Abstract
Key message
Spring growth in barley controlled by natural variation at Vrn-H1 and Vrn-H2 improved yield stability in marginal Syrian environments.
Abstract
The objective of the present study was to identify QTL influencing agronomic performance in rain-fed Mediterranean environments in a recombinant inbred line (RIL) population, ARKE derived from the Syrian barley landrace, Arta and the Australian feed cultivar, Keel. The population was field tested for agronomic performance at two locations in Syria for 4 years with two sowing dates, in autumn and winter. Genotypic variability in yield of the RIL population was mainly affected by year-to-year variation presumably caused by inter-annual differences in rainfall distribution. The spring growth habit and early flowering inherited from the Australian cultivar Keel increased plant height and biomass and improved yield stability in Syrian environments. QTL for yield and biomass coincided with the map location of flowering time genes, in particular the vernalisation genes Vrn-H1 and Vrn-H2. In marginal environments with terminal drought, the Vrn-H1 allele inherited from Keel improved final biomass and yield. Under changing climate conditions, such as shorter winters, reduced rainfall, and early summer drought, spring barley might thus outperform the traditional vernalisation-sensitive Syrian landraces. We present the ARKE population as a valuable genetic resource to further elucidate the genetics of drought adaptation of barley in the field.
Similar content being viewed by others
References
Acevedo E, Craufurd P, Austin R, Perez-Marco P (1991) Traits associated with high yield in barley in low-rainfall environments. J Agric Sci 116:23–36
Alsop BP, Farre A, Wenzl P, Wang JM, Zhou MX, Romagosa I, Kilian A, Steffenson BJ (2011) Development of wild barley-derived DArT markers and their integration into a barley consensus map. Mol Breed 27:77–92
Atlin GN, Frey KJ (1990) Selecting oat lines for yield in low-productivity environments. Crop Sci 30:556–561
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
Baum M, von Korff M, Guo P, Lakew B, Udupa SM, Sayed H, Choumane W, Grando S, Ceccarelli S (2007) Molecular approaches and breeding strategies for drought tolerance in barley. In: Varshney R, Tuberosa R (eds) Genomic assisted crop improvement: vol 2. Genomics applications in Crops, Springer Netherlands, pp 51–79
Blum A (1996) Crop responses to drought and the interpretation of adaptation. J Plant Growth Regul 20:135–148
Borràs-Gelonch G, Denti M, Thomas WTB, Romagosa I (2011a) Genetic control of pre-heading phases in the Steptoe × Morex barley population under different conditions of photoperiod and temperature. Euphytica. doi:10.1007/s10681-011-0526-7
Borràs-Gelonch G, Rebetzke G, Richards R, Romagosa I (2011b) Genetic control of duration of pre-anthesis phases in wheat (Triticum aestivum L.) and relationships to leaf appearance, tillering and dry matter accumulation. J Exp Bot. doi:10.1093/jxb/err230v
Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012a) Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868–880
Campoli C, Shtaya M, Davis SJ, von Korff M (2012b) Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biol 12:97
Casao MC, Igartua E, Karsai I, Lasa JM, Gracia MP, Casas AM (2011a) Expression analysis of vernalization and day length response genes in barley (Hordeum vulgare L.) indicates that VRNH2 is a repressor of PPDH2 (HvFT3) under long days. J Exp Bot 62:1939–1949
Casao MC, Karsai I, Igartua E, Gracia MP, Veisz O, Casas AM (2011b) Adaptation of barley to mild winters: a role for PPDH2. BMC Plant Biol 11:164
Casas AM, Djemel A, Ciudad FJ, Yahiaoui S, Ponce LJ, Contreras-Moreira B, Gracia MP, Lasa JM, Igartua E (2011) HvFT1 (VrnH3) drives latitudinal adaptation in Spanish barleys. Theor Appl Genet 112:1293–1304
