Современные методы в исследованиях генома персика (Prunus persica)
https://doi.org/10.18699/vjgb-25-39
Аннотация
Персик (Prunus persica (L.) Batsch) – одна из основных сельскохозяйственных плодовых косточковых культур семейства розоцветных. Современная селекция направлена на улучшение качества плодов, расширение сроков их получения, создание сортов с устойчивостью к неблагоприятным условиям среды и снижение общих затрат на производство культивируемых сортов. При этом селекция персика – долгий процесс: от гибридизации родительских форм до получения плодоносящих деревьев проходит 10–15 лет. Исследования сор тов персика как доноров желаемых признаков начались с 1980-х годов. Первый вариант генома персика был представлен в 2013 г., и его появление способствовало определению и локализации локусов, с последующим обнаружением генов-кандидатов, под чьим контролем находится хозяйственно ценный признак. Развитие методов NGS ускорило продвижение подходов, основанных на применении диагностических ДНК-маркеров. К таким подходам, позволяющим ускорять процессы классической селекции, относятся маркер-ориентированная селекция и геномная селекция. Для того чтобы разработать ДНК-маркеры, ассоциированные с изучаемыми свойствами, необходимо провести предварительное картирование локусов, контролирующих хозяйственно ценные признаки, создать карты сцепления. Работы по пангеному показали необходимость анализировать большее количество образцов, так как до сих пор не хватает данных для нахождения полиморфных областей генома. Развиваются подходы использования SNP-чипов и методов генотипирования через секвенирование (GBS, genotyping-by-sequencing). В последние годы для обнаружения локусов генома, ассоциированных с хозяйственно ценными признаками, активно применяется метод полногеномного анализа ассоциаций (GWAS, genome-wide association studies), для использования которого требуется скрининг больших выборок сортов по сотням и тысячам SNP. Цель настоящего обзора – систематизация и обобщение основных достижений в области геномных исследований персика за последние 40 лет: построение карт сцепления и физических карт, получение различных молекулярных маркеров, полногеномное секвенирование для персика, а также описание существующих работ полногеномных исследований ассоциаций с маркерами SNP высокой плотности. Этот обзор обеспечивает теоретическую основу для проведения GWAS с целью выявления высокоэффективных маркеров хозяйственно ценных признаков для персика и развития геномной селекции этой культуры.
Об авторах
И. В. РозановаРоссия
Санкт-Петербург
Е. А. Водясова
Россия
п.г.т. Никита, Ялта, Республика Крым
Список литературы
1. Abbott A.G., Georgi L., Yvergniaux D., Wang Y., Blenda A., Reighard G., Inigo M., Sosinski B. Peach: the model genome for Rosaceae. Acta Hortic. 2002;575:145155. doi 10.17660/ActaHortic.2002.575.14
2. Abbott A.G., Arús P., Scorza R. Genetic engineering and genomics. In: Layne D., Bassi D. (Eds) The Peach Botany, Production and Uses. London: CAB International, 2008;85105. doi 10.1079/9781845933869.0085
3. Akagi T., Hanada T., Yaegaki H., Gradziel T.M., Tao R. Genomewide view of genetic diversity reveals paths of selection and cultivar differentiation in peach domestication. DNA Res. 2016;23(3):271282. doi 10.1093/dnares/dsw014
4. Aranzana M.J., Abbassi E.K., Howad W., Arús P. Genetic variation, population structure and linkage disequilibrium in peach commercial varieties. BMC Genet. 2010;11:69. doi 10.1186/147121561169
5. Arulsekar S., Parfitt D.E., Kester D.E. Comparison of isozyme vari ability in peach and almond cultivars. J Hered. 1986a;77(4):272274. doi 10.1093/oxfordjournals.jhered.a110235
6. Arulsekar S., Parfitt D.E., Beres W., Hansche P.E. Genetics of malate dehydrogenase isozymes in the peach. J Hered. 1986b;77(1):4951. doi 10.1093/oxfordjournals.jhered.a110166
7. Arumuganathan K., Earle E.D. Nuclear DNA content of some important plant species. Plant Mol Biol Rep.1991;9:208218. doi 10.1007/BF02672069
