Abstract
A microsatellite (simple sequence repeat; SSR) panel for Cryptomeria japonica was established, using both newly developed and previously reported markers, to construct a frame of linkage map and facilitate localization of important genes in this species. In this study, 32 new expressed sequence tag SSRs (EST-SSRs) and 12 new genomic SSRs (gSSRs) were developed. Their average polymorphism information content (PIC) values were 0.549 and 0.776, respectively. The markers were mapped onto a high-density linkage map. The SSR panel that was established to cover the genome consisted of 46 gSSRs and 47 EST-SSRs. The number of SSR markers in each linkage group, the average map distance between loci within a linkage group, and the average PIC values in each linkage group ranged from 6 to 13, 6.77 to 19.88 and 0.475 to 0.712, respectively. The utility of the SSR panel was tested by using it to localize a male-sterile gene, ms-2. The ms-2 locus was successfully localized on the linkage group 5 using 33 SSR markers (three SSRs per linkage group) which were selected from the SSR panel based on the existence of polymorphisms and the absence of null alleles in the mapping population for ms-2. A partial linkage map surrounding the ms-2 locus was then constructed using a further 57 single nucleotide polymorphisms and three SSRs, to facilitate future development of markers tightly linked to the ms-2 locus for use in marker-assisted selection. The SSR panel covering the C. japonica genome will allow researchers to localize important genes efficiently.
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Aranzana MJ, Pineda A, Cosson P, Dirlewanger E, Ascasibar J, Cipriani G, Ryder CD, Testolin R, Abbott A, King GJ, Iezzoni AF, Arús P (2003) A set of simple-sequence repeat (SSR) markers covering the Prunus genome. Theor Appl Genet 106:819–825
Barrett B, Griffiths A, Schreiber M, Ellison N, Mercer C, Bouton J, Ong B, Forster J, Sawbridge T, Spangenberg G, Bryan G, Woodfield D (2004) A microsatellite map of white clover. Theor Appl Genet 109:596–608
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220
Dekkers JCM (2004) Commercial application of marker- and gene-assisted selection in livestock: strategies and lessons. J Anim Sci 82:E313–E328
Devey ME, Delfino-Mix A, Kinloch BB Jr, Neale DB (1995) Random amplified polymorphic DNA markers tightly linked to a gene for resistance to white pine blister rust in sugar pine. Proc Natl Acad Sci USA 92:2066–2070
Futamura N, Ujino-Ihara T, Nishiguchi M, Kanamori H, Yoshimura K, Sakaguchi M, Shinohara K (2006) Analysis of expressed sequence tags from Cryptomeria japonica pollen reveals novel pollen-specific transcripts. Tree Physiol 26:1517–1528
Futamura N, Totoki Y, Toyoda A, Igasaki T, Nanjo T, Seki M, Sakaki Y, Mari A, Shinozaki K, Shinohara K (2008) Characterization of expressed sequence tags from a full-length enriched cDNA library of Cryptomeria japonica male strobili. BMC Genomics 9:383
Guan L, Shiraishi S (2011) Tetranucleotide microsatellite markers in Cryptomeria japonica. Conserv Genet Resour 3:283–285
Harkins DM, Johnson GN, Skaggs PA, Mix AD, Dupper GE, Devey ME, Kinloch BB Jr, Neal DB (1998) Saturation mapping of a major gene for resistance to white pine blister rust in sugar pine. Theor Appl Genet 97:1355–1360
Heffner EL, Sorrells ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12
Hizume M, Kondo T, Shibata F, Ishizuka R (2001) Flow cytometric determination of genome size in the Taxodiaceae, Cupressaceae sensu stricto and Sciadopityaceae. Cytologia 66:307–311
Horner HT, Palmer RG (1995) Mechanisms of genic male sterility. Crop Sci 35:1527–1535
Iwata H, Ujino-Ihara T, Yoshimura K, Nagasaka K, Mukai Y, Tsumura Y (2001) Cleaved amplified polymorphic sequence markers in sugi, Cryptomeria japonica D. Don, and their locations on a linkage map. Theor Appl Genet 103:881–895
Jackson RE, Bradley JR Jr, Van Duyn JW (2003) Field performance of transgenic cottons expressing one or two Bacillus thuringiensis endotoxins against bollworm, Helicoverpa zea (Boddie). J Cotton Sci 7:57–64
Kitamura K, Kawahara T (2009) Clonal identification by microsatellite loci in sporadic flowering of a dwarf bamboo species, Sasa cernua. J Plant Res 122:299–304
