Advertisement

Plant Molecular Biology Reporter

, Volume 36, Issue 4, pp 643–652 | Cite as

Identification of QTLs Associated with Conversion of Sucrose to Hexose in Mature Fruit of Japanese Pear

  • Sogo Nishio
  • Toshihiro Saito
  • Shingo Terakami
  • Norio Takada
  • Hidenori Kato
  • Akihiro Itai
  • Toshiya Yamamoto
Original Paper

Abstract

Sweetness is the most important trait for fruit breeding and is fundamentally determined by both total and individual sugar contents. We analyzed the contents of sucrose, fructose, glucose, and sorbitol in mature fruit in an F1 population derived from crossing modern Japanese pear cultivar ‘Akizuki’ and breeding line ‘373-55’. A genetic linkage map was constructed using simple sequence repeats (SSRs) and single-nucleotide polymorphisms (SNP). We identified two regions associated with individual sugar contents on linkage group (LG) 1 and LG 7. The percentages of the variance in sucrose, fructose, and glucose explained by the quantitative trait loci (QTLs) were 26.6, 15.9, and 18.5%, respectively, for the region on LG 1, and 22.2, 20.0, and 9.5%, respectively, for the region on LG 7. In both regions, genotypes associated with increases in sucrose were associated with decreases in both fructose and glucose. The 1.5-LOD support intervals of the QTLs on LGs 1 and 7 include SSRs within the regions flanking acid invertase genes PPAIV3 and PPAIV1, respectively. Because acid invertase is a key enzyme in the conversion of sucrose to hexose, these are promising candidates for genes underlying those QTLs and controlling individual sugar contents. We also found one region on LG 11 that explained 21.4% of the variation in total sugar content but was not significantly associated with variation for individual sugars. The information obtained in this study will accelerate research and breeding programs to improve fruit sweetness.

Keywords

Pyrus pyrifolia Fruit quality Sugars Acid invertase 

Notes

Acknowledgments

We are deeply indebted to all the people involved in the Japanese pear breeding program at the Institute of Fruit Tree and Tea Science, NARO.

Supplementary material

11105_2018_1106_MOESM1_ESM.pdf (383 kb)
Supplementary Fig. 1 Distributions of individual sugars in an F1 population derived from crossing ‘Akizuki’ and ‘373-55’ (PDF 383 kb)
11105_2018_1106_MOESM2_ESM.pdf (380 kb)
Supplementary Fig. 2 Linkage maps of ‘Akizuki’, ‘373-55’, and their integrated map. “CP” indicates that the integrated LG maps were built using the cross-pollination mode of JoinMap v. 4.1. Markers with segregation distortion are identified by asterisks (*P < 0.05; **P < 0.01; ***P < 0.001) (PDF 380 kb)
11105_2018_1106_MOESM3_ESM.pdf (1.9 mb)
Supplementary Fig. 3 Significant QTLs for sucrose (SUC), fructose (FRU), glucose (GLU), sorbitol (SOR), and total sugar content (TSC). “CP” indicates that the integrated maps were built using the cross-pollination mode of JoinMap v. 4.1. Marker loci and significant QTLs are shown to the right of the linkage groups. Boxes and range lines indicate 1-LOD and 1.5-LOD support intervals, respectively. Markers with segregation distortion are identified by asterisks (*P < 0.05; **P < 0.01; ***P < 0.001) (PDF 1995 kb)
11105_2018_1106_MOESM4_ESM.xlsx (101 kb)
ESM 1 (XLSX 101 kb)

