Abstract
Multi-environment trials represent a highly valuable tool for the identification of the genetic bases of crop yield potential and stress adaptation. A Diversity Array Technology®-based barley map has been developed in the ‘Nure’ × ‘Tremois’ biparental Doubled Haploid population, harbouring the genomic position of a gene set with a putative role in the regulation of flowering time and abiotic stress response in barley. The population has been evaluated in eighteen location-by-year combinations across the Mediterranean basin. QTL mapping identified several genomic regions responsible for barley adaptation to Mediterranean conditions in terms of phenology, grain yield and yield component traits. The most frequently detected yield QTL had the early flowering HvCEN_EPS2 locus (chromosome 2H) as peak marker, showing a positive effect from the early winter parent ‘Nure’ in eight field trials, and explaining up to 45.8 % of the observed variance for grain yield. The HvBM5A_VRN-H1 locus on chromosome 5H and the genomic region possibly corresponding to PPD-H2 on chromosome 1H were significantly associated to grain yield in five and three locations, respectively. Environment-specific QTLs for grain yield, and clusters of yield component QTLs not related to phenology and or developmental genes (e.g. on chromosome 4H, BIN_09) were observed as well. The results of this work provide a valuable source of knowledge and tools for both explaining the genetic bases of barley yield adaptation across the Mediterranean basin, and using QTL-associated markers for MAS pre-breeding and breeding programmes.
Similar content being viewed by others
References
Acreche M, Briceño-Félix G, Martín Sánchez JA, Slafer GA (2008) Physiological bases of genetic gains in Mediterranean bread wheat yield in Spain. Eur J Agron 28:162–170
Aghnoum R, Marcel TC, Johrde A, Pecchioni N, Schweizer P, Niks RE (2010) Basal host resistance of barley to powdery mildew: connecting quantitative trait loci and candidate genes. Mol Plant Microbe Interact 23:91–102
Araus JL, Slafer GA, Reynolds MP, Royo C (2002) Plant breeding and drought in C3 cereals: what should we breed for? Ann Bot 89:925–940
Araus JL, Slafer GA, Royo C, Serret MD (2008) Breeding for yield potential and stress adaptation in cereals. Crit Rev Plant Sci 27:1–36
Baum M, Grando S, Backes G, Jahoor A, Sabbagh A, Ceccarelli S (2003) QTLs for agronomic traits in the Mediterranean environment identified in recombinant inbred lines of the cross ‘Arta’ × H. spontaneum 41–1. Theor Appl Genet 107:1215–1225
Bolle H-J (2003) Climate, climate variability, and impacts in the Mediterranean Area: an overview. In: Bolle H-J (ed) Mediterranean climate: variability and trends. Springer, Berlin, pp 5–86
Borràs-Gelonch G, Slafer GA, Casas AM, van Eeuwijk F, Romagosa I (2010) Genetic control of pre-heading phases and other traits related to development in a double-haploid barley (Hordeum vulgare L.) population. Field Crop Res 119:36–47
Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Mare C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14
Ceccarelli S (1989) Wide adaptation. How wide? Euphytica 40:197–205
Ceccarelli S, Grando S (1991) Selection environment and environmental sensitivity in barley. Euphytica 57:157–167
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
Comadran J, Russell JR, van Eeuwijk FA, Ceccarelli S, Grando S, Baum M, Stanca AM, Pecchioni N, Mastrangelo AM, Akar T, Al-Yassin A, Benbelkacem A, Choumane W, Ouabbou H, Dahan R, Bort J, Araus J-L, Pswarayi A, Romagosa I, Hackett CA, Thomas WTB (2008) Mapping adaptation of barley to droughted environments. Euphytica 161:35–45
Comadran J, Thomas WT, van Eeuwijk FA, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A, Benbelkacem A, Ouabbou H, Bort J, Romagosa I, Hackett CA, Russell JR (2009) Patterns of genetic diversity and linkage disequilibrium in a highly structured Hordeum vulgare association-mapping population for the Mediterranean basin. Theor Appl Genet 119:175–187
Comadran J, Russell JR, Booth A, Pswarayi A, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A, Benbelkacem A, Ouabbou H, Bort J, van Eeuwijk FA, Thomas WT, Romagosa I (2011) Mixed model association scans of multi-environmental trial data reveal major loci controlling yield and yield related traits in Hordeum vulgare in Mediterranean environments. Theor Appl Genet 122:1363–1373
