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Effects of Rht-B1 and Ppd-D1 loci on pollinator traits in wheat

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Abstract

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Elite wheat pollinators are critical for successful hybrid breeding. We identified Rht-B1 and Ppd-D1 loci affecting multiple pollinator traits and therefore represent major targets for improving hybrid seed production.

Abstract

Hybrid breeding has a great potential to significantly boost wheat yields. Ideal male pollinators would be taller in stature, contain many spikelets well-spaced along the spike and exhibit high extrusion of large anthers. Most importantly, flowering time would match with that of the female parent. Available genetic resources for developing an elite wheat pollinator are limited, and the genetic basis for many of these traits is largely unknown. Here, we report on the genetic analysis of pollinator traits using biparental mapping populations. We identified two anther extrusion QTLs of medium effect, one on chromosome 1BL and the other on 4BS coinciding with the semi-dwarfing Rht-B1 locus. The effect of Rht-B1 alleles on anther extrusion is genotype dependent, while tall plant Rht-B1a allele is consistently associated with large anthers. Multiple QTLs were identified at the Ppd-D1 locus for anther length, spikelet number and spike length, with the photoperiod-sensitive Ppd-D1b allele associated with favourable pollinator traits in the populations studied. We also demonstrated that homeoloci, Rht-D1 and Ppd-B1, influence anther length among other traits. These results suggest that combinations of Rht-B1 and Ppd-D1 alleles control multiple pollinator traits and should be major targets of hybrid wheat breeding programs.

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References

  • Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–1056

    Article  CAS  PubMed  Google Scholar 

  • Alghabari F, Lukac M, Jones HE, Gooding MJ (2014) Effect of Rht alleles on the tolerance of wheat grain set to high temperature and drought stress during booting and anthesis. J Agron Crop Sci 200:36–45

    Article  CAS  Google Scholar 

  • Beales J, Turner A, GriYths S, Snape JW, Laurie DA (2007) A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733

    Article  CAS  PubMed  Google Scholar 

  • Binghua L, Jingyang D (1986) A dominant gene for male-sterility in wheat. Plant Breed 97:204–209

    Article  Google Scholar 

  • Boden SA, Cavanagh C, Cullis BR, Ramm K, Greenwood J, Jean Finnegan E, Trevaskis B, Swain SM (2015) Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nat Plants 1:14016

    Article  CAS  PubMed  Google Scholar 

  • Boeven PHG, Longin CFH, Leiser WL, Kollers S, Ebmeyer E, Wurschum T (2016) Genetic architecture of male floral traits required for hybrid wheat breeding. Theor Appl Genet 129:2343–2357

    Article  PubMed  Google Scholar 

  • Boeven PHG, Würschum T, Rudloff J, Ebmeyer E, Longin CFH (2018) Hybrid seed set in wheat is a complex trait but can be improved indirectly by selection for male floral traits. Euphytica 214:110

    Article  CAS  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  Google Scholar 

  • Buerstmayr M, Buerstmayr H (2015) Comparative mapping of quantitative trait loci for Fusarium head blight resistance and anther retention in the winter wheat population Capo × Arina. Theor Appl Genet 128:1519–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buerstmayr M, Buerstmayr H (2016) The semidwarfing alleles Rht-D1b and Rht-B1b show marked differences in their associations with anther-retention in wheat heads and with Fusarium head blight susceptibility. Phytopathology 106:1544–1552

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daviere JM, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9:10–20

    Article  CAS  PubMed  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184

    Article  CAS  PubMed  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2015) Statistical pocketbook world food and agriculture 2015. Food and Agriculture Organization of the United Nations. http://www.fao.org/3/a-i4691e.pdf. Accessed 25 Nov 2018

  • Ghanem ME, Marrou H, Sinclair TR (2015) Physiological phenotyping of plants for crop improvement. Trends Plant Sci 20:139–144

    Article  CAS  PubMed  Google Scholar 

  • Gilmour A, Gogel B, Cullis B, Thompson R (2009) ASReml user guide release 3.0. VSN International Ltd. https://www.vsni.co.uk/downloads/asreml/release3/UserGuide.pdf. Accessed 25 Nov 2018

  • Gils M, Kempe K, Boudichevskaia A, Jerchel R, Pescianschi D, Schmidt R, Kirchhoff M, Schachschneider R (2013) Quantitative assessment of wheat pollen shed by digital image analysis of trapped airborne pollen grains. Adv Crop Sci Technol 2:119

    Google Scholar 

  • Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855–1867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Z, Song Y, Zhou R, Ren Z, Jia J (2010) Discovery, evaluation and distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol 185:841–851