References

  1. Byrne DH, Nikolic AN, Burns EE (1991) Variability in sugars, acids, firmness, and color characteristics of 12 peach genotypes. J Am Soc Hortic Sci 116:1004–1006Google Scholar
  2. Celton JM, Tustin DS, Chagne D, Gardiner SE (2009) Construction of a dense genetic linkage map for apple rootstocks using SSRs developed from Malus ESTs and Pyrus genomic sequences. Tree Genet Genomes 5:93–107CrossRefGoogle Scholar
  3. Chen H, Song Y, Li L-T, Khan MA, Li X-G, Korban SS, Wu J, Zhang S-L (2015a) Construction of a high-density simple sequence repeat consensus genetic map for pear (Pyrus spp.). Plant Mol Biol Report 33:316–325CrossRefGoogle Scholar
  4. Chen J, Wang N, Fang LC, Liang ZC, Li SH, Wu BH (2015b) Construction of a high-density genetic map and QTLs mapping for sugars and acids in grape berries. BMC Plant Biol 15:28CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cirilli M, Bassi D, Ciacciulli A (2016) Sugars in peach fruit: a breeding perspective. Hortic Res 3:15067CrossRefPubMedPubMedCentralGoogle Scholar
  6. Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R, Di Pierro EA, Gouzy J, Rees DJG, Guérif P, Muranty H, Durel CE, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, van de Weg E, Troggio M, Bucher E (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106CrossRefPubMedGoogle Scholar
  7. Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A, Plomion C, Monet R (1999) Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet 98:18–31CrossRefGoogle Scholar
  8. Dondini L, Pierantoni L, Gaiotti F, Chiodini R, Tartarini S, Bazzi C, Sansavini S (2005) Identifying QTLs for fire-blight resistance via a European pear (Pyrus communis L.) genetic linkage map. Mol Breed 14:407–418CrossRefGoogle Scholar
  9. Doty T (1976) Fructose sweetness: a new dimension. Cereal Foods World 21:62–63Google Scholar
  10. Etienne C, Rothan C, Moing A, Plomion C, Bodenes C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159CrossRefPubMedGoogle Scholar
  11. Fernández-Fernández F, Harvey N, James C (2006) Isolation and characterization of polymorphic microsatellite markers from European pear (Pyrus communis L.). Mol Ecol Resour 6:1039–1041CrossRefGoogle Scholar
  12. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedPubMedCentralGoogle Scholar
  13. Guan Y, Peace C, Rudell D, Verma S, Evans K (2015) QTLs detected for individual sugars and soluble solids content in apple. Mol Breed 35:135CrossRefGoogle Scholar
  14. Guilford P, Prakash S, Zhu J, Rikkerink E, Gardiner S, Bassett H, Forster R (1997) Microsatellites in Malus x domestica (apple): abundance, polymorphism and cultivar identification. Theor Appl Genet 94:249–254CrossRefGoogle Scholar
  15. Hecke K, Herbinger K, Veberic R, Trobec M, Toplak H, Stampar F, Keppel H, Grill D (2006) Sugar-, acid- and phenol contents in apple cultivars from organic and integrated fruit cultivation. Eur J Clin Nutr 60:1136–1140CrossRefPubMedGoogle Scholar
  16. Hyun TK, Eom SH, Kim JS (2011) Genomic analysis and gene structure of the two invertase families in the domesticated apple (Malus x domestica Borkh.). Plant Omics 4:391–399Google Scholar
  17. Iketani H, Yamamoto T, Katayama H, Uematsu C, Mase N, Sato Y (2010) Introgression between native and prehistorically naturalized (archaeophytic) wild pear (Pyrus spp.) populations in Northern Tohoku, Northeast Japan. Conserv Genet 11:115–126CrossRefGoogle Scholar
  18. Iketani H, Katayama H, Uematsu C, Mase N, Sato Y, Yamamoto T (2012) Genetic structure of East Asian cultivated pears (Pyrus spp.) and their reclassification in accordance with the nomenclature of cultivated plants. Plant Syst Evol 298:1689–1700CrossRefGoogle Scholar
