitative real-time PCR using shoot and leaf tissue from 5-day-old seedlings of genotypes lacking or containing the 5′ insertions revealed no major effect on Rht-B1 transcript accumulation. This research provides insights into the genetic diversity present at the Rht-1 loci in modern bread wheat and in relation to ancestral wheat accessions.
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References
Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092
Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng JR, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94
Alvey L, Boulton MI (2008) DELLA proteins in signalling. Encyclopedia of Life Sciences. John Wiley & Sons Ltd, Chichester
Alvey L, Harberd NP (2005) DELLA proteins: integrators of multiple plant growth regulatory inputs? Physiol Plant 123:153–160
Balfourier F, Roussel V, Strelchenko P, Exbrayat-Vinson F, Sourdille P, Boutet G, Koenig J, Ravel C, Mitrofanova O, Beckert M, Charmet G (2007) A worldwide bread wheat core collection arrayed in a 384-well plate. Theor App Gen 114:1265–1275
Bryan GJ, Collins AJ, Stephenson P, Orry A, Smith JB, Gale MD (1997) Isolation and characterisation of microsatellites from hexaploid bread wheat. Theor Appl Gen 94:557–563
Buerstmayr M, Huber K, Heckmann J, Steiner B, Nelson JC, Buerstmayr H (2012) Mapping of QTL for Fusarium head blight resistance and morphological and developmental traits in three backcross populations derived from Triticum dicoccum × Triticum durum. Theor Appl Gen 125:1751–1765
Caldwell KS, Dvorak J, Lagudah ES, Akhunov E, Luo M-C, Wolters P, Powell W (2004) Sequence polymorphism in polyploidy wheat and their D-genome diploid ancestor. Genetics 167:941–947
Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and Physiological Characterization. Plant Physiol 129:181–190
Chao S, Zhang W, Akhunov E, Sherman J, Ma Y, Luo M-C, Dubcovsky J (2009) Analysis of gene-derived SNP marker polymorphism in US wheat (Triticum aestivum L.) cultivars. Mol Breeding 23:23–33
Cho CH, Hong BH, Park MW, Shim JW, Kim BK (1980) Origin, dissemination, and utilization of wheat semi-dwarf genes in Korea. Annu Wheat Newsl 27:67
Chrpova JS, Skorpik M, Prasilova P, Sip V (2003) Detection of Norin 10 dwarfing genes in winter wheat varieties registered in the Czech Republic. Czech J Genet Plant Breed 39:89–92
Coram TE, Wang MN, Chen XM (2008) Transcriptome analysis of the wheat - Puccinia striiformis f. sp tritici interaction. Molec Plant Pathol 9:157–169
Dalrymple DG (1986) Development and spread of high-yielding wheat varieties in developing countries. Agency for International Development, Washington
Dan L, FangPing Y, ZhongHu H, DaNian Y, XianChun X (2009) Characterization of Lr34/Yr18, Rht-B1b, Rht-D1b genes in CIMMYT wheat cultivars and advanced lines using STS markers. Sci Agric Sin 42:17–27
Doebley JF (2004) The genetics of maize evolution. Ann Rev Gen 38:37–59
Draeger R, Gosman N, Steed A, Chandler E, Thomsett M, Srinivasachary, Schondelmaier J, Buerstmayr H, Lemmens M, Schmolke M, Mesterhazy A, Nicholson P (2007) Identification of QTLs for resistance to Fusarium head blight, DON accumulation and associated traits in the winter wheat variety Arina. Theor Appl Genet 115:617–625
Duan J, Wu J, Liu Y, Xiao J, Zhao G, Gu Y, Jia J, Kong X (2012) New cis-regulatory elements in the Rht-D1b locus region of wheat. Funct Integr Genomics 12:489–500
Dvorak J, Akhunov ED (2005) Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploidy evolution in the Aegilops-Triticum alliance. Genetics 171:323–332
Ellis MH, Spielmeyer W, Gale KR, Rebetzke GJ, Richards RA (2002) “Perfect” markers for the Rht-B1b and Rht-D1b dwarfing genes in wheat. Theor Appl Gen 105:1038–1042
Febrer M, Wilhelm E, Al-Kaff N, Wright J, Powell W, Bevan MW, Boulton MI (2009) Rapid identification of the three homoeologues of the wheat dwarfing gene Rht using a novel PCR-based screen of three-dimensional BAC pools. Genome 52:993–1000
