Skip to main content
Log in

A high-density linkage map with 2560 markers and its application for the localization of the male-sterile genes ms3 and ms4 in Cryptomeria japonica D. Don

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Cryptomeria japonica pollinosis is one of the most serious allergic diseases in Japan; this is a social problem because C. japonica is the most important Japanese forestry species. In order to reduce the amount of pollen dispersed, breeding programs using trees with male-sterile genes have been implemented. High-density linkage maps with stable ordering of markers facilitate the localization of male-sterile genes and the construction of partial linkage maps around them in order to develop markers for use in marker-assisted selection. In this study, a high-density linkage map for C. japonica with 2560 markers was constructed. The observed map length was 1266.2 cM and the mean distance between adjacent markers was 0.49 cM. Using information from this high-density map, we newly located two male-sterile genes (ms3 and ms4) on the first and fourth linkage groups, respectively, and constructed partial linkage maps around these loci. We also constructed new partial linkage maps around the ms1 and ms2 loci using additional SNP markers. The closest markers to the ms1, ms2, ms3, and ms4 male-sterile loci were estSNP04188 (1.8 cM), estSNP00695 (7.0 cM), gSNP05415 (3.1 cM), and estSNP01408 (7.0 cM) respectively. These results allowed us to develop SNP markers tightly linked to the male sterile genes for use in MAS; this will accelerate the future isolation of these genes by map-based cloning approaches.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baba K, Nakae K (2008) The national epidemiological survey of allergic rhinitis in 2008—comparison between 1998 and 2008. Prog Med 28:2001–2012 (in Japanese)

    Google Scholar 

  • Baxter SW, Davey JW, Johnston JS, Shelton AM, Heckel DG, Jiggins CD, Blaxter ML (2011) Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS One 6:e19315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cartwright DA, Troggio M, Velasco R, Gutin A (2007) Genetic mapping in the presence of genotyping errors. Genetics 176:2521–2527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dekkers JCM (2004) Commercial application of marker- and gene-assisted selection in livestock: strategies and lessons. J Anim Sci 82:E313–E328

    PubMed  Google Scholar 

  • Dokku P, Das KM, Rao GJN (2013) Pyramiding of four resistance genes of bacterial blight in Tapaswini, an elite rice cultivar, through marker-assisted selection. Euphytica 192:87–96

    Article  Google Scholar 

  • Echt CS, Saha S, Krutovsky KV, Wimalanathan K, Erpelding JE, Liang C, Nelson CD (2011) An annotated genetic map of loblolly pine based on microsatellite and cDNA markers. BMC Genet 12:17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forestry Agency (2014) Statistical handbook of forest and forestry. Forestry Agency, Ministry of Agriculture, Forestry and Fisheries. P8-9 (in Japanese)

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kakioka R, Kokita T, Kumada H, Watanabe K, Okuda N (2013) A RAD-based linkage map and comparative genomics in the gudgeons (genus Gnathopogon, Cyprinidae). BMC Genomics 14:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang BY, Mann IK, Major JE, Rajora OP (2010) Near-saturated and complete genetic linkage map of black spruce (Picea mariana). BMC Genomics 11:515

    Article  PubMed  PubMed Central  Google Scholar 

  • Karaagac E, Vargas AM, de Andrés MT, Carreño I, Ibáñez J, Carreño J, Martínez-Zapater JM, Cabezas JA (2012) Marker assisted selection for seedlessness in table grape breeding. Tree Genet Genomes 8:1003–1015

    Article  Google Scholar 

  • Koide Y, Kawasaki A, Telebanco-Yanoria MJ, Hairmansis A, Nguyet NTM, Bigirimana J, Fujita D, Kobayashi N, Fukuta Y (2010) Development of pyramided lines with two resistance genes, Pish and Pib, for blast disease (Magnaporthe oryzae B. Couch) in rice (Oryza sativa L.). Plant Breed 129:670–675

    Article  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Kusumi J, Tsumura Y, Yoshimaru H, Tachida H (2000) Phylogenetic relationships in Taxodiaceae and Cupressaceae based on matK, chlL, trnL-trnF IGS region and trnL intron sequences. Am J Bot 87:1480–1488

    Article  CAS  PubMed  Google Scholar 

  • Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 34:842–845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maccaferri M, Ricci A, Salvio S, Milner SG, Noli E, Martelli PL, Casadio R, Akhunov E, Scalabrin S, Vendramin V, Ammar K, Blanco A, Desiderio F, Distelfeld A, Dubcovsky J, Fahima T, Faris J, Korol A, Massi A, Mastrangelo AM, Morgante M, Pozniak C, N’Diaye A, Xu S, Tuberosa R (2014) A high-density, SNP-based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotech J (online early)

  • Martínez-García PJ, Stevens KA, Wegrzyn JL, Liechty J, Crepeau M, Langley CH, Neale DB (2013) Combination of multipoint maximum likelihood (MML) and regression mapping algorithms to construct a high-density genetic linkage map for loblolly pine (Pinus taeda L.). Tree Genet Genomes 9:1529–1535

    Article  Google Scholar 

  • Matsumoto A, Tsumura Y (2004) Evaluation of cleaved amplified polymorphic sequence markers for Chamaecyparis obtusa based on expressed sequence tag information from Cryptomeria japonica. Theor Appl Genet 110:80–91

