Skip to main content
Log in

Hybrid seedling inviability locus (HIs1) mapped on linkage group 4 of the Japanese flowering cherry, Cerasus × yedoensis ‘Somei-yoshino’

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

Abstract

Cerasus × yedoensis ‘Somei-yoshino’ (2n = 16), one of the most popular cultivars of Japanese flowering cherry, is considered a hybrid between Cerasus spachiana and Cerasus speciosa. In the present study, we observed segregation of the trait for seedling growth in F 1 progenies of Somei-yoshino. In all three families crossed with ancestral wild species, C. spachiana, approximately half of the seedlings showed growth failure. To identify loci involved in seedling inviability, we constructed a genetic linkage map of Somei-yoshino. Both normal growth (N = 77) and growth failure seedlings (N = 101) of an F 1 progenies crossed between Somei-yoshino (CY) and C. spachiana (E750) were used for map construction. In accordance to pseudo-testcross strategy, female (CY) and male (E750) linkage maps were constructed. The CY map consists of eight linkage groups with 59 simple sequence repeat (SSR) and 17 amplified fragment length polymorphism (AFLP) markers. The map length is 574.9 cM. In contrast, the E750 map reached 196.8 cM and included 17 SSRs. Subsequently, we explored positions of loci associated to seedling inviability along with linkage maps. Results of segregation distortion of markers, association analysis, and interval mapping consistently showed that an inviability gene was located between two SSR markers, EMPaS13 and BPPCT005 in the fourth linkage group (LG4) of the Somei-yoshino map with 99.6 % explanations for the inviability trait but not present in LG4 of the E750 map. From the genotypes and expressions of seedling inviability, we named the locus Hybrid Inviability of seedlings 1 (HIs1). Finally, HIs1 was mapped to LG4 as Mendelian trait loci and was completely linked with an SSR, EMPaS13. Although the mechanisms of seedling inviability cannot be explained by only one locus model of HIs1, one of the candidate genes involved in hybrid incompatibility between Somei-yoshino and C. spachiana is certainly located on LG4 of the CY map.

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

  • Aranzana MJ, Garcia-Mas J, Carbó J, Arús P (2002) Development and variability analysis of microsatellite markers in peach. Plant Breed 121:87–92

    Article  CAS  Google Scholar 

  • Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott AG (2012) The Peach Genome. Tree Genet Genome 8:531–547

    Article  Google Scholar 

  • Bliss FA, Arulsekar S, Foolad MR, Becerra V, Gillen AM, Warburton ML, Dandekar AM, Kocsisne GM, Mydin KK (2002) An expanded genetic linkage map of Prunus based on an interspecific cross between almond and peach. Genome 45:520–529

    Article  CAS  PubMed  Google Scholar 

  • Bomblies K, Weigel D (2007) Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8:382–393

    Article  CAS  PubMed  Google Scholar 

  • Chagné D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C, Ireland H, Fiers M, Dzierzon H, Cestaro A, Fontana P et al (2014) The draft genome sequence of European pear (Pyrus communis L. ‘Bartlett’). PLoS One 9:e92644

    Article  PubMed Central  PubMed  Google Scholar 

  • Cipriani G, Lot G, Huang WG, Marrazzo MT, Peterlunger E, Testolin R (1999) AC/GT and AG/CT microsatellite repeats in peach [Prunus persica (L) Batsch]: isolation, characterisation and cross-species amplification in Prunus. Theor Appl Genet 99:65–72

    Article  CAS  Google Scholar 

  • Clarke JB, Tobutt KR (2003) Development and characterization of polymorphic microsatellites from Prunus avium ‘Napoleon’. Mol Ecol Notes 3:578–580

    Article  CAS  Google Scholar 

  • Clarke JB, Sargent DJ, Bošković RI, Belaj A, Tobutt KR (2009) A cherry map from the inter-specific cross Prunus avium ‘Napoleon’ × P. nipponica based on microsatellite, gene-specific and isoenzyme markers. Tree Genet Genome 5:41–51

    Article  Google Scholar 

  • Dirlewanger E, Cosson P, Tavaud M, Aranzana MJ, Poizat C, Zanetto A, Arús A, Laigret F (2002) Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet 105:127–138

    Article  CAS  PubMed  Google Scholar 

  • Dirlewanger E, Graziano E, Joobeur T, Garriga-Calderé F, Cosson P, Howad W, Arús P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci U S A 101:9891–9896

