Abstract
In the present study, the genetic diversity of 120 barley genotypes was investigated through 14 phenologic and agronomic traits as well as 50 SSR markers that cover the seven chromosomes of barley. In addition, the relationships between these marker loci and the studied traits were assessed via multiple regressions in two conditions. The field experiment was conducted in two planting dates, namely before the ideal time of the region planting date and the ideal planting date of the region in the experimental field of the Faculty of Agriculture and Natural Resources, Gonbad-e-Kavous University. A randomized complete block design with two replications was laid out for both planting dates. The results of cluster analysis based on SSR data classified the studied barley genotypes into six groups. For all the traits, except for spike length, more than one informative marker was detected. The results of stepwise regression analysis revealed significant associations between the traits and 60 SSR marker alleles under cold stress conditions. Under normal conditions, 63 SSR marker alleles showed a significant correlation with the studied traits. Among the 50 SSR markers, particular attention should be paid to a number of them, including the Bmag0211 marker with the highest coefficient of determination (R2) in regression analyses of grain yield, 1000-kernel weight under non-stress conditions, and grain width and days to maturity under cold stress conditions as well as HVBM5A marker associated with spike length, 1000-kernel weight, and days to flowering under cold stress conditions. These markers may be a novel finding and relatively more reliable than the other identified markers. The informative markers could be suitable for marker-assisted breeding in barley after confirming them in other experiments.
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06 May 2023
A Correction to this paper has been published: https://doi.org/10.1007/s11105-023-01383-9
References
Abedini R, GhaneGolmohammadi F, PishkamRad R, Pourabed E, Jafarnezhad A, Shobbar ZS, Shahbazi M (2017) Plant dehydrins: shedding light on structure and expression patterns of dehydrin gene family in barley. Int J Plant Res 130:747–763
Abou-Elwafa S (2016) Association mapping for drought tolerance in barley at the reproductive stage. Genet Mol Biol 339:51–59
Adhikari L, Baral R, Paudel D, Min D, Makaju SO, Poudel HP, Acharya JP, Missaoui AM (2022) Cold stress in plants: strategies to improve cold tolerance in forage species. Plant Stress 4:1–21
Alfonso C, Igartua E, Ciudad F, Codesal P, Russell JR, Molina-Cano JL, MoralejoPéter Szűcs M, Gracia MP, Lasa M, Casas AM (2008) Heading date QTL in a spring × winter barley cross evaluated in Mediterranean environments Mol Breed 21:455–471
Bassam BJ, Caetano-Anolles G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196:80–83
Barati AM, Moghaddam SA, Mohammadi A, Ghazvini HA, Sadeghzadeh B (2017) Identification of QTLs associated with agronomic and physiological traits under salinity stress in barley. J Agr Sci Tech 19:185–200
Beheshtizadeh H, Fakheri BA, Aghnoum R, Mahdinezhad N, Pourdad SS, Masoudi B (2018) QTL mapping of grain yield and its components under normal and drought stress conditions in barley (Hordeum vulgare L.). Indian J Genet 78:69–80
Bengtsson T, Manninen O, Jahoor A, Orabi J (2017) Genetic diversity, population structure and linkage disequilibrium in Nordic spring barley (Hordeum vulgare L. subsp. vulgare). Genet Resour Crop Evol 64:2021–2033