8. Bailey J.S., French A.P. The Inheritance of Certain Fruit and Foliage Characters in the Peach. Amherst, MA: University of Massachusetts Press, 1949
9. Bassi D., Monet R. Botany and taxonomy. In: Layne D.R., Bassi D. (Eds) The Peach: Botany, Production and Uses. Wallingford: CAB International, 2008;136. doi 10.1079/9781845933869.0001
10. Batley J., Barker G., O’Sullivan H., Edwards K.J., Edwards D. Mining for single nucleotide polymorphisms and insertions/deletions in maize expressed sequence tag data. Plant Physiol. 2003;132(1): 8491. doi 10.1104/pp.102.019422
11. Belthoff L.E., Ballard R., Abbott A., Morgens P., Callahan A., Scorza R., Baird W.V., Monet R. Development of a saturated linkage map of Prunus persica using molecular based marker systems. Acta Hortic. 1993;336:5156. doi 10.17660/ActaHortic.1993.336.5
12. Bianco L., Cestaro A., Linsmith G., Muranty H., Denancé C., Théron A., Poncet C., … Davassi A., Laurens F., Velasco R., Durel C.E., Troggio M. Development and validation of the Axiom® Apple480K SNP genotyping array. Plant J. 2016;86(1):6274. doi 10.1111/tpj.13145
13. Bielenberg D.G., Rauh B., Fan S., Gasic K., Abbott A.G., Reighard G.L., Okie W.R., Wells C.E. Genotyping by sequencing for SNPbased linkage map construction and QTL analysis of chilling requirement and bloom date in peach [Prunus persica (L.) Batsch]. PloS One. 2015;10(10):e0139406. doi 10.1371/journal.pone.0139406
14. Bliss F.A. Markerassisted breeding in horticultural crops. Acta Hort. 2010;859:339350. doi 10.17660/ActaHortic.2010.859.40
15. Byrne D.H., Sherman W.B., Bacon T.A. Stone fruit genetic pool and its exploitation for growing under warm winter conditions. In: Erez A. (Ed.) Temperate Fruit Crops in Warm Climates. Dordrecht: Springer, 2000;157230. doi 10.1007/9789401732154_8
16. Byrne D.H., Bassols M., Bassi D., Piagnani M., Gasic K., Reighard G., Moreno M., Pérez S. Peach. In: Badenes M.L., Byrne D.H. (Eds) Fruit Breeding. New York: Springer Science, 2012;505570. doi 10.1007/9781441907639_14
17. Callahan A., Scorza R., Morgens P., Mante S., Cordts J., Cohen R. Breeding for cold hardiness: searching for genes to improve fruit quality in cold-hardy peach germplasm. HortScience. 1991;26(5):522526. doi 10.21273/HORTSCI.26.5.522
18. Cao K., Wang L., Zhu G., Fang W., Chen C., Luo J. Genetic diversity, linkage disequilibrium, and association mapping analyses of peach (Prunus persica) landraces in China. Tree Genet Genomes. 2012; 8(5):975990. doi 10.1007/s1129501204778
19. Cao K., Zheng Z., Wang L., Liu X., Zhu G., Fang W., Cheng S., … Li Y., Li H., Guo J., Xu X., Wang J. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 2014;15:415. doi 10.1186/s1305901404151
20. Cao K.E., Zhou Z., Wang Q., Guo J., Zhao P., Zhu G., Fang W., Chen C., Wang X., Wang X., Tian Z., Wang L. Genomewide association study of 12 agronomic traits in peach. Nat Commun. 2016;7(1): 13246. doi 10.1038/ncomms13246
21. Cao K., Li Y., Deng C.H., Gardiner S.E., Zhu G., Fang W., Chen C., Wang X., Wang L. Comparative population genomics identified genomic regions and candidate genes associated with fruit domestication traits in peach. Plant Biotechnol J. 2019;17(10):19541970. doi 10.1111/pbi.13112
22. Cao K., Peng Z., Zhao X., Li Y., Liu K., Arus P., Zhu G., Deng S., Fang W., Chen C., Wang X., Wu J., Fei Z., Wang L. Pangenome analyses of peach and its wild relatives provide insights into the genetics of disease resistance and species adaptation. BioRxiv. 2020. doi 10.1101/2020.07.13.200204
23. Cao K., Yang X., Li Y., Zhu G., Fang W., Chen C., Wang X., Wu J., Wang L. New high‐quality peach (Prunus persica L. Batsch) genome assembly to analyze the molecular evolutionary mechanism of volatile compounds in peach fruits. Plant J. 2021;108(1):281295. doi 10.1111/tpj.15439
24. Carter G.E. Jr., Brock M.M. Identification of peach cultivars through protein analysis. HortScience. 1980;15(3):292293 Cartwright D.A., Troggio M., Velasco R., Gutin A. Genetic mapping in the presence of genotyping errors. Genetics. 2007;176(4):2521 2527. doi 10.1534/genetics.106.063982