    Article  CAS  PubMed  Google Scholar 

  • Halliwell J, Borrill P, Gordon A, Kowalczyk R, Pagano ML, Saccomanno B, Bentley AR, Uauy C, Cockram J (2016) Systematic investigation of FLOWERING LOCUS T-like Poaceae gene families identifies the short-day expressed flowering pathway gene, TaFT3 in wheat (Triticum aestivum L.). Plant Sci 7:857

    Google Scholar 

  • He X, Lillemo M, Shi JR, Wu JR, Bjornstad A, Belova T, Dreisigacker S, Duveiller E, Singh P (2016a) QTL characterization of Fusarium head blight resistance in CIMMYT bread wheat line Soru#1. PLoS ONE 11:e0158052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He X, Singh PK, Dreisigacker S, Singh S, Lillemo M, Duveiller E (2016b) Dwarfing genes Rht-B1b and Rht-D1b are associated with both Type I FHB susceptibility and low anther extrusion in two bread wheat populations. PLoS ONE 11:e0162499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • International Wheat Genome Sequencing C (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191

    Article  CAS  Google Scholar 

  • Jimenez-Berni JA, Deery DM, Rozas-Larraondo P, Condon ATG, Rebetzke GJ, James RA, Bovill WD, Furbank RT, Sirault XRR (2018) High throughput determination of plant height, ground cover, and above-ground biomass in wheat with LiDAR. Front Plant Sci 9:237

    Article  PubMed  PubMed Central  Google Scholar 

  • Kneipp J (2017) Control of Fusarium head blight in northern NSW. https://grdc.com.au/research/reports/report?id=1916. Accessed 25 Nov 2018

  • Kosuge K, Watanabe N, Kuboyama T, Melnik VM, Yanchenko VI, Rosova MA, Goncharov NP (2008) Cytological and microsatellite mapping of mutant genes for spherical grain and compact spikes in durum wheat. Euphytica 159:289–296

    Article  CAS  Google Scholar 

  • Kowalski AM, Gooding M, Ferrante A, Slafer GA, Orford S, Gasperini D, Griffiths S (2016) Agronomic assessment of the wheat semi-dwarfing gene Rht8 in contrasting nitrogen treatments and water regimes. Field Crops Res 191:150–160

    Article  PubMed  PubMed Central  Google Scholar 

  • Langer SM, Longin CFH, Wurschum T (2014) Phenotypic evaluation of floral and flowering traits with relevance for hybrid breeding in wheat (Triticum aestivum L.). Plant Breed 133:433–441

    Article  Google Scholar 

  • Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longin CFH, Muhleisen J, Maurer HP, Zhang HL, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096

    Article  PubMed  Google Scholar 

  • Longin CF, Gowda M, Muhleisen J, Ebmeyer E, Kazman E, Schachschneider R, Schacht J, Kirchhoff M, Zhao Y, Reif JC (2013) Hybrid wheat: quantitative genetic parameters and consequences for the design of breeding programs. Theor Appl Genet 126:2791–2801

    Article  PubMed  Google Scholar 

  • Lu Q, Lillemo M, Skinnes H, He X, Shi J, Ji F, Dong Y, Bjornstad A (2013) Anther extrusion and plant height are associated with Type I resistance to Fusarium head blight in bread wheat line ‘Shanghai-3/Catbird’. Theor Appl Genet 126:317–334

    Article  CAS  PubMed  Google Scholar 

  • Manske GGB, Ortiz-Monasterio JI, van Ginkel RM, Rajaram S, Vlek PLG (2002) Phosphorus use efficiency in tall, semi-dwarf and dwarf near-isogenic lines of spring wheat. Euphytica 125:113–119

    Article  CAS  Google Scholar 

  • Miedaner T, Schulthess AW, Gowda M, Reif JC, Longin CF (2017) High accuracy of predicting hybrid performance of Fusarium head blight resistance by mid-parent values in wheat. Theor Appl Genet 130:461–470

    Article  CAS  PubMed  Google Scholar 

  • Milohnic J, Jost M (1970) Pollen production and anther extrusion of wheat (Triticum aestivum L. Em Thell.). Acta Agron Acad Sci Hung 19:17–23

    Google Scholar 

  • Mulki MA, Bi X, von Korff M (2018) FLOWERING LOCUS T3 controls spikelet initiation but not floral development. Plant Physiol 178:1170–1186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muqaddasi QH, Lohwasser U, Nagel M, Borner A, Pillen K, Roder MS (2016) Genome-wide association mapping of anther extrusion in hexaploid spring wheat. PLoS ONE 11:e0155494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muqaddasi QH, Brassac J, Borner A, Pillen K, Roder MS (2017a) Genetic architecture of anther extrusion in spring and winter wheat. Front Plant Sci 8:754