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Moriguchi Y, Ueno S, Ujino-Ihara T, Futamura N, Matsumoto A, Shinohara K, Tsumura Y (2009) Characterization of EST-SSRs from Cryptomeria japonica. Conserv Genet Resour 1:373–376

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Moriguchi Y, Ueno S, Higuchi Y, Miyajima D, Itoo S, Futamura N, Tsumura Y (2014a) Establishment of a microsatellite panel covering the sugi (Cryptomeria japonica) genome, and its application for localization of a male sterile gene (ms2). Mol Breed 33:315–325

  • Moriguchi Y, Ueno S, Saito M, Higuchi Y, Miyajima D, Itoo S, Tsumura Y (2014b) A simple allele-specific PCR marker for identifying male-sterile trees: towards DNA marker-assisted selection Cryptomeria japonica breeding program. Tree Genet Genetics 10:1069–1077

  • Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neves LG, Davis JM, Barbazuk WB, Kirst M (2014) A high-density gene map of loblolly pine (Pinus taeda L.) based on exome sequence capture genotyping. G3-Genes Genomes Genet 4:29–37

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pavy N, Pelgas B, Beauseigle S, Blais S, Gagnon F, Gosselin I, Lamothe M, Isabel N, Bousquet J (2008) Enhancing genetic mapping of complex genomes through the design of highly-multiplexed SNP arrays: application to the large and unsequenced genomes of white spruce and black spruce. BMC Genomics 9:21

    Article  PubMed  PubMed Central  Google Scholar 

  • Pavy N, Pelgas B, Laroche J, Rigault P, Isabel N, Bousquet J (2012) A spruce gene map infers ancient plant genome reshuffling and subsequent slow evolution in the gymnosperm lineage leading to extant conifers. BMC Biol 10:84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plomion C, Chancerel E, Endelman J, Lamy JB, Mandrou E, Lesur I, Ehrenmann F, Isik F, Bink MC, van Heerwaarden J, Bouffier L (2014) Genome-wide distribution of genetic diversity and linkage disequilibrium in a mass-selected population of maritime pine. BMC Genomics 15:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Remington DL, Whetten RW, Liu BH, O’Malley DM (1999) Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor Appl Genet 98:1279–1292

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • Taira H, Saito M, Furuta Y (1999) Inheritance of the trait of male sterility in Cryptomeria japonica. J For Res 4:271–273

    Article  Google Scholar 

  • Tani N, Takahashi T, Iwata H, Yuzuru M, Ujino-Ihara T, Matsumoto A, Yoshimura K, Yoshimaru H, Murai M, Nagasaka K, Yoshihiko T (2003) A consensus linkage map for sugi (Cryptomeria japonica) from two pedigrees, based on microsatellites and expressed sequence tags. Genetics 165:1551–1568

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMap version 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen

    Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Westbrook JW, Chhatre VE, Wu LS, Chamala S, Neves LG, Muñoz P, Martínez-García PJ, Neale DB, Kirst M, Mockaitis K, Nelson CD, Peter GF, Davis JM, Echt CS (2015) An annotated consensus genetic map for Pinus taeda L. and extent of linkage disequilibrium in three genotype-phenotype discovery populations. bioRxiv. doi:10.1101/012625

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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)

    Article  Google Scholar 

  • Zhong S, Toubia-Rahme H, Steffenson BJ, Smith KP (2006) Molecular mapping and marker-assisted selection of genes for septoria speckled leaf blotch resistance in barley. Phytopathology 96:993–999

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank M. Koshiba, Y. Komatsu, Y. Taguchi, and S. Totsuka for the assistance with laboratory work and the sampling of leaves in the nursery. We also thank K. Arai, K. Nemoto, M. Sugiyama, H. Kimura, T. Suzuki, and Y. Hosoya for raising of the plant materials. This work was partly supported by a Grant-in-Aid from the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry, Research Grant #201421 of the Forestry and Forest Products Research Institute and JSPS KAKENHI Grant Numbers 25850116 and 25450223.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yoshihiko Tsumura.

Additional information

Communicated by D. Grattapaglia

Data archiving statement

All marker information and marker/position information from the linkage map were submitted to DDBJ and the TreeGenes Database, respectively.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Positions of the 508 common markers mapped on two Cryptomeria japonica linkage maps in Moriguchi et al. (2012) and the present study. Both axes indicate cumulative centimorgans (cM). (JPG 73 kb)

High resolution image (EPS 839 kb)

Fig. S2

Partial linkage maps around the ms2 gene constructed in the present study (right) and that by Moriguchi et al. (2014a) (left). Marker names are indicated to the right of the linkage groups. Centimorgan distances (Kosambi) are indicated to the left of each linkage group. The last letter of the locus indicates the nature of the markers, i.e., S indicates genomic SSRs. (JPG 273 kb)

High resolution image (EPS 1519 kb)

ESM 3

(XLSX 11 kb)

ESM 4

(XLSX 10 kb)

ESM 5

(XLSX 41.7 kb)

ESM 6

(XLSX 9.70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moriguchi, Y., Uchiyama, K., Ueno, S. et al. A high-density linkage map with 2560 markers and its application for the localization of the male-sterile genes ms3 and ms4 in Cryptomeria japonica D. Don. Tree Genetics & Genomes 12, 57 (2016). https://doi.org/10.1007/s11295-016-1011-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-016-1011-1

Keywords

Navigation