Ceccarelli S (1989) Wide adaptation. How wide? Euphytica 40:197–205
Ceccarelli S, Grando S, Hamblin J (1992) Relationship between barley grain yield measured in low- and high yielding environments. Euphytica 64:49–58
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(2):243–254
Cockram J, Chiapparino E, Taylor SA, Stamati K, Donini P, Laurie DA, O’Sullivan DM (2007) Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype. Theor Appl Genet 115:993–1001
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, Russell JR, Booth A, Pswarayi A, Ceccarelli S, Grando S, Stanca AM, Pecchioni N, Akar T, Al-Yassin A (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(7):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 Centroradialis contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44:1388–1392
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033
Coventry SJ, Baum M, Sayed H, Grando S, Ceccarelli S, Barr AR, Eglinton JK (2004)The genetic basis of adaptation to low rainfall environments in Australia. In: Proceedings of the 9th international barley genetics symposium
Cseri A, Cserhati M, von Korff M, Nagy B, Horvath GV, Palagyi A, Pauk J, Dudits D, Toerjek O (2011) Allele mining and haplotype discovery in barley candidate genes for drought tolerance. Euphytica 181(3):341–356
Cuesta-Marcos A, Igartua E, Ciudad FJ, Codesal P, Russell JR, Molina-Cano JL, Moralejo M, Szűcs P, Gracia MP, Lasa JM, Casas AM (2008) Heading date QTL in a spring × winter barley cross evaluated in Mediterranean environments. Mol Breed 21:455–471
Cuesta-Marcos A, Casas AM, Hayes PM, Gracia MP, Lasa JM, Ciudad F, Codesal P, Molina-Cano JL, Igartua E (2009) Yield QTL affected by heading date in Mediterranean barley. Plant Breed 128:46–53
Dhillon T, Pearce SP, Stockinger EJ, Distelfeld A, Li C, Knox AK, Vashegyi I, Vágújfalvi A, Galiba G, Dubcovsky J (2010) Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1Connection. Plant Physiol 153(4):1846–1858
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42
Eglinton JK, Baum M, Grando S, Ceccarelli S, Barr AR (2001) Towards understanding the genetic basis of adaptation to low rainfall environments. In: Proceedings of the 10th Australian Barley Technical Symposium
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, Tondelli A, Rizza F, Badeck FW, Li Destri Nicosia 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 Crops Res 120(1):169–178
Gepts P (2006) Plant genetic resources conservation and utilization: the accomplishments and future of a societal insurance policy. Crop Sci 46:2278–2292
Gleeson A (1997) Spatial analysis. In: Kempton RA, Fox PN (eds) Statistical methods for plant variety evaluation. Chapman and Hall, London, pp 68–85
González FG, Slafer GA, Miralles DJ (2002) Vernalization and photoperiod responses in wheat pre-flowering reproductive phases. Field Crops Res 74(2–3):183–195
González FG, Miralles DJ, Slafer GA (2011) Wheat floret survival as related to pre-anthesis spike growth. J Exp Bot 62(14):4889–4901
Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in Barley. Plant Physiol 147:355–366
Hemming MN, Fieg S, Peacock WJ, Dennis ES, Trevaskis B (2009) Regions associated with repression of the barley Hordeum vulgare VERNALIZATION1 gene are not required for cold induction. Mol Genetics Genomics 282:107–117
Jia Q, Zhang J, Westcott S, Zhang X, Bellgard M, Lance R, Li C (2009) GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley. Funct Integr Genomics 9:255–262
Karsai I, Szücs P, Meszaros K, Filichkina T, Hayes PM, Skinner JS, Lang L, Bedo Z (2005) The Vrn-H2 locus is a major determinant of flowering time in a facultative winter growth habit barley (Hordeum vulgare L.) mapping population. Theor Appl Genet 110:1458–1466
Kato K, Miura H, Sawada S (1999) QTL mapping of genes controlling ear emergence time and plant height on chromosome 5A of wheat. Theor Appl Genet 98:472–477
