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Genetic analysis of developmental and adaptive traits in three doubled haploid populations of barley (Hordeum vulgare L.)

Abstract

Key message

Study of three interconnected populations identified 13 maturity QTL of which eight collocate with phenology genes, and 18 QTL for traits associated with adaptation to drought-prone environments.

Abstract

QTL for maturity and other adaptive traits affecting barley adaptation were mapped in a drought-prone environment. Three interconnected doubled haploid (DH) populations were developed from inter-crossing three Australian elite genotypes (Commander, Fleet and WI4304). High-density genetic maps were constructed using genotyping by sequencing and single nucleotide polymorphisms (SNP) for major phenology genes controlling photoperiod response and vernalization requirement. Field trials were conducted on the three DH populations in six environments at three sites in southern Australia and over two cropping seasons. Phenotypic evaluations were done for maturity, early vigour, normalized difference vegetation index (NDVI) and leaf chlorophyll content (SPAD), leaf waxiness and leaf rolling. Thirteen maturity QTL were identified, all with significant QTL × environment interaction with one exception. Eighteen QTL were detected for other adaptive traits across the three populations, including three QTL for leaf rolling, six for leaf waxiness, three for early vigour, four for NDVI, and two QTL for SPAD. The three interlinked populations with high-density linkage maps described in this study are a significant resource for examining the genetic basis for barley adaptation in low-to-medium rainfall Mediterranean type environments.

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References

  1. Adamski NM, Bush MS, Simmonds J, Turner AS, Mugford SG, Jones A, Findlay K, Pedentchouk N, von Wettstein-Knowles P, Uauy C (2013) The inhibitor of wax 1 locus (Iw1) prevents formation of beta- and OHbeta- diketones in wheat cuticular waxes and maps to a sub-cM interval on chromosome arm 2BS. Plant J 74:989–1002

  2. Ahn SJ, Costa J, Emanuel JR (1996) PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR. Nucleic Acids Res 24:2623–2625

  3. Alqudah AM, Sharma R, Pasam RK, Graner A, Kilian B, Schnurbusch T (2014) Genetic dissection of photoperiod response based on GWAS of pre-anthesis phase duration in spring barley. PLoS ONE 9:e113120

  4. Barr AR, Jefferies SP, Broughton S, Chalmers KJ, Kretschmer JM, Boyd WJR, Collins HM, Roumeliotis S, Logue SJ, Coventry SJ, Moody DM, Read BJ, Poulsen D, Lance RCM, Platz GJ, Park RF, Panozzo JF, Karakousis A, Lim P, Verbyla AP, Eckermann PJ (2003) Mapping and QTL analysis of the barley population Alexis × Sloop. Aust J Agric Res 54:1117–1123

  5. Bennett D, Izanloo A, Edwards J, Kuchel H, Chalmers K, Tester M, Reynolds M, Schnurbusch T, Langridge P (2012) Identification of novel quantitative trait loci for days to ear emergence and flag leaf glaucousness in a bread wheat (Triticum aestivum L.) population adapted to southern Australian conditions. Theor Appl Genet 124:697–711

  6. Bezant J, Laurie D, Practchett N, Hojecki J, Kearsey M (1996) Marker regression mapping of QTL controlling flowering time and plant height in a spring barley (Hordeum vulgare L.) cross. Heredity 77:64–73

  7. Black CA, Evans DD, White JL (1965) Methods of soil analysis—Part 1 physical and mineralogical properties, including statistics of measurement and sampling. American Society of Agronomy, Madison, Wisconsin

  8. Borràs-Gelonch G, Slafer G, Casas A, van Eeuwijk F, Romagosaa I (2010) Genetic control of pre-heading phases and other traits related to development in a double-haploid barley (Hordeum vulgare L.) population. Field Crops Res 119:36–47

  9. Boyd WR, Li C, Grime C, Cakir M, Potipibool S, Kaveeta L, Men S, Kamali M, Barr A, Moody D, Lance R, Logue S, Raman H, Read B (2003) Conventional and molecular genetic analysis of factors contributing to variation in the timing of heading among spring barley (Hordeum vulgare L.) genotypes grown over a mild winter growing season. Aust J Agric Res 54:1277–1301

  10. Broman K (2010) Genetic map construction with R/qtl. Revised 21 March 2012: edn. University of Wisconsin-Madison

  11. Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012) Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868–880

  12. Casao MC, Karsai I, Igartua E, Gracia MP, Veisz O, Casas AM (2011) Adaptation of barley to mild winters: a role for PPDH2. BMC Plant Biol 11:164

  13. Chen A, Baumann U, Fincher GB, Collins NC (2009) Flt-2L, a locus in barley controlling flowering time, spike density, and plant height. Funct Integr Genomics 9:243–254

  14. Cheverud JM (2001) A simple correction for multiple comparisons in interval mapping genome scans. Heredity 87:52–58

  15. Christiansen MW, Gregersen PL (2014) Members of the barley NAC transcription factor gene family show differential co-regulation with senescence-associated genes during senescence of flag leaves. J Exp Bot 65:4009–4022