Cai S, Yu G, Chen X, Huang Y, Jiang X, Zhang G, Jin X (2013) Grain protein content variation and its association analysis in barley. BMC Plant Biol 13:35–42
Cakir M, poulsen D, Galwey NW, Ablet GA, Chalmers KJ, (2003) Mapping and QTL analysis of the barley population Tallone×Kaputar. Aust J Agric Res 54:1155–1162
Cary NC (2004a) SAS Institute. The SAS system for windows. Release 9.1. Cary, SAS Institute, p 654
Cary NC (2004b) SAS Institute. The SAS system for windows Release 9.1. Cary, SAS Institute, p 654
Cheghamirza K, Zarei L, Zebarjadi A, Honarmand SJ (2017) A study of the association between ISSR and RAPD markers and some agronomic traits in barley using a multiple regression analysis. Biotechnol 98:33–40
Chen G, Suprunova T, Krugman T, Fahima T (2004) Ecogeographic and genetic determinants of kernel weight and colour of wild barley (Hordeum spontaneum) populations in Israel. Seed Sci Res 14:137–146
Du B, Liu L, Wang Q, Sun G, Ren X, Li C, Sun D (2019) Identification of QTL underlying the leaf length and area of different leaves in barley. Sci Rep 9:31–44
Du B, Wang Q, Sun G, Ren X, Cheng Y, Wang Y, Gao S, Li C, Sun D (2019a) Mapping dynamic QTL dissects the genetic architecture of grain size and grain filling rate at different grain-filling stages in barley. Sci Rep 9:1–10
Eshghi R, Salayeva S, Ebrahimpour F, Rahimi M, Baraty M, Ojaghi J (2013) Advanced-backcross QTL analysis in hulless barley: I. Detection of exotic alleles for yield and yield components introgressed from Hordeum vulgare ssp. Spontaneum Intl J Agric Crop Sci 5:95–100
FAO (2020) FAO crop estimate data http://faostat.fao.org/site/565/defact.aspx
Fatemi F, Kianersi F, Pour-Aboughadareh A, Poczai P, Jadidi O (2022) Overview of Identified Genomic Regions Associated with Various Agronomic and Physiological Traits in Barley under Abiotic Stresses 12:51–89
Faure S, Higgins J, Turner A, Laurie DA (2007) The flowering locus T-like gene family in barley (Hordeum vulgare). GSA 176:599–609
Fiust A, Rapacz M (2020) Downregulation of three novel candidate genes is important for freezing tolerance of field and laboratory cold acclimated barley. J Plant Physiol 244:1–13
Francia E, Barabaschi D, Tondelli A, Laidò 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, Rizza F, Cattivelli L (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680
Ghomi K, Rabiei B, Sabouri H, Sabouri A (2013) Mapping QTLs for traits related to salinity tolerance at seedling stage of rice (Oryza sativa L.): an agrigenomics study of an Iranian rice population. OMICS 17:242–251
Gilliham M, Able JA, Roy SJ (2017) Translating knowledge about abiotic stress tolerance breeding programmes. Plant J 90:898–917
Golabadi M, Arzani A, Mirmohammadi Maibody SAM, Sayed Tabatabaei BE, Mohammadi SA (2011) Identification of microsatellite markers linked with yield components under drought stress at terminal growth stages in durum wheat. Euphytica 177:207–221
Gyawali B, Neupane D, Vaidya A, Sandbak A, Kallestrup P (2018) Community-based intervention for management of diabetes in Nepal (COBIN-D trial): study protocol for a cluster-randomized controlled trial. Study Protocol 19:1–10
Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802
Hommel GA (1988) Stagewise rejective multiple test procedure based on a modified Bonferroni test. Biometrika 75:383–386
Hamam KA (2004) Improving crop varieties of spring barley for drought and heat tolerance with AB-QTLanalysis. Phd dissertation, Bonn, University.