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 CENTRODIALIS contributed to spring growth habit and environmental adaptation in barley. Nat Genet 44:1388–1392
Cuesta-Marcos A, Casas AM, Hayes PM, Gracia MP, Lasa JM, Ciudad F, Codesal P, Molina-Cano JL, Igartua E (2008a) Yield QTL affected by heading date in Mediterranean grown barley. Plant Breed 128:46–53
Cuesta-Marcos A, Igartua E, Ciudad FJ, Codesal P, Russell JR, Molina-Cano JL, Moralejo M, Szűcs P, Gracia MP, Lasa JM, Casas AM (2008b) Heading date QTL in a spring × winter barley cross evaluated in Mediterranean environments. Mol Breed 21:455–471
Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184
Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176:599–609
Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Toth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680
Francia E, Barabaschi D, Tondelli A, Laido G, Rizza F, Stanca AM, Busconi M, Fogher C, Stockinger EJ, Pecchioni N (2007) Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091
Francia E, Tondelli A, Rizza F, Badeck FW, Li Destri O, Akar T, Grando S, Al-Yassin A, Benbelkacem A, Thomas WTB, van Eeuwijk F, Romagosa I, Stanca AM, Pecchioni N (2011) Determinants of barley grain yield in a wide range of Mediterranean environments. Field Crop Res 120:169–178
Francia E, Tondelli A, Rizza F, Badeck FW, Thomas WTB, van Eeuwijk F, Romagosa I, Stanca AM, Pecchioni N (2013) Determinants of barley grain yield in drought-prone Mediterranean environments. Ital J Agron 8:e1
Higgins JA, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5:e10065
Horsley RD, Schmierer D, Maier C et al (2006) Identification of QTLs associated with Fusarium head blight resistance in barley accession CIho 4196. Crop Sci 46:145–156
Igartua E, Casas AM, Ciudad F, Montoya JL, Romagosa I (1999) RFLP markers associated with major genes controlling heading date evaluated in a barley germplasm pool. Heredity 83:551–559
Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35
Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134:74–86
Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 104:1424–1429
Lacaze X, Hayes PM, Korol A (2009) Genetics of phenotypic plasticity: QTL analysis in barley, Hordeum vulgare. Heredity 102:163–173
Laurie DA, Pratchett N, Benzant JH, Snape JW (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
Lewis S, Faricelli ME, Appendino ML, Valárik M, Dubcovsky J (2008) The chromosome region including the earliness per se locus Eps-Am 1 affects the duration of early developmental phases and spikelet number in diploid wheat. J Exp Bot 59:3595–3607
Mayer KFX, Waugh R, Langridge P, Close TJ, Wise RP, Graner A, Matsumoto T, Sato K, Schulman AGH, Muehlbauer GJ et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716
Payne RW, Harding SA, Murray DA, Soutar DM, Baird DB, Welham SJ, Kane AF, Gilmour AR, Thompson R, Webster R, Wilson GT (2008) GenStat release 11 reference manual, part 2 directives. VSN International, Hemel Hempstead
Pecchioni N, Milc J, Pasquariello M, Francia E (2012) Barley: Omics approaches for abiotic stress tolerance. In: Tuteja N, Gill SS, Tubercio AF, Tuteja R (eds) Improving crop resistance to abiotic stress, vol 2. Wiley, Weinheim, pp 779–884
Pswarayi A, van Eeuwijk FA, Ceccarelli S, Grando S, Comadran J, Russell JR, Pecchioni N, Tondelli A, Akar T, Al-Yassin A, Benbelkacem A, Ouabbou H, Thomas WTB, Romagosa I (2008a) Changes in allele frequencies in landraces, old and modern barley cultivars of marker loci close to QTL for grain yield under high and low input conditions. Euphytica 163:435–447
Pswarayi A, van Eeuwijk FA, Ceccarelli S, Grando S, Comadran J, Russell JR, Francia E, Pecchioni N, Li Destri O, Akar T, Al-Yassin A, Benbelkacem A, Choumane W, Karrou M, Ouabbou H, Bort J, Araus JL, Molina-Cano JL, Thomas WTB, Romagosa I (2008b) Barley adaptation and improvement in the Mediterranean basin. Plant Breed 127:554–560
Ramsay L, Comadran J, Druka A, Marshall DF, Thomas WTB, 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. Nat Genet 43:169–172
Reynolds M, Foulkes MJ, Slafer G, Berry P, Parry MAJ, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60:1899–1918