25. Chagné D., Crowhurst R.N., Troggio M., Davey M.W., Gilmore B., Lawley C., Vanderzande S., … Wilhelm L., Van de Weg E., Gardiner S.E., Bassil N., Peace C. Genomewide SNP detection, validation, and development of an 8K SNP array for apple. PLoS One. 2012;7(2):e31745. doi 10.1371/journal.pone.0031745
26. Chaparro J.X., Durham R.E., Moore G.A., Sherman W.B. Utilization of isozyme techniques to identify peach × ‘Nonpareil’ almond hybrids. HortScience. 1987;22(2):300302. doi 10.21273/HORTSCI.22.2.300
27. Chaparro J.X., Werner D.J., O’Malley D., Sederoff R.R. Targeted mapping and linkage analysis of morphological isozyme, and RAPD markers in peach. Theor Appl Genet. 1994;87(7):805815. doi 10.1007/BF00221132
28. Chesnokov Yu.V., Artem’eva A.M. Association mapping in plants (review). Sel’ skokhozyaystvennaya Biologiya = Agricultural Bio logy. 2011;46(5):316 (in Russian)
29. Cirilli M., Baccichet I., Chiozzotto R., Silvestri C., Rossini L., Bassi D. Genetic and phenotypic analyses reveal major quantitative loci associated to fruit size and shape traits in a nonflat peach collection (P. persica L. Batsch). Hortic Res. 2021;8:232. doi 10.1038/s41438021006615
30. Collard B.C.Y., Jahufer M.Z.Z., Brouwer J.B., Pang E.C.K. An introduction to da Silva Linge C., Cai L., Fu W., Clark J., Worthington M., Rawandoozi Z., Byrne D.H., Gasic K. Multilocus genomewide association studies reveal fruit quality hotspots in peach genome. Front Plant Sci. 2021;12:644799. doi 10.3389/fpls.2021.644799
31. Demirel S., Pehluvan M., Aslantaş R. Evaluation of genetic diversity and population structure of peach (Prunus persica L.) genotypes using intersimple sequence repeat (ISSR) markers. Genet Resour Crop Evol. 2024;71(3):13011312. doi 10.1007/s10722023016919
32. Dettori M.T., Quarta R., Verde I. A peach linkage map integrating RFLPs, SSRs, RAPDs, and morphological markers. Genome. 2001; 44(5):783790. doi 10.1139/g01065
33. Dirlewanger E., Moing A., Rothan C., Svanella L., Pronier V., Guye A., Plomion C., Monet R. Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet. 1999;98: 1831. doi 10.1007/s001220051035
34. Dirlewanger E., Cosson P., Tavaud M., Aranzana M., Poizat C., Zanetto A., Arús P., Laigret F. 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. 2002;105(1):127138. doi 10.1007/s0012200208677
35. Dirlewanger E., Graziano E., Joobeur T., GarrigaCalderé F., Cosson P., Howad W., Arús P. Comparative mapping and markerassisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA. 2004;101(23): 98919896. doi 10.1073/pnas.0307937101
36. Dirlewanger E., Cosson P., Boudehri K., Renaud C., Capdeville G., Tauzin Y., Laigret F., Moing A. Development of a secondgeneration genetic linkage map for peach [Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genomes. 2007;3:113. doi 10.1007/s1129500600531
37. Dirlewanger E., Claverie J., Iezzoni A.F., Wünsch A. Sweet and sour cherries: linkage maps, QTL detection and marker assisted selection. In: Folta K.M., Gardiner S.E. (Eds) Genetics and Genomics of Rosaceae. Plant Genetics and Genomics: Crops and Models. Vol. 6. New York, NY: Springer, 2009;291313. doi 10.1007/9780387774916_14
38. Dirlewanger E., QueroGarcía J., Le Dantec L., Lambert P., Ruiz D., Dondini L., Illa E., QuilotTurion B., Audergon J.M., Tartarini S., Letourmy P., Arús P. Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity. 2012;109(5): 280292. doi 10.1038/hdy.2012.38
39. Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant pathogen interactions. Nat Rev Genet. 2010;11(8):539548. doi 10.1038/nrg2812
40. Durham R.E., Moore G.A., Sherman W.B. Isozyme banding patterns and their usefulness as genetic markers in peach. J Am Soc Hortic Sci. 1987;112(6):10131018. doi 10.21273/JASHS.112.6.1013