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flower Association of Japan (1982) Manual of Japanese flowering cherries. Flower association of Japan, Tokyo

    Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137

    PubMed Central  CAS  PubMed  Google Scholar 

  • Iketani H, Ohta S, Kawahara T, Katsuki T, Mase N, Sato Y, Yamamoto T (2007) Analysis of clonal status in ‘Somei-yoshino’ and confirmation of genealogical record in other cultivars of Prunus × yedoensis by microsatellite markers. Breed Sci 57:1–6

    Article  Google Scholar 

  • Innan H, Terauchi R, Miyashita NT, Tsunewaki K (1995) DNA fingerprinting study on the intraspecific variation and the origin of Prunus yedoensis (Someiyoshino). Japan J Genet 70:185–196

    Article  CAS  Google Scholar 

  • Joobeur T, Viruel MA, de Vicente MC, Jauregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Messeguer R, Battle I et al (1998) Construction of a saturated linkage map for Prunus using an almond × peach F2 progeny. Theor Appl Genet 97:1034–1041

    Article  CAS  Google Scholar 

  • Kato S, Ishikawa H, Ohta Y, Hattori SO, Mukai Y (2009) Use of self-incompatibility gene and nuclear SSRs as a molecular tool to detect the genome derived from Prunus yedoensis “Someiyoshino”. J Jpn For Soc 91:354–359

    Article  CAS  Google Scholar 

  • Kato S, Matsumoto A, Yoshimura K, Katsuki T, Iwamoto K, Kawahara T, Mukai Y, Tsuda Y, Ishio S, Nakamura K et al (2014) Origins of Japanese flowering cherry (Prunus subgenus Cerasus) cultivars revealed using nuclear SSR markers. Tree Genet Genome 10:477–487

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lyttel TW (1991) Segregation distorters. Annu Rev Genet 25:511–557

    Article  Google Scholar 

  • Matsubara K, Ando T, Mizubayashi T, Ito S, Yano M (2007) Identification and linkage mapping of complementary recessive genes causing hybrid breakdown in an intraspecific rice cross. Theor Appl Genet 115:179–186

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Yamamoto E, Morinaka Y, Takashi T, Kitano H, Matsuoka M, Ashikari M (2008) The hybrid breakdown 1(t) locus induces interspecific hybrid breakdown between rice Oryza sativa cv. Koshihikari and its wild relative O. nivara. Breed Sci 58:99–105

    Article  CAS  Google Scholar 

  • Mnejja M, Garcia-Mas J, Howad W, Badenes ML, Arús P (2004) Simple-sequence repeat (SSR) markers of Japanese plum (Prunus salicina Lindl.) are highly polymorphic and transferable to peach and almond. Mol Ecol Notes 4:163–166

    Article  CAS  Google Scholar 

  • Moyle LC, Graham EB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169:355–373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moyle LC, Nakazato T (2008) Comparative genetics of hybrid incompatibility: sterility in two Solanum species crosses. Genetics 179:1437–1453

    Article  PubMed Central  PubMed  Google Scholar 

  • Oginuma K (1977) Karyomorphological speculation on the origin of Prunus × yedoensis ‘Yedoensis’. Bull Biol Soc Hiroshima Univ 43:53–55 (in Japanese with English summary)

    Google Scholar 

  • Oginuma K, Tanaka R (1976) Karyomorphological studies on some cherry trees in Japan. J Japan Bot 51:104–109

    Google Scholar 

  • Ohba H, Kawasaki T, Tanaka H (2007) Flowering cherries of Japan, Newth edn. Yama-kei Publishers, Tokyo (in Japanese)

    Google Scholar 

  • Ohta S, Katsuki T, Tanaka T, Hayashi T, Sato Y, Yamamoto T (2005) Genetic variation in flowering cherries (Prunus subgenus Cerasus) characterized by SSR markers. Breed Sci 55:415–424

    Article  CAS  Google Scholar 

  • Ohta S, Osumi S, Katsuki T, Nakamura I, Yamamoto T, Sato Y (2006) Genetic characterization of flowering cherries (Prunus subgenus Cerasus) using rpl16-rpl14 spacer sequences of chloroplast DNA. J Japan Soc Hort Sci 75:72–78