  19. Illa E, Sargent DJ, Girona EL, Bushakra J, Cestaro A, Crowhurst R, Pindo M, Cabrera A, van der Knaap E, Iezzoni A, Gardiner S, Velasco R, Arus P, Chagne D, Troggio M (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11Google Scholar
  20. Ishimizu T, Inoue K, Shimonaka M, Saito T, Terai O, Norioka S (1999) PCR-based method for identifying the S-genotypes of Japanese pear cultivars. Theor Appl Genet 98:961–967CrossRefGoogle Scholar
  21. Iwata H, Hayashi T, Terakami S, Takada N, Sawamura Y, Yamamoto T (2013) Potential assessment of genome-wide association study and genomic selection in Japanese pear Pyrus pyrifolia. Breed Sci 63:125–140CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jung S, Cestaro A, Troggio M, Main D, Zheng P, Cho I, Folta KM, Sosinski B, Abbott A, Celton J-M (2012) Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies. BMC Genomics 13:129CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kajiura I, Suzuki K, Yamazaki T (1975) Color chart for Japanese pear (Pyrus serotina var. culta Rehder). HortScience 10:257–258Google Scholar
  24. Kajiura I, Yamaki S, Omura M, Akihama T, Machida Y (1979) Improvement of sugar content and composition in fruits, and classifications of East Asian pears by the principal component analysis of sugar compositions in fruits. Jpn J Breed 29:1–12CrossRefGoogle Scholar
  25. Kanayama Y (2017) Sugar metabolism and fruit development in the tomato. Hortic J 86:417–425CrossRefGoogle Scholar
  26. Katayama H, Adachi S, Yamamoto T, Uematsu C (2007) A wide range of genetic diversity in pear (Pyrus ussuriensis var. aromatica) genetic resources from Iwate, Japan revealed by SSR and chloroplast DNA markers. Genet Resour Crop Evol 54:1573–1585CrossRefGoogle Scholar
  27. Kenis K, Keulemans J, Davey MW (2008) Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes 4:647–661CrossRefGoogle Scholar
  28. Kikuchi A (1948) Horticulture of fruit trees, vol 1. Yokendo, TokyoGoogle Scholar
  29. Kliewer WM (1966) Sugars and organic acids of Vitis vinifera. Plant Physiol 41:923–931CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175CrossRefGoogle Scholar
  31. Kotobuki K, Saito T, Machida Y, Sato Y, Abe K, Kurihara A, Ogata T, Terai O, Nishibata T, Kozono T, Fukuda H, Kihara T, Suzuki K (2002) New Japanese pear cultivar ‘Akizuki’. Bull Natl Inst Fruit Tree Sci 1:11–21 (In Japanese with English abstract)Google Scholar
  32. Kunihisa M, Moriya S, Abe K, Okada K, Haji T, Hayashi T, Kim H, Nishitani C, Terakami S, Yamamoto T (2014) Identification of QTLs for fruit quality traits in Japanese apples: QTLs for early ripening are tightly related to preharvest fruit drop. Breed Sci 64:240–251CrossRefPubMedPubMedCentralGoogle Scholar
  33. Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993CrossRefPubMedPubMedCentralGoogle Scholar
  34. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760CrossRefPubMedPubMedCentralGoogle Scholar
  35. Li M, Feng F, Cheng L (2012) Expression patterns of genes involved in sugar metabolism and accumulation during apple fruit development. PLoS One 7:e33055CrossRefPubMedPubMedCentralGoogle Scholar
  36. Liebhard R, Gianfranceschi L, Koller B, Ryder C, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol Breed 10:217–241CrossRefGoogle Scholar
  37. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526CrossRefPubMedGoogle Scholar
  38. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12CrossRefGoogle Scholar
  39. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefPubMedPubMedCentralGoogle Scholar
  40. Moriguchi T, Ishizawa Y, Sanada T (1990a) Differences in sugar composition in Prunus persica fruit and the classification by the principal component analysis. J Jpn Soc Hortic Sci 59:307–312CrossRefGoogle Scholar