41. Eduardo I., Pacheco I., Chietera G., Bassi D., Pozzi C., Vecchietti A., Rossini L. QTL analysis of fruit quality traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genomes. 2011;7:323335. doi 10.1007/s1129501003346
42. Elsadr H. A genome wide association study of flowering and fruit quality traits in peach [(Prunus persica (L.) Batsch]: Doctoral dissertation. University of Guelph, 2016
43. Elshire R.J., Glaubitz J.C., Sun Q., Poland J.A., Kawamoto K., Buckler E.S., Mitchell S.E. A robust, simple genotypingbysequencing (GBS) aproach for high diversity species. PloS One. 2011;6(5): e19379. doi 10.1371/journal.pone.0019379
44. Faust M., Timon B. Origin and dissemination of the peach. In: Janick J. (Ed.) Horticultural Reviews. John Wiley & Sons, Inc., 1995;331379. doi 10.1002/9780470650585.ch10
45. Font i Forcada C., Oraguzie N., Igartua E., Moreno M.Á., Gogorcena Y. Population structure and markertrait associations for pomological traits in peach and nectarine cultivars. Tree Genet Genomes. 2013;9:331349. doi 10.1007/s1129501205530
46. Font i Forcada C., Guajardo V., ChinWo S.R., Moreno M.Á. Association mapping analysis for fruit quality traits in Prunus persica using SNP markers. Front Plant Sci. 2019;9:2005. doi 10.3389/fpls.2018.02005
47. Foolad M.R., Arulsekar S., Becerra V., Bliss F.A. A genetic map of Prunus based on an interspecific cross between peach and almond. Theor Appl Genet. 1995;91:262269. doi 10.1007/BF00220887
48. Fu W., da Silva Linge C., Gasic K. Genomewide association study of brown rot (Monilinia spp.) tolerance in peach. Front Plant Sci. 2021;12:635914. doi 10.3389/fpls.2021.635914
49. Gao L., Gonda I., Sun H., Ma Q., Bao K., Tieman D.M., BurzynskiChang E.A., … van der Knaap E., Huang S., Klee H.J., Giovannoni J.J., Fei Z. The tomato pangenome uncovers new genes and a rare allele regulating fruit flavor. Nat Genet. 2019;51(6):10441051. doi 10.1038/s4158801904102
50. Gasic K., Da Silva Linge C., Bianco L., Troggio M., Rossini L., Bassi D., Aranzana M.J., Arus P., Verde I., Peace C., Iezzoni A. Development and evaluation of a 9K SNP addition to the peach IPSC 9K SNP array v1. HortScience. 2019;54(9S):S188
51. Guajardo V., Solís S., Almada R., Saski C., Gasic K., Moreno M.Á. Genomewide SNP identification in Prunus rootstocks germplasm collections using GenotypingbySequencing: phylogenetic analysis, distribution of SNPs and prediction of their effect on gene function. Sci Rep. 2020;10(1):1467. doi 10.1038/s41598020582715
52. Guan L., Cao K., Li Y., Guo J., Xu Q., Wang L. Detection and application of genome-wide variations in peach for association and genetic relationship analysis. BMC Genet. 2019;20(1):101. doi 10.1186/s1286301907998
53. Hamblin M.T., Warburton M.L., Buckler E.S. Empirical comparison of simple sequence repeats and single nucleotide polymorphisms in assessment of maize diversity and relatedness. PLoS One. 2007;2(12): e1367. doi 10.1371/journal.pone.0001367
54. Herrero J., Cambra M., Tabuenca M.C. Cartografía de Frutales de Hueso y Pepita. Zaragoza: Estación Experimental de Aula Dei (EEAD CSIC), 1964
55. Hesse C.O. Peaches. In: Janick J., Moore J.N. (Eds) Advances in Fruit Breeding. West Lafayette, Ind.: Purdue University Press, 1975; 285335
56. Hong J.H., Yi S.I., Kwon Y.S., Kim Y., Choi K.J. Genetic diversity analysis of peach [Prunus persica (L.) Batsch] varieties using SSR markers. Korean J Breed Sci. 2013;45(3):201211. doi 10.9787/KJBS.2013.45.3.201
57. Howad W., Yamamoto T., Dirlewanger E., Testolin R., Cosson P., Cipriani G., Monforte A.J., Georgi L., Abbott A.G., Arus P. Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics. 2005;171(3):13051309. doi 10.1534/genetics.105.043661
58. Huang Z., Shen F., Chen Y., Cao K., Wang L. Preliminary identification of key genes controlling peach pollen fertility using genomewide association study. Plants. 2021;10(2):242. doi 10.3390/plants10020242
59. Hübner S., Bercovich N., Todesco M., Mandel J.R., Odenheimer J., Ziegler E., Lee J.S., ... Kubach T., Muños S., Langlade N.B., Burke J.M., Rieseberg L.H. Sunflower pangenome analysis shows that hybridization altered gene content and disease resistance. Nat Plants. 2019;5(1):5462. doi 10.1038/s4147701803290