Kondo H, Tahira T, Hayashi H, Oshima K, Hayashi K (2000) Microsatellite genotyping of post-PCR fluorescently labeled markers. Biotechniques 29:868–872
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Martin MA, Mattioni C, Cherubini M, Taurchini D, Villani F (2010) Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genet Genomes 6:735–744
Matsumoto A, Uchida K, Taguchi Y, Tani N, Tsumura Y (2010) Genetic diversity and structure of natural fragmented Chamaecyparis obtusa populations as revealed by microsatellite markers. J Plant Res 123:689–699
Miyajima D, Yoshii E, Hosoo Y, Taira H (2010) Cytological and genetic studies on male sterility in Cryptomeria japonica D. Don (Shindai 8). J Jpn For Soc 92:106–109 (In Japanese with English summary)
Mohan M, Nair S, Bhagwat A, Krishna TG, Yano M, Bhatia CR, Sasaki T (1997) Genome mapping, molecular markers and marker-assisted selection in crop plants. Mol Breed 3:87–103
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30:194–200
Moriguchi Y, Iwata H, Ihara T, Yoshimura K, Taira H, Tsumura Y (2003) Development and characterization of microsatellite markers for Cryptomeria japonica D. Don. Theor Appl Genet 106:751–758
Moriguchi Y, Kang KS, Lee KY, Lee SW, Kim YY (2009a) Genetic variation of Picea jezoensis populations in South Korea revealed by chloroplast, mitochondrial and nuclear DNA markers. J Plant Res 122:153–160
Moriguchi Y, Ueno S, Ujino-Ihara T, Futamura N, Matsumoto A, Shinohara K, Tsumura Y (2009b) Characterization of EST-SSRs from Cryptomeria japonica. Conserv Genet Resour 1:373–376
Moriguchi Y, Yomogida H, Iwata H, Takahashi M, Taira H, Tsumura Y (2011) Paternity analysis in a progeny test of Cryptomeria japonica revealed adverse effects of pollen contamination from outside seed orchards on morphological traits. Tree Genet Genomes 7:1089–1097
Moriguchi Y, Ujino-Ihara T, Uchiyama K, Futamura N, Saito M, Ueno S, Matsumoto A, Tani N, Taira H, Shinohara K, Tsumura Y (2012) The construction of a high-density linkage map for identifying SNP markers that are tightly linked to a nuclear-recessive major gene for male sterility in Cryptomeria japonica D. Don. BMC Genomics 13:95
Moritsuka E, HisatakaY TamuraM, Uchiyama K, Watanabe A, Tsumura Y, Tachida H (2012) Extended linkage disequilibrium in noncoding regions in a conifer, Cryptomeria japonica. Genetics 190:1145–1148
Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev 12:111–122
Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330
Nikaido AM, Ujino T, Iwata H, Yoshimura K, Yoshimura H, Suyama Y, Murai M, Nagasaka K, Tsumura Y (2000) AFLP and CAPS linkage maps of Cryptomeria japonica. Theor Appl Genet 100:825–831
Peakall R, Smouse PE (2006) GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Portnoy DS, Hollenbeck CM, Renshaw MA, Gold JR (2011) Microsatellite panels for gene localization in red drum, Sciaenops ocellatus. Aquaculture 319:505–508
Saito M (2010) Breeding strategy for the pollinosis preventive cultivars of Cryptomeria japonica D Don. J Jpn For Soc 92:316–323 In Japanese with English summary
Saito M, Taira H, Furuta Y (1998) Cytological and genetical studies on male sterility in Cryptomeria japonica D. Don. J For Res 3:167–173
Sharma PC, Grover A, Kahl G (2007) Mining microsatellites in eukaryotic genomes. Trends Biotechnol 25:490–498
Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2:202–224
Singh S, Sidhu JS, Huang N, Vikal Y, Li Z, Brar DS, Dhaliwal HS, Khush GS (2001) Pyramiding three bacterial blight resistance genes (xa5, xa13 and Xa21) using marker-assisted selection into indica rice cultivar PR106. Theor Appl Genet 102:1011–1015
Stallings RL, Ford AF, Nelson D, Torney DC, Hildebrand CE, Moyzis RK (1991) Evolution and distribution of (GT) n repetitive sequences in mammalian genomes. Genomics 10:807–815
Taira H, Teranishi H, Kenda Y (1993) A case study of male sterility in sugi (Cryptomeria japonica). J Jpn For Soc 75:377–379 In Japanese with English summary
Taira H, Saito M, Furuta Y (1999) Inheritance of the trait of male sterility in Cryptomeria japonica. J For Res 4:271–273
Tani N, Takahashi T, Ujino-Ihara T, Iwata H, Yoshimura K, Tsumura Y (2004) Development and characteristics of microsatellite markers for sugi (Cryptomeria japonica D. Don) from microsatellite enriched libraries. Ann For Sci 61:569–575