Han M, Wong J, Su T, Beatty HH, Good AG (2016) Identification of nitrogen use efficiency genes in barley: searching for QTLs controlling complex physiological traits. Front Plant Sci 7:1–17
Hayes PM, Blake T, Chen THH, Tragoonrung S, Chen F, Pan A, Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare L.) chromosome-7 associated with components of winterhardiness. Genome 36:66–71
Inostroza L, Pozo A, Matus I, Castillo D, Hayes P, Machado S, Corey A (2009) Association mapping of plant height, yield, and yield stability in recombinant chromosome substitution lines (RCSLs) using Hordeum vulgare subsp. spontaneum as a source of donor alleles in a Hordeum vulgare subsp. Vulgare Background Mol Breeding 23:365–376
Intergovernmental Panel on Climate Change, IPCC (2021) Available online at: http://www.ipcc.ch/index.htm
IPGRI (International Plant Genetic Resources Instit) (1994) Descriptors for barley (Hordeum vulgare L.). Rome, Publishing
Jabbari M, Fakheri B, Aghnoum R, Darvishzadeh R, Nezhad N, Ataei R, Koochakpour Z, Razi M (2021) Association analysis of physiological traits in spring barley (Hordeum vulgare L.) under water-deficit conditions. Food Sci Nutr 9:1761–1779
Jamali Seyed H, Mohammadi SA, Sadeghzadeh B (2017) Association mapping for morphological traits relevant to registration of barley varieties. SpMan J Agric Res 15:1–13
Kopahnke D, Nachtigall M, Ordon F, Stefenson BJ (2004) Evaluation and mapping of a leaf rust resistance gene derived from Hordeum vulgare subsp. Spontaneum Czech J Genet Plant Breed 40:86–90
Koppolu R, Jiang G, Milner S, Muqaddasi Q, Rutten T, Himmelbach A, Guo Y, Stein N, Mascher M, Schnurbusch T (2022) The barley mutant multiflorus2.b reveals quantitative genetic variation for new spikelet architecture. TAG 135:571–590
Lai Y, Yu Y, Liu X, Wan H, Zhang Z, Wang L, Leng Y, Ma L, Yang W, Feng Z (2017) Association mapping of grain weight, length and width in barley (Hordeum vulgare L.) breeding germplasm. Int J Agric Biol 19:1175–1186
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
Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of Wve major genes and eight quantitative trait loci controlling Xowering time in a winter £ spring barley (Hordeum vulgare L) cross. Genome 38:575–585
Lawati A, Saleem K, Nadaf, Nadiya A, AlSaady, Saleh A, Hinai A, Almandhar R, Maawali A (2021) Genetic diversity of Omani barley (Hordeum vulgare L.) germplasm. Open Agri 6(1):1–12
Li H, Chen G, Yan W (2015) Molecular characterization of barley 3H semi-dwarf genes. PLoS ONE 10:1–16
Li ZH, Li D, Du X, Wang H, Larroque O, Jenkins C, Jobling S, Morell M (2011) The barley amo1 locus is tightly linked to the starch synthase IIIa gene and negatively regulates expression of granule-bound starch synthetic genes. J Exp Bot 62:5217–5231
Liu H, Bao G, Dou Z, Liu H, Bai J, Chen Y, Yuan Y, Zhang X, Xi J (2022b) Response characteristics of highland barley under freeze-thaw, drought and artemisinin stresses. BMC Plant Biol 22(126). https://doi.org/10.1186/s12870-022-03520-0
Liu H, Wang W, Yang M, Yuan P, John P, Graham H, King J, Ding G, White F, Wang S, Cai H, Wang C, Lu C, Xu F, Shi L (2022a) Genome-wide association studies of important agronomic traits in Brassica napus: what we have learned and where we are headed. Annu Plant Rev Online 5(2):1–10
Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681
Manninen OM, Jalli M, Kalendar R, Schulman A, Afanasenko O (2006) Mapping of major spot-type and net-type netblotch resistance genes in the Ethiopian barley line CI 9819. Genome 49:1564–1571
Maurer A, Draba V, Pillen K (2016) Genomic dissection of plant development and its impact on thousand grain weight in barley through nested association mapping. J Exp Bot 67:2507–2518