60. International Peach Genome Initiative; Verde I., Abbott A.G., Scalab rin S., Jung S., Shu S., Marroni F., … Silva H., Salamini F., Schmutz J., Morgante M., Rokhsar D.S. The highquality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013; 45(5):487494. doi 10.1038/ng.2586
61. Jayakodi M., Padmarasu S., Haberer G., Bonthala V.S., Gundlach H., Monat C., Lux T., ... Mayer K.F.X., Spannagl M., Li C., Mascher M., Stein N. The barley pangenome reveals the hidden legacy of mutation breeding. Nature. 2020;588(7837):284289. doi 10.1038/s4158602029478
62. Joiret M., Mahachie John J.M., Gusareva E.S., Van Steen K. Confounding of linkage disequilibrium patterns in large scale DNA based genegene interaction studies. BioData Min. 2019;12:11. doi 10.1186/s1304001901997
63. Jones N., Ougham H., Thomas H. Markers and mapping: we are all geneticists now. New Phytol. 1997;137(1):165177. doi 10.1046/j.14698137.1997.00826.x
64. Joobeur T., Viruel M.A., de Vicente M.C., Jáuregui B., Ballester J., Dettori M.T., Verde I., Truco M.J., Messeguer R., Batlle I., Quarta R., Dirlewanger E., Arús P. Construction of a saturated linkage map for Prunus using an almond × peach F2 progeny. Theor Appl Genet. 1998;97:10341041. doi 10.1007/s001220050988
65. Jung S., Staton M., Lee T., Blenda A., Svancara R., Abbott A., Main D. GDR (Genome Database for Rosaceae): integrated webdatabase for Rosaceae genomics and genetics data. Nucleic Acids Res. 2008; 36:D1034D1040. doi 10.1093/nar/gkm803
66. Jung S., Ficklin S.P., Lee T., Cheng C.H., Blenda A., Zheng P., Yu J., Bombarely A., Cho I., Ru S., Evans K., Peace C., Abbott A.G., Mueller L.A., Olmstead M.A., Main D. The genome database for Rosaceae (GDR): year 10 update. Nucleic Acids Res. 2014;42: D1237D1244. doi 10.1093/nar/gkt1012
67. Khlestkina E.K. Molecular markers in genetic studies and breeding. Russ J Genet Appl Res. 2014;4;236244. https://link.springer.com/article/10.1134/S2079059714030022#citeas
68. Kim J.S., Ku Y.S., Park S.G., Kim S.H., Park H.W., Won S.Y. Anticipated polymorphic SSRs and their application based on next generation sequencing of Prunus persica. Korean J Breed Sci. 2021;53(4): 350360. doi 10.9787/KJBS.2021.53.4.350
69. KoningBoucoiran C.F., Esselink G.D., Vukosavljev M., van’t Westende W.P., Gitonga V.W., Krens F.A., Voorrips R.E., van de Weg W.E., Schulz D., Debener T., Maliepaard C., Arens P., Smulders M.J. Using RNASeq to assemble a rose transcriptome with more than 13,000 fulllength expressed genes and to develop the WagRhSNP 68k Axiom SNP array for rose (Rosa L.). Front Plant Sci. 2015;6:249. doi 10.3389/fpls.2015.00249
70. Kuhn D.N., Livingstone D.S., Richards J.H., Manosalva P., Van den Berg N., Chambers A.H. Application of genomic tools to avocado (Persea americana) breeding: SNP discovery for genotyping and germplasm characterization. Sci Hortic. 2019;246:111. doi 10.1016/j.scienta.2018.10.011
71. Lambert P., Campoy J.A., Pacheco I., Mauroux J.B., Da Silva Linge C., Micheletti D., Bassi D., ... Pascal T., Troggio M., Aranzana M.J., Patocchi A., Arús P. Identifying SNP markers tightly associated with six major genes in peach [Prunus persica (L.) Batsch] using a highdensity SNP array with an objective of markerassisted selection (MAS). Tree Genet Genomes. 2016;12:121. doi 10.1007/s1129501610801
72. Lander E.S., Green P., Abrahamson J., Barlow A., Daly M.J., Lincoln S.E., Newburg L. Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987;1(2):174181. doi 10.1016/08887543(87)900103
73. Laucou V., Launay A., Bacilieri R., Lacombe T., AdamBlondon A. F., Bérard A., Chauveau A., … Maul E., Ponnaiah M., Töpfer R., Péros J.P., Boursiquot J.M. Extended diversity analysis of cultivated grapevine Vitis vinifera with 10K genomewide SNPs. PLoS One. 2018;13(2):e0192540. doi 10.1371/journal.pone.0192540