Feuillet C, Langridge P, Waugh R (2008) Cereal breeding takes a walk on the wild side. Trends Genet 24:24–32
Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209
Gale MD, Youssefian S (1985) Dwarfing genes in wheat. In: Russell GE (ed) Progress in plant breeding. Butterworth, London, pp 1–35
Gilbert J, Tekauz A (2000) Review: recent developments in research on Fusarium head blight of wheat in Canada. Can J Plant Pathol 22:1–8
Guedira M, Brown-Guedira G, Van Sanford D, Sneller C, Souza E, Marshall D (2010) Distribution of Rht genes in modern and historic winter wheat cultivars from the Eastern and Central USA. Crop Sci 50:1811–1822
Gulyas G, Bognar Z, Lang L, Rakszegi M, Bedo Z (2011) Distribution of dwarfing genes (Rht-B1b and Rht-D1b) in Martonvasar wheat breeding materials. Acta Agron Hung 59:249–254
Haseneyer G, Ravel C, Dardevet M, Balfourier F, Sourdille P, Charmet G, Brunel D, Sauer S, Geiger HH, Graner A, Stracke S (2008) High level of conservation between genes coding for the GAMYB transcription factor in barley (Hordeum vulgare L.) and bread wheat (Triticum aestivum L.) collections. Theor Appl Genet 117:321–331
Haudry A, Cenci A, Ravel C, Bataillon T, Brunel D, Poncet C, Hochu I, Poirier S, Santoni S, Glemin S, David J (2007) Grinding up wheat: a massive loss of nucleotide diversity since domestication. Mol Biol Evol 24:1506–1517
Hedden P (2003) The genes of the Green Revolution. Trends in Genet 19:5–9
Hilton AJ, Jenkinson P, Hollins TW, Parry DW (1999) Relationship between cultivar height and severity of Fusarium ear blight in wheat. Plant Path 48:202–208
Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Nat Acad Sci USA 99:8133–8138
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010
Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70
Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J 35:104–115
Knopf C, Becker H, Ebmeyer E, Korzun V (2008) Occurrence of three dwarfing Rht genes in German winter wheat varieties. Cer Res Comm 36:553–560
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Li Y, Bhosale S, Haussmann BIG, Stich B, Melchinger AE, Parzies HK (2010) Genetic diversity and linkage disequilibrium of two homologous genes to maize D8: sorghum SbD8 and pearl millet PgD8. J Plant Breed and Crop Sci 2:117–128
Li XP, Zhao XQ, He X, Zhao GY, Li B, Liu DC, Zhang AM, Zhang XY, Tong YP, Li ZS (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytol 189:449–458
Li Y, Xiao J, Wu J, Duan J, Liu Y, Ye X, Zhang X, Guo X, Gu Y, Zhang L, Jia J, Kong X (2012a) A tandem segmental duplication (TSD) in green revolution gene Rht-D1b region underlies plant height variation. New Phytol 196:282–291
Li A, Yang W, Guo X, Liu D, Sun J, Zhang A (2012b) Isolation of a gibberellin-insensitive dwarfing gene, Rht-B1e, and development of an allele-specific PCR marker. Mol Breeding 30:1443–1451
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129
McGrann GRD, Townsend BJ, Antoniw JF, Asher MJC, Mutasa-Goettgens ES (2009) Barley elicits a similar early basal defence response during host and non-host interactions with Polymyxa root parasites. Eur J of Plant Pathol 123:5–15
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nicholas KB, Nicholas HB (1997) GeneDoc: a tool for editing and annotation multiple sequence alignments. Distributed by the author (www.psc.edu/biomed/genedoc)
Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA, Al-Kaff N, Korolev A, Boulton MI, Phillips AL, Hedden P, Nicholson P, Thomas SG (2011) Molecular characterisation of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831
Peng JR, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45
Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WT, Macaulay M, MacKenzie K, Simpson C, Fuller J, Bonar N, Hayes PM, Lundqvist U, Franckowiak JD, Close TJ, Muehlbauer GJ, Waugh R (2011) INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1. Nature Genet 43:169–173
Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour F, Chalhoub B, Brunel D, Béckert M, Charmet G (2006) Single-nucleotide polymorphism frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139