    Article  CAS  Google Scholar 

  • Ohta S, Yamamoto T, Nishitani C, Katsuki T, Iketani H, Omura M (2007) Phylogenetic relationships among Japanese flowering cherries (Prunus subgenus Cerasus) based on nucleotide sequences of chloroplast DNA. Plant Syst Evol 263:209–225

    Article  CAS  Google Scholar 

  • Olmstead JW, Sebolt AM, Cabrera A, Sooriyapathirana SS, Hammar S, Iriarte G, Wang D, Chen CY, van der Knaap E, Iezzoni AF (2008) Construction of an intra-specific sweet cherry (Prunus avium L.) genetic linkage map and synteny analysis with the Prunus reference map. Tree Genet Genome 4:897–910

    Article  Google Scholar 

  • Orr HA (1996) Dobzhansky, Bateson, and the genetics of speciation. Genetics 144:1331–1335

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sosinski B, Gannavarapu M, Hager LD, Beck LE, King GJ, Ryder CD, Rajapakse S, Baird WV, Ballard RE, Abbott AG (2000) Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 101:421–428

    Article  CAS  Google Scholar 

  • Sweigart AL, Fishman L, Willis JH (2006) A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172:2465–2479

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Testolin R, Marrazzo T, Cipriani G, Quarta R, Verde I, Dettori MT, Pancaldi M, Sansavini S (2000) Microsatellite DNA in peach (Prunus persica L. Batsch) and its use in fingerprinting and testing the genetic origin of cultivars. Genome 43:512–520

    Article  CAS  PubMed  Google Scholar 

  • Tsuda Y, Ueno S, Kato S, Katsuki T, Mukai Y, Tsumura Y (2009) Development of 13 EST-SSRs for Cerasus jamasakura and their transferability for Japanese flowering cherries. Conserv Genet 10:685–688

    Article  CAS  Google Scholar 

  • Tsuruta M, Ishikawa H, Kato S, Mukai Y (2012a) Estimation of the hybridization range between cv. Somei-yoshino and wild flowering cherries, and the factors influencing inter-specific gene flow. J Jpn For Soc 94:229–235 (in Japanese with English summary)

    Article  Google Scholar 

  • Tsuruta M, Wang C, Mukai Y (2012b) Self-incompatibility and stages of a cross-compatible difference in the flowering cherry, ‘Somei-yoshino’. Hort Res (Japan) 11:321–325 (in Japanese with English summary)

    Article  Google Scholar 

  • Vaughan SP, Russell K (2004) Characterization of novel microsatellites and development of multiplex PCR for large-scale population studies in wild cherry, Prunus avium. Mol Ecol Notes 4:429–431

    Article  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  PubMed  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 

  • Wang S, Basten CJ, Zeng ZB (2012) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC

  • Watanabe K, Yoshikawa K (1967) Notes on variation and self-incompatibility in Japanese flowering cherries. Bot Mag Tokyo 80:257–260

    Article  Google Scholar 

  • Wilson EH (1916) The cherries of Japan. University press, Cambridge

    Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H et al (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamamoto E, Takashi T, Morinaka Y, Lin S, Kitano H, Matsuoka M, Ashikari M (2007) Interaction of two recessive genes, hbd2 and hbd3, induces hybrid breakdown in rice. Theor Appl Genet 115:187–194

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto E, Takashi T, Morinaka Y, Lin S, Wu J, Matsumoto T, Kitano H, Matsuoka M, Ashikari M (2010) Gain of deleterious function causes an autoimmune response and Bateson-Dobzhansky-Muller incompatibility in rice. Mol Genet Genomics 283:305–315

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Sasakawa Scientific Research Grant from The Japan Science Society.

Data archiving statement

Genetic linkage maps of Somei-yoshino (CY) and C. spachiana (E750) are currently being prepared for submitting to Genome Database for Rosaceae (www.rosaceae.org).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Momi Tsuruta.

Additional information

Communicated by E. Dirlewanger

This article is part of the Topical Collection on Genome Biology

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 117 kb)

ESM 2

(PDF 133 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsuruta, M., Mukai, Y. Hybrid seedling inviability locus (HIs1) mapped on linkage group 4 of the Japanese flowering cherry, Cerasus × yedoensis ‘Somei-yoshino’. Tree Genetics & Genomes 11, 88 (2015). https://doi.org/10.1007/s11295-015-0910-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-015-0910-x

Keywords

Navigation