  16. Clarke JM (1986) Effect of leaf rolling on leaf water loss in Triticum spp. Can J Plant Sci 66:885–891

  17. Cockram J, Jones H, Leigh FJ, O’Sullivan D, Powell W, Laurie DA, Greenland AJ (2007) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot 58:1231–1244

  18. Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal M, Shaw P, Bayer M, Thomas W, Marshall D, Hedley P, Tondelli A, Pecchioni N, Francia E, Korzun V, Walther A, Waugh R (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44:1388–1392

  19. Coventry J, Barr A, Eglinton J, McDonald G (2003) The determinants and genome locations influencing grain weight and size in barley (Hordeum vulgare L.). Aust J Agric Res 54:1103–1115

  20. Cullis BR, Smith AB, Coombes NE (2006) On the design of early generation variety trials with correlated data. J Agric Biol Environ Stat 11:381–393

  21. Deng W, Casao MC, Wang P, Sato K, Hayes PM, Finnegan EJ, Trevaskis B (2015) Direct links between the vernalization response and other key traits of cereal crops. Nat Commun 6:5882

  22. Dunford RP, Griffiths S, Christodoulou V, Laurie DA (2005) Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor Appl Genet 110:925–931

  23. 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

  24. Emebiri LC (2013) QTL dissection of the loss of green colour during post-anthesis grain maturation in two-rowed barley. Theor Appl Genet 126:1873–1884

  25. Febrero A, Fernandez S, Molina-Cano J, Araus J (1998) Yield, carbon isotope discrimination, canopy reflectance and cuticular conductance of barley isolines of differing glaucousness. J Exp Bot 49:1575–1581

  26. Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol 127:1676–1681

  27. González A, Ayerbe L (2009) Effect of terminal water stress on leaf epicuticular wax load, residual transpiration and grain yield in barley. Euphytica 172:341–349

  28. Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622

  29. 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

  30. Hanumappa M, Pratt LH, Cordonnier-Pratt M, Deitzer GF (1999) A photoperiod-insensitive barley line contains a light-labile phytochrome B. Plant Physiol 119:1033–1039

  31. Houston K, McKim SM, Comadran J, Bonar N, Druka I, Uzrek N, Cirillo E, Guzy-Wrobelska J, Collins NC, Halpin C, Hansson M, Dockter C, Druka A, Waugh R (2013) Variation in the interaction between alleles of HvAPETALA2 and microRNA172 determines the density of grains on the barley inflorescence. Proc Natl Acad Sci USA 110:16675–16680

  32. Kadioglu A, Terrzi R (2007) A dehydration avoidance mechanism: leaf rolling. Bot Rev 73:290–302

  33. Kikuchi R, Kawahigashi H, Ando T, Tonooka T, Handa H (2009) Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiol 149:1341–1353

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

  35. Kosová K, Vítámvás P, Urban MO, Kholová J, Prášil IT (2014) Breeding for enhanced drought resistance in barley and wheat–drought-associated traits, genetic resources and their potential utilization in breeding programs. Czech J Genet Plant Breed 50:247–261

  36. Langridge P, Barr A (2003) Preface. Aust J Agric Res 54:1–4

  37. Laurie D, Pratchett N, Bezant J, Snape J (1994) Genetic analysis of a photoperiod response gene on the short arm of chromosome 2 (2H) of Hordeum vulgare (barley). Heredity 72:619–627

  38. Laurie D, Pratchett N, Snape J, Bezant J (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L.) cross. Genome 38:575–585

  39. Le TP (2011) Genotyping of three parental barley lines and study of their mechanisms of tolerance to drought. Dissertation, University of Adelaide, South Australia

  40. Li J, Ji L (2005) Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity 95:221–227

  41. Liu L, Sun G, Ren X, Li C, Sun D (2015) Identification of QTL underlying physiological and morphological traits of flag leaf in barley. BMC Genet 16:29

  42. Long NR, Jefferies SP, Warner P, Karakousis A, Kretschmer JM, Hunt C, Lim P, Eckermann PJ, Barr AR (2003) Mapping and QTL analysis of the barley population Mundah × Keel. Aust J Agric Res 54:1163–1171

  43. Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215

  44. Marquez-Cedillo LA, Hayes PM, Kleinhofs A, Legge WG, Rossnagel BG, Sato K, Ullrich SE, Wesenberg DM, Project TNABGM (2001) QTL analysis of agronomic traits in barley based on the doubled haploid progeny of two elite North American varieties representing different germplasm groups. Theor Appl Genet 103:625–637

  45. Maydup ML, Graciano C, Guiamet JJ, Tambussi EA (2012) Analysis of early vigour in twenty modern cultivars of bread wheat (Triticum aestivum L.). Crop Pasture Sci 63:987

  46. Mimida N, Goto K, Kobayashi Y, Araki T, Ahn J, Weigel D, Murata M, Motoyoshi F, Sakamoto W (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6:327–336