Meszaros K, Karsai I, Kuti C, Banyai J, Lang L, Bedo Z (2007) Efficiency of different marker systems for genotype fingerprinting and for genetic diversity studies in barley (Hordeum vulgare L.). S AFR J BOT 73:43–48
Mikołajczak K, Ogrodowicz P, Gudyś K, Krystkowiak K, Sawikowska A, Frohmberg W, Górny A, Kędziora A, Jankowiak J, Józefczyk D, Karg G, Andrusiak J, Krajewski P (2016) Quantitative trait loci for yield and yield related traits in spring barley populations derived from crosses between European and syrian cultivars. PLoS ONE 11:1–26
Moualeu-Ngangue D, Dolch C, Schneider M, Le´on J, Uptmoor R, StutzelID H, (2020) Physiological and morphological responses of different spring barley genotypes to water deficit and associated QTLs. PLOSE ONE 15:1–33
Pan Y, Zhang H, Zhang D, Li J, Xiong H, Yu J, Li J, Abdul M, Rashid R, Li G, Ma X (2015) Genetic analysis of cold tolerance at the germination and booting stages in rice by association mapping. PLoS ONE 10:1–14
Pillen K, Zacharias A, Leon J (2003) Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107:340–352
Ren XF, Sun DF, Dong WB, Sun LCD (2014) Molecular detection of QTL controlling plant height components in a doubled haploid barley population. GMR 13:3089–3099
Roy JK, Bandopadhyay R, Rustgi S, Balyan HS, Gupta PK (2006) Association analysis of agronomically important traits using SSR, SAMPL and AFLP markers in bread wheat. Curr Sci 90:683–689
Saghai Maroof MA, Biyashev R, Yang GP, Zhang Q, Allard RW (1994) Extraordinarily polymorphic microsatellite DNA in barley: species diversity, chromosomal locations and population dynamics. P NATL ACAD SCI USA 91:5466–5470
Sallam AH, Smith KP, Hu G, Sherman J, Baenziger PS, Wiersma JJ, Duley C, Stockinger EJ Sorrells ME, Szinyei T, Loskutov IG, Kovaleva ON, Eberly J, Steffenson BJ (2021) Cold conditioned: discovery of novel alleles for low-temperature tolerance in the vavilov barley collection. Front Plant Sci 12 https://doi.org/10.3389/fpls.2021.800284
Sayed M, Schumann H, Pillen K, Naz AA, Léon J (2012) AB-QTL analysis reveals new alleles associated to proline accumulation and leaf wilting under drought stress conditions in barley (Hordeum vulgare L.). BMC Genet 13:1–12
Sayed MA, El-sadek AN, Bakry A, Ali MB, Leon J, Salem EM (2017) QTL analysis in barley across environments in Egypt. Egypt J Agron 39:53–70
Shehadi M, Lakkis GH, Hamze K, Abou Hamdan H, Kobaissi A (2014) Molecular and physiological characterization of local Lebanese barley (Hordeum vulgare L.) genotypes. IJSTR 3:216–222
Singh R, Prasad A, Muthamilarasan M, Parida S (2020) Breeding and biotechnological interventions for trait improvement: status and prospects. Planta 252:1–9
Sokal RR, Michener CD (1958) A statistical methods for evaluating relationships. University of Kansas Science Bulletin 38:1409–1448
Skinner S, Szucs P, Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen H, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112:832–842
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 51:308–321
Sun D, Ren W, Sun G (2011) Molecular diversity and association mapping of quantitative traits in Tibetan wild and worldwide originated barley (Hordeum vulgare L.) germplasm. Euphytica 178:31–43
Talukdar ZA, Rohman S, Begum F, Amiruzaman M (2014) Polymorphysm study in barley (Hordeum vulgare) genotypes using microsatellite (SSR) markers. Bangladesh j Agric Res 39:33–45
Teklemariam SS, Bayissa NN, Negisho K, Matros A, Pillen K, Ordon F, Wehner G (2022) The genetic diversity of Ethiopian barley genotypes in relation to their geographical origin. PLOSE ONE. https://doi.org/10.1371/journal.pone.0260422
Thabet SG, Alomari DZ, Brinch-Pedersen H, Alqudah AM (2022) Genetic analysis toward more nutritious barley grains for a food secure world. Bot Stud 63(6):1–15
Tyrka M, Cinrapacz M, Fiust A, Dalenaw M (2015) Quantitative trait loci mapping of freezing tolerance and photosynthetic acclimation to cold in winter two- and six-rowed barley. Plant Breed 134:1–12