    Article  PubMed  PubMed Central  Google Scholar 

  • Muqaddasi QH, Pillen K, Plieske J, Ganal MW, Roder MS (2017b) Genetic and physical mapping of anther extrusion in elite European winter wheat. PLoS ONE 12:e0187744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemoto Y, Kisaka M, Fuse T, Yano M, Ogihara Y (2003) Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J 36:82–93

    Article  CAS  PubMed  Google Scholar 

  • Nguyen V, Fleury D, Timmins A, Laga H, Hayden M, Mather D, Okada T (2015) Addition of rye chromosome 4R to wheat increases anther length and pollen grain number. Theor Appl Genet 128:953–964

    Article  CAS  PubMed  Google Scholar 

  • Okada T, Whitford R (2019) Hybrid wheat and abiotic stress. In: Rajpal VR, Sehgal D, Kumar A, Raina SN (eds) Genomics assisted breeding of crops for abiotic stress tolerance, vol 2. Sustainable development and biodiversity 21. Springer, Switzerland. https://doi.org/10.1007/978-3-319-99573-1_12

  • Okada T, Jayasinghe J, Nansamba M, Baes M, Warner P, Kouidri A, Correia D, Nguyen V, Whitford R, Baumann U (2018) Unfertilized ovary pushes wheat flower open for cross-pollination. J Exp Bot 69:399–412

    Article  CAS  PubMed  Google Scholar 

  • 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 characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, 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

    Article  CAS  PubMed  Google Scholar 

  • Pickett A (1993) Hybrid wheat results and problems. Paul Parey Scientific, Berlin

    Google Scholar 

  • Poland J, Endelman J, Dawson J, Rutkoski J, Wu SY, Manes Y, Dreisigacker S, Crossa J, Sanchez-Villeda H, Sorrells M, Jannink JL (2012) Genomic selection in wheat breeding using genotyping-by-sequencing. Plant Genome 5:103–113

    Article  CAS  Google Scholar 

  • Rebetzke GJ, Richards RA, Fettell NA, Long M, Condon AG, Forrester RI, Botwright TL (2007) Genotypic increases in coleoptile length improves stand establishment, vigour and grain yield of deep-sown wheat. Field Crops Res 100:10–23

    Article  Google Scholar 

  • Richards RA (1992) The effect of dwarfing genes in spring wheat in dry environments. 1. Agronomic characteristics. Aust J Agric Res 43:517–527

    Article  Google Scholar 

  • Rogowsky PM, Sorrels ME, Shepherd KW, Langridge P (1993) Characterization of wheat-rye recombinants with RFLP and PCR probes. Theor Appl Genet 85:1023–1028

    Article  CAS  PubMed  Google Scholar 

  • RStudio_Team (2015) RStudio: integrated development for R. RStudio, Inc. http://www.rstudio.com/. Accessed 25 Nov 2018

  • Sasakuma T, Maan SS, Williams ND (1978) EMS-induced male-sterile mutants in euplasmic and alloplasmic common wheat. Crop Sci 18:850–853

    Article  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) FIJI: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    Article  CAS  PubMed  Google Scholar 

  • Shaw LM, Turner AS, Laurie DA (2012) The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J 71:71–84

    Article  CAS  PubMed  Google Scholar 

  • Skinnes H, Semagn K, Tarkegne Y, Maroy AG, Bjornstad A (2010) The inheritance of anther extrusion in hexaploid wheat and its relationship to Fusarium head blight resistance and deoxynivalenol content. Plant Breed 129:149–155

    Article  CAS  Google Scholar 

  • Song X, Feng J, Cui Z, Zhang C, Sun D (2018) Genome-wide association study for anther length in some elite bread wheat germplasm. Czech J Genet Plant Breed 54:109–114

    Article  Google Scholar 

  • Tanio M, Kato K (2007) Development of near-isogenic lines for photoperiod-insensitive genes, Ppd-B1 and Ppd-D1, carried by the Japanese wheat cultivars and their effect on apical development. Breed Sci 57:65–72

    Article  Google Scholar 

  • Taylor J, Butler D (2017) R package ASMap: efficient genetic linkage map construction and diagnosis. J Stat Softw 79:1–29