Tani N, Tsumura Y, Kado T, Taguchi Y, Lee SL, Muhammad N, Ng KKS, Numata S, Nishimura S, Konuma A, Okuda T (2009) Paternity analysis-based inference of pollen dispersal patterns, male fecundity variation, and influence of flowering tree density and general flowering magnitude in two dipterocarp species. Ann Bot 104:1421–1434
Tsumura Y (2011) Cryptomeria. In: Kole C (ed) Wild crop relatives: genomics and breeding resources, forest trees. Springer, New York, pp 49–64
Tsumura Y, Suyama Y, Yoshimura K, Shirato N, Mukai Y (1997) Sequence-tagged-sites (STSs) of cDNA clones in Cryptomeria japonica and their evaluation as molecular markers in conifers. Theor Appl Genet 94:764–772
Uchiyama K, Ujino-Ihara T, Ueno S, Taguchi Y, Futamura N, Shinohara K, Tsumura Y (2012) Single nucleotide polymorphisms in Cryptomeria japonica: their discovery and validation for genome mapping and diversity studies. Tree Genet Genomes 8:1213–1222
Ueno S, Moriguchi Y, Uchiyama K, Ujino-Ihara T, Futamura N, Sakurai T, Shinohara K, Tsumura Y (2012) A second generation framework for the analysis of microsatellites in expressed sequence tags and the development of EST-SSR markers for a conifer, Cryptomeria japonica. BMC Genomics 13:136
Ujino-Ihara T, Yoshimura K, Ugawa Y, Yoshimaru H, Nagasaka K, Tsumura Y (2000) Expression analysis of ESTs derived from the inner bark of Cryptomeria japonica. Plant Mol Biol 43:451–457
Ujino-Ihara T, Taguchi Y, Yoshimura K, Tsumura Y (2003) Analysis of expressed sequence tags derived from developing seed and pollen cones of Cryptomeria japonica. Plant Biol 5:600–607
Ujino-Ihara T, Kanamori H, Yamane H, Taguchi Y, Namiki N, Mukai Y, Yoshimura K, Tsumura Y (2005) Comparative analysis of expressed sequence tags of conifers and angiosperms reveals sequences specifically conserved in conifers. Plant Mol Biol 59:895–907
Van Ooijen JW, Voorrips RE (2001) JoinMap version 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang CM, Zhu ZY, Lo LC, Feng F, Lin G, Yang WT, Li J, Yue GH (2007) A microsatellite linkage map of Barramundi, Lates calcarifer. Genetics 175:907–915
Werner K, Friedt W, Ordon F (2005) Strategies for pyramiding resistance genes against the barley yellow mosaic virus complex (BaMMV, BaYMV, BaYMV-2). Mol Breed 16:45–55
Woodhead M, Russell J, Squirrell J, Hollingsworth PM, Mackenzie K, Gibby M, Powell W (2005) Comparative analysis of population genetic structure in Athyrium distentifolium (Pteridophyta) using AFLPs and SSRs from anonymous and transcribed gene regions. Mol Ecol 14:1681–1695
Xu Y, Crouch JH (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48:391–407
Yoshida K, Nishiguchi M, Futamura N, Nanjo T (2007) Expressed sequence tags from Cryptomeria japonica sapwood during the drying process. Tree Physiol 27:1–9
Yoshii E, Taira H (2007) Cytological and genetical studies on male sterile sugi (Cryptomeria japonica D. Don), Shindai 1 and Shindai 5. J Jpn For Soc 89:26–30 In Japanese with English summary
Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E, McCown B, Harbut R, Simon P (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99:193–208
Zhang L, Yuan D, Yu S, Li Z, Cao Y, Miao Z, Qian H, Tang K (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinfomatics 20:1081–1086
Zhang H, Wang H, Guo S, Ren Y, Gong G, Weng Y, Xu Y (2012) Identification and validation of a core set of microsatellite markers for genetic diversity analysis in watermelon, Citrullus lanatus Thunb. Matsum. & Nakai. Euphytica 186:329–342
Acknowledgments
The authors would like to thank M. Koshiba and Y. Komatsu for assistance with laboratory work. This work was partly supported by a Grant-in-Aid (Development of Technologies for Control of Pollen Production by Genetic Engineering) from the Forest Agency of Japan and by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry and JSPS KAKENHI Grant Number 25850116.
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Moriguchi, Y., Ueno, S., Higuchi, Y. et al. Establishment of a microsatellite panel covering the sugi (Cryptomeria japonica) genome, and its application for localization of a male-sterile gene (ms-2). Mol Breeding 33, 315–325 (2014). https://doi.org/10.1007/s11032-013-9951-8
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DOI: https://doi.org/10.1007/s11032-013-9951-8