Abstract
Fruit skin type is one of the most important components of fruit appearance. Pears have three types of fruit skin—russet, intermediate, and smooth—depending on the extent of the cork layer on the epicarp. Russet type is controlled by a dominant genetic factor, R, and a quantitative trait locus (QTL) associated with fruit skin type has been identified on chromosome 8. Although some markers have been developed, the relationship between their alleles and fruit skin type has not been established across multiple cultivars; thus, the effectiveness of these markers in marker-assisted selection (MAS) has not been demonstrated. In this study, haplotypes of 93 accessions estimated by Beagle 4.0 were classified into the major haplotypes HAP1–HAP8 using new simple sequence repeat (SSR) markers Psc07, Psc34, and Psc03. Out of the eight haplotypes, HAP1–HAP7 were found in Japanese pear, whereas HAP8 was specific to Chinese pear. By comparing the haplotypes and phenotypes of accessions and F1 populations, we found that HAP1–HAP3 and HAP7 had dominant effects and promoted cork layer formation, whereas HAP4–HAP6 and HAP8 were recessive and did not contribute to russeting. All eight haplotypes can be distinguished completely by Psc07 and Psc03, which would be useful for MAS. This information on haplotype structure of accessions and molecular markers associated with fruit skin type will be useful for future pear breeding programs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Banno K, Ishikawa H, Hamauzu Y, Tabira H (1999) Identification of a RAPD marker linked to the susceptible gene of black spot disease in Japanese pear. J Japan Soc Hort Sci 3:476–481. https://doi.org/10.2503/jjshs.68.476
Bao L, Chen K, Zhang D, Li X, Teng Y (2008) An assessment of genetic variability and relationships within Asian pears based on AFLP (amplified fragment length polymorphism) markers. Sci Hortic (Amsterdam) 116:374–380. https://doi.org/10.1016/j.scienta.2008.02.008
Bell RL, Itai A (2011) Chapter 8 Pyrus. In: Wild crop relatives: genomic and breeding resources: temperate fruits. Pp 147–177
Bell RL, Quamm HA, Layne REC, Skirvin RM (1996) PEARS. In: Jack J, Moore JN (eds) Fruit breeding volume 1: tree and tropical fruits. John Wiley. Ind, New York, pp 441–514
Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097. https://doi.org/10.1086/521987
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010. https://doi.org/10.2144/96206st01
Dirlewanger E, Graziano E, Joobeur T, et al (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops 101:9891–9896. https://doi.org/10.1073/pnas.0307937101
Dondini L, Sansavini S (2012) European pear. In: Badenes ML, Byrne DH (eds) Fruit Breeding. Springer, Boston, pp 369–413
Fernández-Fernández F, Harvey NG, James CM (2006) Isolation and characterization of polymorphic microsatellite markers from European pear (Pyrus communis L.). Mol Ecol Notes 6:1039–1041. https://doi.org/10.1111/j.1471-8286.2006.01422.x
FAOSTAT (2018) http://www.fao.org/faostat/en/#data/QC accessed November 19, 2020
Heng W, Liu L, Wang M, Jia B, Liu P, Ye ZF, Zhu LW (2014) Differentially expressed genes related to the formation of russet fruit skin in a mutant of “Dangshansuli” pear (Pyrus bretschnederi Rehd.) determined by suppression subtractive hybridization. Euphytica 196:285–297. https://doi.org/10.1007/s10681-013-1032-x
Iketani H, Abe K, Yamamoto T, Kotobuki K, Sato Y, Saito T, Terai O, Matsuta N, Hayashi T (2001) Mapping of disease-related genes in Japanese pear using a molecular linkage bap with RAPD markers. Breed Sci 51:179–184. https://doi.org/10.1270/jsbbs.51.179
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 298:1689–1700. https://doi.org/10.1007/s00606-012-0670-0
Inoue E, Kasumi M, Sakuma F, Anzai H, Amano K, Hara H (2006) Identification of RAPD marker linked to fruit skin color in Japanese pear (Pyrus pyrifolia Nakai). Sci Hortic (Amsterdam) 107:254–258. https://doi.org/10.1016/j.scienta.2005.07.009