  41. Moriguchi T, Sanada T, Yamaki S (1990b) Seasonal fluctuations of some enzymes relating to sucrose and sorbitol metabolism in peach fruit. J Am Soc Hortic Sci 115:278–281Google Scholar
  42. Moriguchi T, Abe K, Sanada T, Yamaki S (1992) Levels and role of sucrose synthase, sucrose-phosphate synthase, and acid invertase in sucrose accumulation in fruit of Asian pear. J Am Soc Hortic Sci 117:274–278Google Scholar
  43. Moriya S, Iwanami H, Kotoda N, Haji T, Okada K, Terakami S, Mimida N, Yamamoto T, Abe K (2012) Aligned genetic linkage maps of apple rootstock cultivar ‘JM7’ and Malus sieboldii ‘Sanashi 63’ constructed with novel EST–SSRs. Tree Genet Genomes 8:709–723CrossRefGoogle Scholar
  44. Nishio S, Hayashi T, Yamamoto T, Yamada M, Takada N, Kato H, Nishitani C, Saito T (2016a) Validation of molecular markers associated with fruit ripening day of Japanese pear (Pyrus pyrifolia Nakai) using variance components. Sci Hortic 199:9–14CrossRefGoogle Scholar
  45. Nishio S, Takada N, Saito T, Yamamoto T, Iketani H (2016b) Estimation of loss of genetic diversity in modern Japanese cultivars by comparison of diverse genetic resources in Asian pear (Pyrus spp.). BMC Genet 17:81CrossRefPubMedPubMedCentralGoogle Scholar
  46. Nishitani C, Terakami S, Sawamura Y, Takada N, Yamamoto T (2009) Development of novel EST-SSR markers derived from Japanese pear (Pyrus pyrifolia). Breed Sci 59:391–400CrossRefGoogle Scholar
  47. Okada K, Tonaka N, Moriya Y, Norioka N, Sawamura Y, Matsumoto T, Nakanishi T, Takasaki-Yasuda T (2008) Deletion of a 236 kb region around S4-RNase in a stylar-part mutant S4 sm-haplotype of Japanese pear. Plant Mol Biol 66:389–400CrossRefPubMedGoogle Scholar
  48. Ozaki K, Uchida A, Takabe T, Shinagawa F, Tanaka Y, Takabe T, Hayashi T, Hattori T, Rai AK, Takabe T (2009) Enrichment of sugar content in melon fruits by hydrogen peroxide treatment. J Plant Physiol 166:569–578CrossRefPubMedGoogle Scholar
  49. Pancoast HM, Junk WR (1980) Handbook of sugars. AVI Publishing Co., Westport, pp 387–389Google Scholar
  50. Pangborn R (1963) Relative taste intensities of selected sugars and organic acids. J Food Sci 28:726–733CrossRefGoogle Scholar
  51. Quilot B, Wu BH, Kervella J, Genard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897CrossRefPubMedGoogle Scholar
  52. Saito T (2016) Advances in Japanese pear breeding in Japan. Breed Sci 66:46–59CrossRefPubMedPubMedCentralGoogle Scholar
  53. Salazar JA, Ruiz D, Campoy JA, Sánchez-Pérez R, Crisosto CH, Martínez-García PJ, Blenda A, Jung S, Main D, Martínez-Gómez P (2014) Quantitative trait loci (QTL) and Mendelian trait loci (MTL) analysis in Prunus: a breeding perspective and beyond. Plant Mol Biol Report 32:1–18CrossRefGoogle Scholar
  54. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116CrossRefPubMedGoogle Scholar
  55. Silfverberg-Dilworth E, Matasci C, Van de Weg W, Van Kaauwen M, Walser M, Kodde L, Soglio V, Gianfranceschi L, Durel C, Costa F (2006) Microsatellite markers spanning the apple (Malus x domestica Borkh.) genome. Tree Genet Genomes 2:202–224CrossRefGoogle Scholar
  56. Tamura F (2006) Japanese pear. In: Jpn Soc Hort Sci (ed) Horticulture in Japan 2006. Shoukadoh Publication, Kyoto, pp. 50–58Google Scholar
  57. Terakami S, Shoda M, Adachi Y, Gonai T, Kasumi M, Sawamura Y, Iketani H, Kotobuki K, Patocchi A, Gessler C, Hayashi T, Yamamoto T (2006) Genetic mapping of the pear scab resistance gene Vnk of Japanese pear cultivar Kinchaku. Theor Appl Genet 113:743–752CrossRefPubMedGoogle Scholar
  58. Terakami S, Adachi Y, Iketani H, Sato Y, Sawamura Y, Takada N, Nishitani C, Yamamoto T (2007) Genetic mapping of genes for susceptibility to black spot disease in Japanese pears. Genome 50:735–741CrossRefPubMedGoogle Scholar