Kempton RA, Gleeson A (1997) Unreplicated trials. In: Kempton RA, Fox PN (eds) Statistical methods for plant variety evaluation. Chapman and Hall, London, pp 86–100
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
Korol A, Ronin Y, Minkov D, Britvin E, Mester D, Korostishevsky M, Malkin I, Frenkel Z, Orion O, Cohen L, Brailovsky A (2005) MultiQTL version 2.5. Institute of Evolution, Haifa University, Haifa
Lakew B, Henry RJ, Ceccarelli S, Grando S, Eglinton J, Baum M (2012) Genetic analysis and phenotypic associations for drought tolerance in Hordeum spontaneum introgression lines using SSR and SNP markers. Euphytica 189:9–29
Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques MC, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729
Nitcher R, Distelfeld A, Tan C, Yan L, Dubcovsky J (2013) Increased copy number at the HvFT1 locus is associated with accelerated flowering time in barley. Mol Genet Genomics 288(5–6):261–275
Payne RW (ed) (2011) The guide to GenStat® Release 14. Part 2: statistics. VSN International, Hemel Hempstead, UK
Pillen K, Zacharias A, Léon J (2003) Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107:340–352
Pillen K, Zacharias A, Léon J (2004) Comparative AB-QTL analysis in barley using a single exotic donor of Hordeum vulgare ssp. spontaneum. Theor Appl Genet 108:1591–1601
Ponce-Molina LJ, Casas AM, Pilar Gracia M, Silvar C, Mansour E, Thomas WBT, Schweizer G, Herz M, Igartua E (2012) QTL and candidate loci for heading date in a large population of a wide barley cross. Crop Sci. doi:10.2135/cropsci2012.01.0029
Pswarayi A, van Eeuwijk F, Ceccarelli S, Grando S, Comadran J, Russell JR, Stanca AM, Francia E, Pecchioni N, Akar T, Al-Yassin A, Benbelkacem A, Choumane W, Karrou M, Ouabbou H, Bort J, Araus JL, Molina-Cano JL, Thomas WTB, Romagosa I (2008) Barley adaptation and improvement in the Mediterranean basin. Plant Breed 127:554–560
Rollins JA, Habte E, Templer SE, Colby T, Schmidt J, von Korff M (2013) Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J Exp Bot. doi:10.1093/jxb/ert158
Ryan J, Masri S, Garabet S, Diekmann J, Habib H (1997). Soils of ICARDA’s agricultural experiment stations and sites: climate, classification, physical-chemical properties and land use. ICARDA, Aleppo, Syria. Technical Bulletin: 126
Saisho D, Ishii M, Hori K, Sato K (2011) Natural variation of barley vernalization requirements: implication of quantitative variation of winter growth habit as an adaptive trait in East Asia. Plant Cell Physiol 52:724–727
SAS Institute (2009) The SAS system for Windows, release 9.1.3. SAS Institute, Cary, NC, USA
Shakhatreh Y, Kafawin O, Ceccarelli S, Saoub H (2001) Selection of barley lines for drought tolerance in low rainfall areas. J Agron Crop Sci 186:119–127
Simons KJ, Fellers JP, Trick HN, Zhang Z, Tai YS, Gill BS, Faris JD (2006) Molecular characterization of the major wheat domestication gene Q. Genetics 172:547–555
Singh M, Malhotra RS, Ceccarelli S, Sarker A, Grando S, Erskine W (2003) Spatial variability models to improve dryland field trials. Exp Agric 39:151–160
Skirycz A, Vandenbroucke K, Clauw P, Maleux K, De Meyer B, Dhondt S, Pucci A, Gonzalez N, Hoeberichts F, Tognetti VB, Galbiati M, Tonelli C, Van Breusegem F, Vuylsteke M, Inzé D (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotechnol 29:212–214
Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51(2):308–321
Talamé V, Sanguineti MC, Chiapparino E, Bahri H, Ben Salem M, 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(3):309–319
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K (2007) Hd3a protein is a mobile flowering signal in rice. Science 316:1033–1036
Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822