Ishimizu T, Mitsukami Y, Shinkawa T, Natsuka S, Hase S, Miyagi M, Sakiyama F, Norioka S (1999) Presence of asparagine-linked N-acetylglucosamine and chitobiose in Pyrus pyrifolia S-RNases associated with gametophytic self-incompatibility. Eur J Biochem 263:624–634. https://doi.org/10.1046/j.1432-1327.1999.00499.x
Itai A, Kotaki T, Tanabe K, Tamura F, Kawaguchi D, Fukuda M (2003) Rapid identification of 1-aminocyclopropane-1-carboxylate (ACC) synthase genotypes in cultivars of Japanese pear (Pyrus pyrifolia Nakai) using CAPS markers. Theor Appl Genet 106:1266–1272. https://doi.org/10.1007/s00122-002-1186-8
Jové P, Olivella MÀ, Laura Cano (2011) Study of the variability in chemical composition of bark layers of Quercus suber L. from different production areas. BioResources 6:1806–1815. https://doi.org/10.15376/biores.6.2.1806-1815
Kajiura I, Sato Y (1990) Recent progress in Japanese pear (Pyrus pyrifolia Nakai) breeding, and descriptions of cultivars based on a literature review. Bull fruit tree res Stn extra no.1:
Kikuti A (1924) On the origin of Japanese pears and the inheritance of the skin colours of their fruits. J Genet 3:1–27
Kikuti A (1930) On skin color of the Japanese pear and its inheritance (in Japanese). Contr Inst Plant Ind 8:1–50
Legay S, Guerriero G, Deleruelle A, Lateur M, Evers D, André CM, Hausman JF (2015) Apple russeting as seen through the RNA-seq lens: strong alterations in the exocarp cell wall. Plant Mol Biol 88:21–40. https://doi.org/10.1007/s11103-015-0303-4
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus x domestica Borkh.). Mol Breed 10:217–241. https://doi.org/10.1023/A:1020525906332
Linsmith G, Rombauts S, Montanari S et al (2019) Pseudo-chromosome length genome assembly of a double haploid ‘Bartlett’ pear (Pyrus communis L.). bioRxiv. https://doi.org/10.1093/gigascience/giz138
Luby JJ, Shaw DV (2000) Does marker-assisted selection make dollars and sense in a fruit breeding program: molecular genetics: applications in small and tree fruits: where is it working. HortScience 36:872–879
Minamikawa MF, Takada N, Terakami S, Saito T, Onogi A, Kajiya-Kanegae H, Hayashi T, Yamamoto T, Iwata H (2018) Genome-wide association study and genomic prediction using parental and breeding populations of Japanese pear (Pyrus pyrifolia Nakai). Sci Rep 8:11994. https://doi.org/10.1038/s41598-018-30154-w
Mori H (1953) Studies on the inheritance of the main characteristics of deciduous fruit trees (peach, Japanese pear and Japanese persimmon). Agric Sci E 2:1–66
Nashima K, Terakami S, Nishio S, Kunihisa M, Nishitani C, Saito T, Yamamoto T (2015) S-genotype identification based on allele-specific PCR in Japanese pear. Breed Sci 65:208–215. https://doi.org/10.1270/jsbbs.65.208
Nishio S, Takada N, Saito T, Yamamoto T, Iketani H (2016) Estimation of loss of genetic diversity in modern Japanese cultivars by comparison of diverse genetic resources in Asian pear (Pyrus spp.). BMC Genet 17:1–12. https://doi.org/10.1186/s12863-016-0380-7
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 59:391–400. https://doi.org/10.1270/jsbbs.59.391
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 S4sm-haplotype of Japanese pear. Plant Mol Biol 66:389–400. https://doi.org/10.1007/s11103-007-9277-1
Pereira H (1988) Chemical composition and variability of cork from Quercus suber L. Wood Sci Technol 22:211–218. https://doi.org/10.1007/BF00386015
Saito T (2016) Advances in Japanese pear breeding in Japan. Breed Sci 66:46–59. https://doi.org/10.1270/jsbbs.66.46
Sawamura Y, Saito T, Takada N, Yamamoto T, Kimura T, Hayashi T, Kotobuki K (2004) Identification of parentage of Japanese pear “Housui.” J Japan Soc Hort Sci 73:511–518 https://doi.org/10.2503/jjshs.73.511, Identification of Parentage of Japanese Pear 'Housui'
Teng Y, Tanabe K (2004) Reconsideration on the origin of cultivated pears native to East Asia. Acta Hortic 634:175–182. https://doi.org/10.17660/ActaHortic.2004.634.21