    Article  Google Scholar 

  • Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822

    Article  CAS  PubMed  Google Scholar 

  • Tricker PJ, ElHabti A, Schmidt J, Fleury D (2018) The physiological and genetic basis of combined drought and heat tolerance in wheat. J Exp Bot 69:3195–3210

    Article  CAS  PubMed  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • VSN_International (2011) GenStat for windows, 14th edn. VSN International, Hemel Hempstead

    Google Scholar 

  • Whitford R, Fleury D, Reif JC, Garcia M, Okada T, Korzun V, Langridge P (2013) Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64:5411–5428

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm EP, Boulton MI, Al-Kaff N, Balfourier F, Bordes J, Greenland AJ, Powell W, Mackay IJ (2013) Rht-1 and Ppd-D1 associations with height, GA sensitivity, and days to heading in a worldwide bread wheat collection. Theor Appl Genet 126:2233–2243

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson PA, Winfield MO, Barker GLA, Allen AM, Burridge A, Coghill JA, Edwards KJ (2012) CerealsDB 2.0: an integrated resource for plant breeders and scientists. BMC Bioinformatics 13:219

    Article  PubMed  PubMed Central  Google Scholar 

  • Würschum T, Liu G, Boeven PHG, Longin CFH, Mirdita V, Kazman E, Zhao Y, Reif JC (2018) Exploiting the Rht portfolio for hybrid wheat breeding. Theor Appl Genet 131:1433–1442

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586

    Article  CAS  PubMed  Google Scholar 

  • Youssefian S, Kirby EJM, Gale MD (1992) Pleiotropic effects of the Ga-Insensitive Rht dwarfing genes in wheat. 2. Effects on leaf, stem, ear and floret growth. Field Crops Res 28:179–190

    Article  Google Scholar 

  • Zadoks JC, Chang TT, Konzak CF (1974) Decimal code for growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhang XK, Xiao YG, Zhang Y, Xia XC, Dubcovsky J, He ZH (2008) Allelic variation at the vernalization genes Vrn-A1, Vrn-B1, Vrn-D1, and Vrn-B3 in Chinese wheat cultivars and their association with growth habit. Crop Sci 48:458–470

    Article  CAS  Google Scholar 

  • Zhao Y, Li Z, Liu G, Jiang Y, Maurer HP, Wurschum T, Mock HP, Matros A, Ebmeyer E, Schachschneider R, Kazman E, Schacht J, Gowda M, Longin CF, Reif JC (2015) Genome-based establishment of a high-yielding heterotic pattern for hybrid wheat breeding. Proc Natl Acad Sci USA 112:15624–15629

    CAS  PubMed  Google Scholar 

  • Zhao XY, Hong P, Wu JY, Chen XB, Ye XG, Pan YY, Wang J, Zhang XS (2016) The tae-miR408-mediated control of TaTOC1 genes transcription is required for the regulation of heading time in wheat. Plant Physiol 170:1578–1594

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by DuPont—Pioneer Hi-Bred International. We thank David Correia, Yuriy Onyskiv, Vy Nguyen, Alex Kovalchuk and Dr Ursula Langridge for assisting with glasshouse work. We also thank Drs Radoslaw Suchecki and Beata Sznajder for data analysis and Dr. Ajay Sandhu for critical advice for the project. We also thank Margaret Pallotta for technical advice and critical reading and editing of the manuscript.

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Correspondence to Takashi Okada.

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Effect of severe dwarf (SD) on pollinator traits and data analysis including SD plants (PDF 546 kb)

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Table S1.

KASPTM markers used for developing genetic linkage map for populations #1 and #2. Table S2. GBS markers used for developing genetic linkage map for population #1. Table S3. GBS markers used for developing genetic linkage map for population #2. Table S4. Summary information for genetic linkage map and QTL analysis for population #1 and #2. Table S5. A list of genetic loci associated with anther extrusion reported in the previous publications. Table S6. Phenology genes mapped on Chinese Spring reference sequence IWGSC RefSeq v1.0 to compare physical location of genetic loci associated with pollinator traits. Table S7. Summary statistics for evaluated traits in Rht-1 and Ppd-1 NILs used in this study. Table S8. Physical location of AE loci and flowering time (FT) or plant/floral architecture (FA) genes/loci in CS reference map IWGSC RefSeq v1.0 (XLSX 483 kb)

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Okada, T., Jayasinghe, J.E.A.R.M., Eckermann, P. et al. Effects of Rht-B1 and Ppd-D1 loci on pollinator traits in wheat. Theor Appl Genet 132, 1965–1979 (2019). https://doi.org/10.1007/s00122-019-03329-w

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