Teulat B, Merah O, Souyris I, This D (2001) QTLs for agronomic traits from a Mediterranean barley progeny grown under several environments. Theor Appl Genet 103:774–787
Tisné S, Schmalenbach I, Reymond M, Dauzat M, Pervent M, Vile D, Granier C (2010) Keep on growing under drought: genetic and developmental bases of the response of rosette area using a recombinant inbred line population. Plant Cell Environ 33:1875–1887
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, Vorrips RE (2001) JoinMap 4, Software for the Calculation of Genetic Linkage Maps. Plant Research International, Wageningen, the Netherlands
Voltas J, van Eeuwijk F, Igartua E, Garcia del Moral LF, Molina Cano JL, Romagosa I (2002) Genotype by environment interaction and adaptation in barley breeding: basic concepts and methods of analysis. Slafer et al (eds) Barley science. Recent advances from molecular biology to agronomy of yield and quality. Food Product Press, Binghamton, NY, pp 205–242
von Korff M, Wang H, Léon J, Pillen K (2006) AB-QTL analysis in spring barley: II. Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H. vulgare ssp. spontaneum). Theor Appl Genet 112(7):1221–1231
von Korff M, Grando S, This D, Baum M, Ceccarelli S (2008) Quantitative trait loci (QTL) associated with agronomic performance of barley under drought. Theor Appl Genet 117:653–669
von Korff M, Léon J, Pillen K (2010) Detection of epistatic interactions between exotic alleles introgressed from wild barley (H. vulgare ssp. spontaneum). Theor Appl Genet 121(8):1455–1464
Weltzien E (1988) Evaluation of barley (Hordeum vulgare L) landrace populations originating from different growing regions in the Near East. Plant Breed 101:95–106
Weltzien E (1989) Differentiation among barley landrace populations from the Near East. Euphytica 43:29–39
Windhausen VS, Wagener S, Magorokosho C, Makumbi D, Vivek B, Piepho H-P, Melchinger AE, Atlin GN (2012) Strategies to subdivide a target population of environments: results from the CIMMYT-led maize hybrid testing programs in Africa. Crop Sci 52:2143–2152
Yan W, Hunt LA, Sheng Q, Szlavnics Z (2000) Cultivar evaluation and mega-environment investigation based on the GGE biplot. Crop Sci 40(3):597–605
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Ac Sci USA 100:6263–6268
Yan L, Loukoianov A, Blech 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
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. PNAS 103:19581–19586
Zeven AC (1998) Landraces: a review of definitions and classifications. Euphytica 104:127–139
Acknowledgments
We are grateful for excellent technical assistance by K. Luxa and E. Luley. This work was supported by the Max Planck Society, the German Plant Genome Research Initiative of the Federal Ministry of Education and Research (BMBF), by grants from the DFG SPP1530 (“Flowering time control: from natural variation to crop improvement”), and by grants to ICARDA from the German Federal Ministry of Economic Cooperation and Development (BMZ, Bonn, Germany), the Generation Challenge Program and the Global Centre of Excellence Program, Tottori University, Japan.
Ethical standards
All experiments described in this manuscript comply with the current laws of the country in which they were performed.
Conflict of interest
The authors declare that they have no conflicts of interests.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. A. Carbonell.
J.A. Rollins and B. Drosse contributed equally to the paper.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rollins, J.A., Drosse, B., Mulki, M.A. et al. Variation at the vernalisation genes Vrn-H1 and Vrn-H2 determines growth and yield stability in barley (Hordeum vulgare) grown under dryland conditions in Syria. Theor Appl Genet 126, 2803–2824 (2013). https://doi.org/10.1007/s00122-013-2173-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-013-2173-y