Ravel C, Martre P, Romeuf I, Dardevet M, El-Malki R, Bordes J, Duchateau N, Brunel D, Balfourier F, Charmet G (2009) Polymorphism in the wheat transcriptional activator Spa influences its pattern of expression and has pleiotropic effects on grain protein composition, dough viscoelasticity, and grain hardness. Plant Physiol 151:2133–2144
Saville RJ, Gosman N, Burt CJ, Makepeace J, Steed A, Corbitt M, Chandler E, Brown JKM, Boulton MI, Nicholson P (2012) The ‘Green Revolution’ dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare. J Exp Bot 63:1271–1283
Smith SM, Yuan Y, Doust AN, Bennetzen JL (2012) Haplotype analysis and linkage disequilibrium at five loci in Eragrostis tef. Genes Genomes Genet 2:407–419
Srinivasachary, Gosman N, Steed A, Simmonds J, Leverington-Waite M, Wang Y, Snape J, Nicholson P (2008) Susceptibility to Fusarium head blight is associated with the Rht-D1b semi-dwarfing allele in wheat. Theor Appl Gen 116:1145–1153
Srinivasachary, Gosman N, Steed A, Hollins TW, Bayles R, Jennings P, Nicholson P (2009) Semi-dwarfing Rht-B1 and Rht-D1 loci of wheat differ significantly in their influence on resistance to Fusarium head blight. Theor Appl Genet 118:695–702
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Tian C, Wan P, Sun S, Li J, Chen M (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Molec Biol 54:519–532
Tosovic-Maric B, Kobiljski B, Obreht D, Vapa L (2008) Evaluation of wheat Rht genes using molecular markers. Genetika 40:31–38
Uchida N, Townsley B, Chung K-H, Sinha N (2007) Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proc Natl Acad Sci USA 104:15953–15958
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034
Wang H, Wang X, Chen P, Liu D (2007) Assessment of genetic diversity of Yunnan, Tibetan, and Xinjiang wheat using SSR markers. J of Genetics and Genomics 34:623–633
White J, Law JR, MacKay I, Chalmers KJ, Smith JSC, Kilian A, Powell W (2008) The genetic diversity of UK, US and Australian cultivars of Triticum aestivum measured by DArT markers and considered by genome. Theor Appl Gen 116:439–453
Wilhelm EP, Howells RM, Al-Kaff N, Jia J, Baker C, Leverington-Waite MA, Griffiths S, Greenland AJ, Boulton MI, Powell W (2013) Genetic characterization and mapping of the Rht-1 homoeologs and flanking sequences in wheat. Theor Appl Gen. doi:10.1007/s00122-013-2055-3
Wu J, Kong X, Wan J, Liu X, Zhang X, Guo X, Zhou R, Zhao G, Jing R, Fu X, Jia J (2011) Dominant and pleiotropic effects of a GAI gene in wheat results from a lack of interaction between DELLA and GID1. Plant Physiol 157:2120–2130
Yan W, Li HB, Cai SB, Ma HX, Rebetzke GJ, Liu CJ (2011) Effects of plant height on type I and type II resistance to fusarium head blight in wheat. Plant Path 60:506–512
Ye S, Dhillon S, Ke X, Collins AR, Day INM (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucl Acids Res 29(17):e88
Zhang X, Yang S, Zhou Y, He Z, Xia X (2006) Distribution of the Rht-B1b, Rht-D1b and Rht8 reduced height genes in autumn-sown Chinese wheats detected by molecular markers. Euphytica 152:109–116
Acknowledgments
We thank the NIAB trust for funding Ed Wilhelm’s research as part of a PhD, with assistance from the Biotechnology and Biological Sciences Research Council. We also thank the NIAB pre-breeding team, the NIAB horticultural staff, and the JIC horticultural staff for their assistance in growing plants, Jizeng Jia (Chinese Academy of Agricultural Sciences) for use of T. urartu sequence prior to publication, and Huw Jones (NIAB) for technical assistance with sequencing and critical review of the manuscript.
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Wilhelm, E.P., Mackay, I.J., Saville, R.J. et al. Haplotype dictionary for the Rht-1 loci in wheat. Theor Appl Genet 126, 1733–1747 (2013). https://doi.org/10.1007/s00122-013-2088-7
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DOI: https://doi.org/10.1007/s00122-013-2088-7