  47. Nair SK, Wang N, Turuspekov Y, Pourkheirandish M, Sinsuwongwat S, Chen G, Sameri M, Tagiri A, Honda I, Watanabe Y, Kanamori H, Wicker T, Stein N, Nagamura Y, Matsumoto T, Komatsuda T (2010) Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc Natl Acad Sci USA 107:490–495

  48. O’Toole JC, Cruth RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432

  49. Pankin A, Campoli C, Dong X, Kilian B, Sharma R, Himmelbach A, Saini R, Davis S, Stein N, Schneeberger K, von Korff M (2014) Mapping-by-sequencing identifies HvPHYTOCHROME C as a candidate gene for the early maturity 5 locus modulating the circadian clock and photoperiodic flowering in barley. Genetics 198:383–396

  50. Pillen K, Zacharias A, Leon J (2003) Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107:340–352

  51. Poland J, Brown P, Sorrells M, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS ONE 7:e32253

  52. Rogowsky PM, Guider ELY, Langridge P, Shepherd KW, Koebner RMD (1991) Isolation and characterization of wheat–rye recombinants involving chromosome arm 1DS of wheat. Theor Appl Genet 82:537–544

  53. Szucs P, Karsai I, von Zitzewitz J, Meszaros K, Cooper LL, Gu YQ, Chen TH, Hayes PM, Skinner JS (2006) Positional relationships between photoperiod response QTL and photoreceptor and vernalization genes in barley. Theor Appl Genet 112:1277–1285

  54. Taylor J (2015) Linkage map construction using the MSTmap algorithm. p 36

  55. ter Steege MW, den Ouden FM, Lambers H, Stam P, Peeters AJ (2005) Genetic and physiological architecture of early vigour in Aegilops tauschii, the D-genome donor of hexaploid wheat. A quantitative trait loci analysis. Plant Physiol 139:1078–1094

  56. Thomas H, Howarth C (2000) Five ways to stay green. J Exp Bot 51:329–337

  57. Thomas H, Ougham H (2015) Senescence and crop performance. In: Sandras VO, Calderini DF (eds) Crop physiology: applications for genetic improvement and agronomy. Elsevier, Amsterdam, pp 223–249

  58. Tiyagi K, Park MR, Lee HJ, Lee CA, Rehman S, Steffenson B, Lee KJ, Yun SJ (2011) Diversity for seedling vigour in wild barley (Hordeum vulgare L. subsp. spontaneum) germplasm. Pak J Bot 43:2167–2173

  59. Trevaskis B, Hemming MN, Peacock WJ, Dennis ES (2006) HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol 140:1397–1405

  60. Trevaskis B, Hemming M, Dennis E, Peacock W (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

  61. Tsunewaki K, Ebana K (1999) Production of near-isogenic lines of common wheat for glaucousness and genetic basis of this trait clarified by their use. Genes Genet Syst 74:33–41

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

  63. von Wettstein P (1972) Genetic control of β-diketone and hydroxy-β-diketone synthesis in epicuticular waxes of barley. Planta 106:113–130

  64. Wang G, Schmalenbach I, von Korff M, Leon J, Kilian B, Rode J, Pillen K (2010) Association of barley photoperiod and vernalization genes with QTLs for flowering time and agronomic traits in a BC2DH population and a set of wild barley introgression lines. Theor Appl Genet 120:1559–1574

  65. Xue DW, Chen MC, Zhou MX, Chen S, Mao Y, Zhang GP (2008) QTL analysis of flag leaf in barley (Hordeum vulgare L.) for morphological traits and chlorophyll content. J Zhejiang Univ Sci B 9:938–943

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

  67. Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

  68. Zhou L, Ni E, Yang J, Zhou H, Liang H, Li J, Jiang D, Wang Z, Liu Z, Zhuang C (2013) Rice OsGL1-6 is involved in leaf cuticular wax accumulation and drought resistance. PLoS ONE 8:e65139

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Acknowledgments

The authors would like to thank Anthony Smith, Donna Marks and the Barley Program team, University of Adelaide, and Davis Leigh from Minnipa Agricultural Research Centre for providing unreserved assistance for the successful completion of the field trials. We also thank Daniel Carrocci, Florian Krimpzer and Thanh Phuoc Le for assisting in the SNP genotyping. This work is partially funded by the South Australia Grain Industry Trust Fund (SAGIT, UA 1202), Australian Research Council (ARC), Grains Research and Development Corporation (GRDC), the South Australian Government, the Department of Further Education, Employment, Science and Technology, and The University of Adelaide.

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Correspondence to Delphine Fleury.

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The authors declare that they have no conflict of interest.

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Communicated by T. Komatsuda.

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Obsa, B.T., Eglinton, J., Coventry, S. et al. Genetic analysis of developmental and adaptive traits in three doubled haploid populations of barley (Hordeum vulgare L.). Theor Appl Genet 129, 1139–1151 (2016). https://doi.org/10.1007/s00122-016-2689-z

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Keywords

  • Quantitative Trait Locus
  • Normalize Difference Vegetation Index
  • Double Haploid
  • Leaf Rolling
  • Double Haploid Population