74. Li X., Singh J., Qin M., Li S., Zhang X., Zhang M., Khan A., Zhang S., Wu J. Development of an integrated 200K SNP genotyping array and application for genetic mapping, genome assembly improvement and genome wide association studies in pear (Pyrus). Plant Biotechnol J. 2019;17(8):15821594. doi 10.1111/pbi.13085
75. Li X., Wang J., Su M., Zhou J., Zhang M., Du J., Zhou H., ... Fang W., Wang L., Jia H., Gao Z., Ye Z. Single nucleotide polymorphism detection for peach gummosis disease resistance by genomewide association study. Front Plant Sci. 2022;12:763618. doi 10.3389/fpls.2021.763618
76. Li X., Wang J., Su M., Zhang M., Hu Y., Du J., Zhou H., Yang X., Zhang X., Jia H., Gao Z., Ye Z. Multiplestatistical genomewide association analysis and genomic prediction of fruit aroma and agronomic traits in peaches. Hortic Res. 2023;10(7):uhad117. doi 10.1093/hr/uhad117
77. Li Y.H., Zhou G., Ma J., Jiang W., Jin L.G., Zhang Z., Guo Y., ... Chang R.Z., Jiang Z., Jackson S.A., Li R., Qiu L.J. De novo assembly of soybean wild relatives for pangenome analysis of diversity and agronomic traits. Nat Biotechnol. 2014;32(10):10451052. doi 10.1038/nbt.2979
78. Li Y., Cao K.E., Zhu G., Fang W., Chen C., Wang X., Zhao P., Guo J., Ding T., Guan L., Zhang Q., Guo W., Fei Z., Wang L. Genomic analy ses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history. Genome Biol. 2019;20(1):36. doi 10.1186/s1305901916489
79. Lirong W., Yong L., Gengrui Z., Weichao F., Changwen C., Ke C., Xinwei W. Peach genomics and breeding programs at Zhengzhou Fruit Research Institute, CAAS. Acta Hortic. 2020;1282:16. doi 10.17660/ActaHortic.2020.1282.1
80. Liu H., Cao K., Zhu G., Fang W., Chen C., Wang X., Wang L. Genomewide association analysis of red flesh character based on resequencing approach in peach. J Am Soc Hortic Sci. 2019;144(3):209216. doi 10.21273/JASHS0462218
81. Liu J., Bao Y., Zhong Y., Wang Q., Liu H. Genomewide association study and transcriptome of olecranon-type traits in peach (Prunus persica L.) germplasm. BMC Genomics. 2021;22(1):702. doi 10.1186/s1286402108017y
82. Liu Y., Du H., Li P., Shen Y., Peng H., Liu S., Zhou G.A., … Wang Z., Zhu B., Han B., Liang C., Tian Z. Pangenome of wild and cultivated soybeans. Cell. 2020;182(1):162176. doi 10.1016/j.cell.2020.05.023
83. Mardis E.R. Nextgeneration DNA sequencing methods. Annu Rev Genomics Hum Genet. 2008;9(1):387402. doi 10.1146/annurev.genom.9.081307
84. Mariette S., Tavaud M., Arunyawat U., Capdeville G., Millan M., Salin F. Population structure and genetic bottleneck in sweet cherry estimated with SSRs and the gametophytic selfincompatibility locus. BMC Genet. 2010;11:77. doi 10.1186/147121561177
85. Marrano A., MartínezGarcía P.J., Bianco L., Sideli G.M., Di Pierro E.A., Leslie C.A., Stevens K.A., Crepeau M.W., Troggio M., Langley C.H., Neale D.B. A new genomic tool for walnut (Juglans regia L.): development and validation of the highdensity AxiomTM J. regia 700K SNP genotyping array. Plant Biotechnol J. 2019; 17(6):10271036. doi 10.1111/pbi.13034
86. MasGómez J., Cantín C.M., Moreno M.Á., Prudencio Á.S., GómezAbajo M., Bianco L., Troggio M., MartínezGómez P., Rubio M., MartínezGarcía P.J. Exploring genomewide diversity in the national peach (Prunus persica) germplasm collection at CITA (Zaragoza, Spain). Agronomy. 2021;11(3):481. doi 10.3390/agronomy
87. MasGómez J., Cantín C.M., Moreno M.Á., MartínezGarcía P.J. Genetic diversity and genome-wide association study of morphological and quality traits in peach using two Spanish peach germplasm collections. Front Plant Sci. 2022;13:854770. doi 10.3389/fpls.2022.854770
88. Meng G., Zhu G., Fang W., Chen C., Wang X., Wang L., Cao K. Identification of loci for single/double flower trait by combining genomewide association analysis and bulked segregant analysis in peach (Prunus persica). Plant Breed. 2019;138(3):360367. doi 10.1111/pbr.12673