Vafadar Shamasbi F, Jamali SH, Sadeghzadeh B, Abdollahi Mandoulakani B (2017) Genetic mapping of quantitative trait loci for yield-affecting traits in a barley doubled haploid population. Front Plant Sci 8:1–9
Varshney RK, Marcel TC, Ramsay L, Russell J, Ro¨ der MS, Stein R, Waugh R, Langridge P, Niks RE, Graner A (2007) A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet 114:1091–1103
Visioni A, Tondelli A, Francia E, Pswarayi A, Malosetti M, Russell J, Thomas W, Waugh R, Pecchioni N, Romagosa I, Comadran J (2013) Genome-wide association mapping of frost tolerance in barley (Hordeum vulgare L.). BMC Genomics 14:1–13
Wabila C, Neumann K, Kilian B, Radchuk V, Graner A (2019) A tiered approach to genome-wide association analysis for the adherence of hulls to the caryopsis of barley seeds reveals footprints of selection. BMC Plant Biol 19:1–8
Wang J, Sun G, Ren X, Li C, Liu L, Wang Q, Du B, Sun D (2016) QTL underlying some agronomic traits in barley detected by SNP markers. BMC Genet 17:103. https://doi.org/10.1186/s12863-016-0409-y
Wang J, Wu X, Yue W, Zhao C, Yang J, Zhou M (2021) Identification of QTL for barley grain size. Peer J 9:1–11
Wang J, Yang J, Jia Q, Zhu J, Shang Y (2014) A New QTL for plant height in barley (Hordeum vulgare L.) showing no negative effects on grain yield. PLoS ONE 9:1–8
Wang M, Jiang N, Jia T, Leach L, Cockram J, Waugh R, Ramsay L, Thomas B, Luo Z (2012) Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor Appl Genet 124:233–246
Wang Q, Sun G, Ren X, Wang J, Du B, Li C, Sun D (2017) Detection of QTLs for seedling characteristics in barley (Hordeum vulgare L.) grown under hydroponic culture condition. BMC Genet 18:1–16
Xu X, Sharma R, Tondelli A, Russell J, Comadran J, Schnaithmann F (2018) Genome-wide association analysis of grain yield-associated traits in a pan-European barley cultivar collection. Plant Genome 11:170–173
Xue DW, Zhou MX, Zhang XG, Chen S, Wei K, Zeng F, Mao Y, Wu F, Zhang GP (2010) Identification of QTLs for yield and yield components of barley under different growth conditions. J Zhejiang Univ Sci B 11:169–176
Yan S, Sun D, Sun G (2015) Genetic divergence in domesticated and non-domesticated gene regions of barley chromosomes. PLoS ONE 10:1–12
Zeng B, Luke R, Grant W, Montgomery AM, Esko T, Franke L, Vosa U, Claringbould A, Kenneth L, Brigham AA, Quyyumi Y, Yang J, Peter Visscher P, Joseph Powell E, Gibson G (2019) Comprehensive multiple eQTL detection and its application to GWAS interpretation. Genet 212(3):905–918
Acknowledgements
The authors thank the University of Guilan and Gonbad-e-Kavous University for their financial supports and agricultural research Center of Gonbad-e-Kavous for providing barley seeds used in this research.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Khadijeh Ghomi, Babak Rabiei, Hossein Sabouri, and Ebrahim Gholamalipour Alamdari. The first draft of the manuscript was written by Khadijeh Ghomi and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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• Our main discovery is assessing genetic variation and identifying markers related to traits in barley. Detected markers (Bmag0211, HVBM5A) may be novel finding and relatively more reliable than the other identified markers. The informative markers can be suitable for marker- assisted breeding in barley after confirming them in other experiments.
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Ghomi, K., Rabiei, B., Sabouri, H. et al. Association between SSR Markers and Phenologic Plus Agronomic Traits in Barley (Hordeum valgare L.) Under Cold Stress Conditions. Plant Mol Biol Rep 41, 164–184 (2023). https://doi.org/10.1007/s11105-022-01346-6
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DOI: https://doi.org/10.1007/s11105-022-01346-6