Rizza F, Badeck FW, Cattivelli L, Li Destri O, Di Fonzo N, Stanca AM (2004) Use of a water stress index to identify barley genotypes adapted to rainfed and irrigated conditions. Crop Sci 44:2127–2137
Rostoks N, Mudie S, Cardle L, Russell J, Ramsay L, Booth A, Svensson J, Wanamaker S, Walia H, Rodriguez E, Hedley P, Liu H, Morris J, Close T, Marshall D, Waugh R (2005) Genome-wide SNP discovery and linkage analysis in barley based on genes responsive to abiotic stress. Mol Genet Genomics 274:515–527
Sato K, Nankaku N, Takeda K (2009) A high density transcript linkage map of barley derived from a single population. Heredity 103:110–117
Schmitz J, Franzen R, Ngyuen TH, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (2000) Cloning, mapping and expression analysis of barley MADS-box genes. Plant Mol Biol 42:899–913
Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551
Slafer GA, Araus JL, Royo C, Del Moral LFG (2005) Promising eco-physiological traits for genetic improvement of cereal yields in Mediterranean environments. Ann Appl Biol 146:61–70
Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, Perovic D, Grosse I, Graner A (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114:823–839
Szűcs P, Blake VC, Bhat PR, Chao S, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay L, Waugh R, Hayes PM (2009) An integrated resource for barley linkage map and malting quality QTL alignment. Plant Genome 2:134–140
Talamé V, Sanguineti MC, Chiapparino E, Bahri H, Salem MB, Forster BP, Ellis RP, Rhouma S, Zoumarou W, Waugh R, Tuberosa R (2004) Identification of Hordeum spontaneum QTL alleles improving field performance of barley grown under rainfed conditions. Ann Appl Biol 144:309–319
Tambussi EA, Nogues S, Ferrio P, Voltas J, Araus JL (2005) Does higher yield potential improve barley performance in Mediterranean conditions? a case of study. Field Crop Res 91:149–160
Teulat B, Merah O, Souyris I, This D (2001) QTLs for agronomic traits from Mediterranean barley progeny grown in several environments. Theor Appl Genet 103:774–787
Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454
Tuberosa R, Salvi S (2006) Genomics-based approaches to improve drought tolerance of crops. Trends Plant Sci 11:405–412
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
Van Ooijen JW (2004) MapQTL®5, software for the mapping of quantitative trait loci in experimental populations. Kyazma BV, Wageningen
Van Ooijen JW (2006) JoinMap®4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen
von Korff M, Grando S, Del Greco A, This D, Baum M, Ceccarelli S (2008) Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theor Appl Genet 117:653–669
von Zitzewitz J, Szucs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen THH, Hayes PM, Skinner JS (2005) Structural and functional characterization of barley vernalization genes. Plant Mol Biol 59:449–467
Wang G, Schmalenbach I, von Korff M, Léon 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
Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinjofs A, Killian A (2004) Diversity arrays technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920
Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesna J, Cakir M, Poulsen D, Wang J, Raman R, Smith K, Muehlbauer GJ, Chalmers KJ, Kleinhofs A, Huttner E, Killian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and phenotypic traits. BMC Genom 7:206
Xu S (2008) Quantitative trait locus mapping can benefit from segregation distortion. Genetics 180:2201–2208
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
Acknowledgments
This work was supported by EU INCO-MED Project MABDE No. ICA3-2002-10073. We would like to thank Nikolai Christov (AgroBioinstitute, Sofia) for supplying sequences of wca11a2 clone, and Hans Jansen (Biometris-Applied Statistics, Wageningen University and Research Centre) for the useful suggestions during map construction.
Author information
Authors and Affiliations
Corresponding author
Additional information
A. Tondelli and E. Francia have contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tondelli, A., Francia, E., Visioni, A. et al. QTLs for barley yield adaptation to Mediterranean environments in the ‘Nure’ × ‘Tremois’ biparental population. Euphytica 197, 73–86 (2014). https://doi.org/10.1007/s10681-013-1053-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-013-1053-5