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 50:735–741. https://doi.org/10.1139/G07-053
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 113:743–752. https://doi.org/10.1007/s00122-006-0344-9
Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422. https://doi.org/10.1007/s00122-002-1031-0
Van Inghelandt D, Melchinger AE, Lebreton C, Stich B (2010) Population structure and genetic diversity in a commercial maize breeding program assessed with SSR and SNP markers. Theor Appl Genet 120:1289–1299. https://doi.org/10.1007/s00122-009-1256-2
Visser T (1964) Juvenile phase and growth of apple and pear seedlings. Euphytica 13:119–129. https://doi.org/10.1007/BF00033299
Wang YZ, Dai MS, Cai DY, Zhang S, Shi ZB (2016) A review for the molecular research of russet/semi-russet of sand pear exocarp and their genetic characters. Sci Hortic (Amsterdam) 210:138–142. https://doi.org/10.1016/j.scienta.2016.07.019
Wang YZ, Zhang S, Dai MS, Shi ZB (2014a) Pigmentation in sand pear (Pyrus pyrifolia) fruit: biochemical characterization, gene discovery and expression analysis with exocarp pigmentation mutant. Plant Mol Biol 85:123–134. https://doi.org/10.1007/s11103-014-0173-1
Wang YZ, Dai MS, Zhang SJ, Shi ZB (2014b) Exploring candidate genes for pericarp russet pigmentation of sand pear (Pyrus pyrifolia) via RNA-seq data in two genotypes contrasting for pericarp color. PLoS One 9:e83675. https://doi.org/10.1371/journal.pone.0083675
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 23:396–408. https://doi.org/10.1101/gr.144311.112
Xue H, Wang S, Yao JL, et al (2018) Chromosome level high-density integrated genetic maps improve the Pyrus bretschneideri “DangshanSuli” v1.0 genome. BMC genomics 19:833. https://doi.org/10.1186/s12864-018-5224-6
Yamamoto T, Kimura T, Shoda M, Ban Y, Hayashi T, Matsuta N (2002) Development of microsatellite markers in the Japanese pear (Pyrus pyrifolia Nakai). Mol Ecol Notes 2:14–16. https://doi.org/10.1046/j.1471-8286.2002.00128.x
Yamamoto T, Terakami S, Moriya S, et al (2013) DNA markers developed from genome sequencing analysis in Japanese pear (Pyrus pyrifolia). Acta Hortic 976:477–484. https://doi.org/10.17660/actahortic.2013.976.67
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 64:351–361. https://doi.org/10.1270/jsbbs.64.351
Yue X, Zheng X, Zong Y, Jiang S, Hu C, Yu P, Liu G, Cao Y, Hu H, Teng Y (2018) Combined analyses of chloroplast DNA haplotypes and microsatellite markers reveal new insights into the origin and dissemination route of cultivated pears native to East Asia. Front Plant Sci 9:1–16. https://doi.org/10.3389/fpls.2018.00591
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.
Funding
This work is supported by the Institute of Fruit Tree and Tea Science, NARO.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation and data collection were performed by Yukie Takeuchi, Sogo Nishio, Shingo Terakami, Norio Takada, Hidenori Kato, and Toshihiro Saito. Formal analysis and data curation were performed by Yukie Takeuchi, Sogo Nishio, and Shingo Terakami. The first draft of the manuscript was written by Yukie Takeuchi, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Code availability
Not applicable
Additional information
Communicated by D. Chagné
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Supplementary Fig. 1
Association between haplotype combinations and fruit skin-type score in seven F1 populations. (PDF 1857 kb)
Table S1
(XLSX 25 kb)
Table S2
(XLSX 26 kb)
Rights and permissions
About this article
Cite this article
Takeuchi, Y., Nishio, S., Terakami, S. et al. Haplotype structure analysis of a locus associated with fruit skin type on chromosome 8 in Japanese pear. Tree Genetics & Genomes 17, 3 (2021). https://doi.org/10.1007/s11295-020-01483-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-020-01483-7