89. Micali S., Vendramin E., Dettori M.T., Verde I. Genetics and genomics of stone fruits. In: Agricultural and Food Biotechnologies of Olea europaea and Stone Fruits. Bentham, 2015;243307. doi 10.2174/9781608059935115010008
90. Micheletti D., Dettori M.T., Micali S., Aramini V., Pacheco I., Da Silva Linge C., Foschi S., ... Rossini L., Verde I., Laurens F., Arús P., Aranzana M.J. Wholegenome analysis of diversity and SNPmajor gene association in peach germplasm. PloS One. 2015;10(9):e0136803. doi 10.1371/journal.pone.0136803
91. Monet R. Peach genetics: past present and future. Acta Hortic. 1988; 254:4958. doi 10.17660/ActaHortic.1989.254.8
92. Monet R., Gibault B. Polymorphisme de l’alphaamylase chez le pecher. Etude genetique. Agronomie (France). 1991;11(5):353358 Monet R., Bastard Y., Gibault B. Genetic studies on the breeding of flat peaches. Agronomie (France). 1985;5(8):727731
93. Monet R., Guye A., Roy M., Dachary N. Peach mendelian genetics: a short review and new results. Agronomie. 1996;16(5):321329. doi 10.1051/agro:19960505
94. Montanari S., Bianco L., Allen B.J., MartínezGarcía P.J., Bassil N.V., Postman J., Knäbel M., … Langley C.H., Evans K., Dhingra A., Troggio M., Neale D.B. Development of a highly efficient Axiom™ 70 K SNP array for Pyrus and evaluation for high-density mapping and germplasm characterization. BMC Genomics. 2019;20(1):331. doi 10.1186/s1286401957123
95. Morozova O., Marra M.A. Aplications of nextgeneration sequencing technologies in functional genomics. Genomics. 2008;92(5):255 264. doi 10.1016/j.ygeno.2008.07.001
96. Nybom H., Lācis G. Recent largescale genotyping and phenotyping of plant genetic resources of vegetatively propagated crops. Plants. 2021;10(2):415. doi 10.3390/plants10020415
97. Parfitt D.E., Arulsekar S., Ramming D.W. Identification of plum × peach hybrids by isoenzyme analysis. HortScience. 1985;20(2): 246248
98. Paterson A.H. Making genetic maps. In: Paterson A.H. Genome Mapping in Plants. Academic Press, 1996;2339
99. Peace C., Bassil N., Main D., Ficklin S., Rosyara U.R., Stegmeir T., Sebolt A., Gilmore B., Lawley C., Mockler T.C., Bryant D.W., Wilhelm L., Iezzoni A. Development and evaluation of a genomewide 6K SNP array for diploid sweet cherry and tetraploid sour cherry. PLoS One. 2012;7(12):e48305. doi 10.1371/journal.pone.0048305
100. Pflieger S., Lefebvre V., Caranta C., Blattes A., Goffinet B., Palloix A. Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. Genome. 1999;42(6):11001110 Pozzi C., Vecchietti A. Peach structural genomics. In: Folta K.M., Gardiner S.E. (Eds) Genetics and Genomics of Rosaceae. Plant Genetics and Genomics: Crops and Models. Vol. 6. New York, NY: Springer, 2009;235257. https://link.springer.com/book/10.1007/9780387774916
101. Purcell S., Neale B., ToddBrown K., Thomas L., Ferreira M.A.R., Bender D., Maller J., Sklar P., de Bakker P.I.W., Daly M.J., Sham P.C. PLINK: A tool set for wholegenome association and populationbased linkage analysis. Am J Hum Genet. 2007;81(3):559575. doi 10.1086/519795
102. Quarta R., Cedrola C., Dettori M.T., Verde I. QTL analysis of agronomic traits in a BC1 peach population. Acta Hortic. 2002;592:291 297. doi 10.17660/ActaHortic.2002.592.41
103. Quilot B., Wu B.H., Kervella J., Génard M., Foulongne M., Moreau K. QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet. 2004;109(4):884897. doi 10.1007/s001220041703z
104. Rasheed A., Hao Y., Xia X., Khan A., Xu Y., Varshney R.K., He Z. Crop breeding chips and genotyping platforms: progress, challenges, and perspectives. Mol Plant. 2017;10(8):10471064. doi 10.1016/j.molp.2017.06.008
105. Ru S., Main D., Evans K., Peace C. Current applications, challenges, and perspectives of markerassisted seedling selection in Rosaceae tree fruit breeding. Tree Genet Genomes. 2015;11:8. doi 10.1007/s1129501508345
106. Salazar J.A., Ruiz D., Campoy J.A., SánchezPérez R., Crisosto C.H., MartínezGarcía P.J., Blenda A., Jung S., Main D., MartínezGómez P., Rubio M. Quantitative trait loci (QTL) and Mendelian trait loci (MTL) analysis in Prunus: a breeding perspective and beyond. Plant Mol Biol Rep. 2013;32:118. doi 10.1007/s1110501306437