  59. Terakami S, Kimura T, Nishitani C, Sawamura Y, Saito T, Hirabayashi T, Yamamoto T (2009) Genetic linkage map of the Japanese pear ‘Housui’ identifying three homozygous genomic regions. J Jpn Soc Hortic Sci 78:417–424CrossRefGoogle Scholar
  60. Terakami S, Nishitani C, Kunihisa M, Shirasawa K, Sato S, Tabata S, Kurita K, Kanamori H, Katayose Y, Takada N, Saito T, Yamamoto T (2014) Transcriptome-based single nucleotide polymorphism markers for genome mapping in Japanese pear (Pyrus pyrifolia Nakai). Tree Genet Genomes 10:853–863CrossRefGoogle Scholar
  61. van Dyk MM, Soeker MK, Labuschagne IF, Rees DJG (2010) Identification of a major QTL for time of initial vegetative budbreak in apple (Malus x domestica Borkh.). Tree Genet Genomes 6:489–502CrossRefGoogle Scholar
  62. Van Ooijen J (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, WageningenGoogle Scholar
  63. Van Ooijen J (2009) MapQTL® 6, Software for the mapping of quantitative trait in experiment populations of diploid species. Kyazma B V, WageningenGoogle Scholar
  64. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica). Nat Genet 42:833–841CrossRefPubMedGoogle Scholar
  65. Verde I, Bassil N, Scalabrin S, Gilmore B, Lawley CT, Gasic K, Micheletti D, Rosyara UR, Cattonaro F, Vendramin E, Main D, Aramini V, Blas AL, Mockler TC, Bryant DW, Wilhelm L, Troggio M, Sosinski B, Aranzana MJ, Arús P, Iezzoni A, Morgante M, Peace C (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494CrossRefPubMedGoogle Scholar
  66. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefPubMedGoogle Scholar
  67. Wu J, Gao H, Zhao L, Liao X, Chen F, Wang Z, Hu X (2007) Chemical compositional characterization of some apple cultivars. Food Chem 103:88–93CrossRefGoogle Scholar
  68. Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wu J, Li LT, Li M, Khan MA, Li XG, Chen H, Yin H, Zhang SL (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781CrossRefPubMedPubMedCentralGoogle Scholar
  70. Yamaki S (2010) Metabolism and accumulation of sugars translocated to fruit and their regulation. J Jpn Soc Hortic Sci 79:1–15CrossRefGoogle Scholar
  71. Yamaki S, Moriguchi T (1989) Seasonal fluctuation of sorbitol-related enzymes and invertase activities accompanying maturation of Japanese pear (Pyrus serotina Rehder var. culta Rehder) fruit. J Jpn Soc Hortic Sci 57:602–607CrossRefGoogle Scholar
  72. Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18CrossRefPubMedGoogle Scholar
  73. Yamamoto T, Kimura T, Terakami S, Nishitani C, Sawamura Y, Saito T, Kotobuki K, Hayashi T (2007) Integrated reference genetic linkage maps of pear based on SSR and AFLP markers. Breed Sci 57:321–329CrossRefGoogle Scholar
  74. Yamamoto T, Terakami S, Takada N, Nishio S, Onoue N, Nishitani C, Kunihisa M, Inoue E, Iwata H, Hayashi T, Itai A, Saito T (2014) Identification of QTLs controlling harvest time and fruit skin color in Japanese pear (Pyrus pyrifolia Nakai). Breed Sci 64:351–361CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zhang R, Wu J, Li X, Khan MA, Chen H, Korban SS, Zhang S (2013) An AFLP, SRAP, and SSR genetic linkage map and identification of QTLs for fruit traits in pear (Pyrus L.). Plant Mol Biol Report 31:678–687CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Sogo Nishio
    • 1
  • Toshihiro Saito
    • 1
  • Shingo Terakami
    • 1
  • Norio Takada
    • 1
  • Hidenori Kato
    • 1
  • Akihiro Itai
    • 2
  • Toshiya Yamamoto
    • 1
  1. 1.Institute of Fruit Tree and Tea ScienceNAROTsukubaJapan
  2. 2.Graduate School of Life and Environmental SciencesKyoto Prefectural UniversitySeikaJapan

Personalised recommendations