Abstract
Grain yield potential in cereals results from the contributions of three main components: inflorescence number per plant, grain number per inflorescence and mean grain weight. In rice, the Dense and erect panicle (DEP1) gene affects three important quantitative traits of the inflorescence and DEP1 homologs have been reported in barley and wheat. In this work, we have performed a detailed characterization of the barley DEP1 (HvDEP1) gene. We obtained a full-length sequence of its transcript, examined its expression in various tissues, genetically mapped it to chromosome 5H and measured its nucleotide diversity in a collection of barley cultivars from Canada. This gene has an exceptionally long 5′ UTR (297 bp) that contains an upstream open reading frame (uORF) coding for a predicted peptide of 70 amino acids. A similarly long 5′ UTR containing a putative uORF was found in all six grass species that we examined. Although HvDEP1 transcripts could be detected in all tissues tested, it was highest in meristematic tissues. In a collection of 167 barley cultivars, a low level of polymorphism was observed (π = 0.001) and the 37 SNPs/indels detected, none of which result in changes in the amino acid sequence of the HvDEP1 protein, defined 8 haplotypes. Diversity was especially low among 83 six-row types, all but one of which carried the exact same haplotype. We suggest that HvDEP1 is involved in the control of cellular growth and differentiation, that the conserved uORF may play a role in its post-transcriptional regulation and that this gene has undergone a very different history of selection within the two-row and six-row Canadian elite germplasm.
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Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, Kurabayashi A, Suzuki T, Tsugane T, Watanabe M, Ooga K, Torii M, Narita T, Shin-i T, Kohara Y, Yamamoto N, Takahashi H, Watanabe Y, Egusa M, Kodama M, Ichinose Y, Kikuchi M, Fukushima S, Okabe A, Arie T, Sato Y, Yazawa K, Satoh S, Omura T, Ezura H, Shibata D (2010) Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genom 11:210–226. doi:10.1186/1471-2164-11-210
Barrett LW, Fletcher S, Wilton SD (2012) Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 69:3613–3634. doi:10.1007/s00018-012-0990-9
Boyeldieu J (1997) Blé tendre. Techniques agricoles, Editions Techniques—Techniques agricoles. Fascicule 2020
Calvo SE, Pagliarini DJ, Mootha VK, Weissman J (2009) Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci USA 106:7507–7512. doi:10.1073/pnas.0810916106
Fu Y (2012) Population-based resequencing analysis of wild and cultivated barley revealed weak domestication signal of selection and bottleneck in the Rrs2 scald resistance gene region. Genome 55:93–104. doi:10.1139/G11-082
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41:494–497. doi:10.1038/ng.352
Jilal A, Grando S, Henry R, Lee L, Rice N, Hill H, Baum M, Ceccarelli S (2008) Genetic diversity of ICARDA’s worldwide barley landrace collection. Genet Resour Crop Evol 55:1221–1230. doi:10.1007/s10722-008-9322-1
Jones H, Leigh FJ, Mackay I, Bower MA, Smith LMJ, Charles MP, Jones G, Jones MK, Brown TA, Powell W (2008) Population-based resequencing reveals that the flowering time adaptation of cultivated barley originated east of the fertile crescent. Mol Biol Evol 25:2211–2219. doi:10.1093/molbev/msn167
Kawaguchi R, Bailey-Serres J (2005) mRNA sequence features that contribute to translational regulation in Arabidopsis. Nucleic Acids Res 33:955–965. doi:10.1093/nar/gki240
Kilian B, Özkan H, Kohl J, von Haeseler A, Barale F, Deusch O, Brandolini A, Yucel C, Martin W, Salamini F (2006) Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication. Mol Genet Genomics 276:230–241. doi:10.1007/s00438-006-0136-6
Komatsuda T, Pourkheirandish M, He CF, 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. doi:10.1073/pnas.0608580104
Kosambi D (1944) The estimation of map distances from recombination values. Annals of Eugenics 12:172–175. doi:10.1111/j.1469-1809.1943.tb02321
Lamara M, Zhang LY, Marchand S, Tinker NA, Belzile F (2013) Comparative analysis of genetic diversity in Canadian barley assessed by SSR, DarT, and pedigree data. Genome 56(6):351–358. doi:10.1139/gen-2013-0048
Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187
Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635–8642. doi:10.1128/MCB.20.23.8635-8642.2000
Pillen K, Zacharias A, Léon J (2003). Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107:340–352
Pourkheirandish M, Komatsuda T (2007) The importance of barley genetics and domestication in a global perspective. Ann Bot 100:999–1008. doi:10.1093/aob/mcm139
Russell J, Dawson IK, Flavell AJ, Steffenson B, Weltzien E, Booth A, Ceccarelli S, Grando S, Waugh R (2011) Analysis of 1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol 191:564–578. doi:10.1111/j.1469-8137.2011.03704
Sakamoto T, Matsuoka M (2008) Identifying and exploiting grain yield genes in rice. Curr Opin Plant Biol 11:209–214. doi:10.1016/j.pbi.2008.01.009
Sato K, Nankaku N, Takeda K (2009) A high density transcript linkage map of barley derived from a single population. Heredity 103:110–117. doi:10.1038/hdy.2009.57
Soltner D (1998) Les grandes productions végétales : céréales, plantes sarclées, prairies. Sainte-Gemme-sur-Loire, Sciences et Techniques Agricoles
Taguchi-Shiobara F, Kawagoe Y, Kato H, Onodera H, Tagiri A, Hara N, Miyao A, Hirochika H, Kitano H, Yano M, Toki S (2011) A loss-of-function mutation of rice DENSE PANICLE 1 causes semi-dwarfness and slightly increased number of spikelets. Breed Sci 61:17–25. doi:10.1270/jsbbs.61.17
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
The International Barley Genome Sequencing Consortium (IBSC) (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716. doi:10.1038/nature11543
Tinker NA, Mather DE, Rossnagel BG, Kasha KJ, Kleinhofs A, Hayes PM, Falk DE, Ferguson T, Shugar LP, Legge WG, Irvine RB, Choo TM, Briggs KG, Ullrich SE, Franckowiak JD, Blake TK, Graf RJ, Dofing SM, Saghai Maroof MA, Scoles GF, Hoffman D, Dahleen LS, Kilian A, Chen F, Biyashev RM, Kudrna DA, Steffenson BJ (1996) Regions of the genome that affect agronomic performance in two-row barley. Crop Science 36:1053–1062
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276. doi:10.1016/0040-5809(75)90020-9
Acknowledgments
S. Bélanger gratefully acknowledges undergraduate and graduate studentships from the National Sciences and Engineering Research Council of Canada. This work was also supported by a research grant from the Natural Sciences and Engineering Research Council of Canada to F. Belzile.
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Bélanger, S., Gauthier, M., Jean, M. et al. Genomic characterization of the Hordeum vulgare DEP1 (HvDEP1) gene and its diversity in a collection of barley accessions. Euphytica 198, 29–41 (2014). https://doi.org/10.1007/s10681-014-1089-1
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DOI: https://doi.org/10.1007/s10681-014-1089-1