107. Scorza R. Gene transfer for the genetic improvement of perennial fruit and nut crops. HortScience. 1991;26(8):10331035
108. Scorza R., Okie W.R. Peaches (Prunus). Acta Hortic. 1991;290:177-234. doi 10.17660/ActaHortic.1991.290.5
109. Scorza R., Mehlenbacher S.A., Lightner G.W. Inbreeding and coancestry of freestone peach cultivars of the eastern United States and implications for peach germplasm improvement. J Am Soc Hortic Sci. 1985;110(4):547552. doi 10.21273/JASHS.110.4.547
110. Siberchicot A., Bessy A., Gueguen L., Marais G.A. Mareymap online: a userfriendly web application and database service for estimating recombination rates using physical and genetic maps. Genome Biol Evol. 2017;9(10):25062509. doi 10.1093/gbe/evx178
111. Smykov A., Shoferistov E., Korzin V., Mesyats N., Saplev N. Promising directions in the selection of peach, apricot and nectarine. E3S Web Conf. 2021;254:01010. doi 10.1051/e3sconf/202125401010
112. Sosinski B., Gannavarapu M., Hager L.D., Beck L.E., King G.J., Ryder C.D., Rajapakse S., Baird W.V., Ballard R.E., Abbott A.G. Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet. 2000;101:421428. doi 10.1007/s001220051499
113. Tan Q., Li S., Zhang Y., Chen M., Wen B., Jiang S., Chen X., Fu X., Li D., Wu H., Wang Y., Xiao W., Li L. Chromosomelevel genome assemblies of five Prunus species and genome-wide association studies for key agronomic traits in peach. Hortic Res. 2021;8(1):213. doi 10.1038/s41438021006482
114. Tanksley S.D., Young N.D., Paterson A.H., Bonierbale M.W. RFLP mapping in plantbreeding – new tools for an old science. Nat Biotechnol. 1989;7:257264. doi 10.1038/nbt0389257
115. Thurow L.B., Gasic K., Bassols Raseira M.C., Bonow S., Marques Castro C. Genomewide SNP discovery through genotyping by sequencing, population structure, and linkage disequilibrium in Brazilian peach breeding germplasm. Tree Genet Genomes. 2020;16:10. doi 10.1007/s112950191406x
116. Trifonova A.A., Boris K.V., Mesyats N.V., Tsiupka V.A., Smykov A.V., Mitrofanova I.V. Genetic diversity of peach cultivars from the collection of the Nikita Botanical Garden based on SSR markers. Plants. 2021;10(12):2609. doi 10.3390/plants10122609
117. Van Ooijen J.W. Joinmap® 4. Software for the calculation of genetic linkage maps in experimental populations. ScienceOpen, Inc., 2006
118. Van Ooijen J.W. MapQTL® 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. ScienceOpen, Inc., 2009
119. Verde I., Bassil N., Scalabrin S., Gilmore B., Lawley C.T., Gasic K., Micheletti D, ... Aranzana M.J., Arús P., Iezzoni A., Morgante M., Peace C. Development and evaluation of a 9K SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PloS One. 2012;7(4):e35668. doi 10.1371/journal.pone.0035668
120. Verde I., Jenkins J., Dondini L., Micali S., Pagliarani G., Vend ramin E., Paris R., ... Shu S., Grimwood J., Tartarini S., Dettori M.T., Schmutz J. The Peach v2. 0 release: highresolution linkage mapping and deep resequencing improve chromosomescale assembly and contiguity. BMC Genomics. 2017;18(1):225. doi 10.1186/s1286401736069
121. Voorrips R.E. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93(1):7778. doi 10.1093/jhered/93.1.77
122. Wang L., Zhu G., Fang W. Peach germplasm and breeding programs at Zhengzhou in China. Acta Hortic. 2001;592:177182. doi 10.17660/ActaHortic.2002.592.25
123. Werner D.J., Okie W.R. A history and description of the Prunus persica plant introduction collection. HortScience. 1998;33(5):787793. doi 10.21273/HORTSCI.33.5.787
124. Winter P., Kahl G. Molecular marker technologies for plant improvement. World J Microbiol Biotechnol. 1995;11(4):438448. doi 10.1007/BF00364619
125. Yamamoto T., Mochida K., Hayashi T. Shanhai Suimitsuto, one of the origins of Japanese peach cultivars. J Japan Soc Hortic Sci. 2003; 72(2):116121
126. Yu J.M., Zhang Z.W., Zhu C.S., Tabanao D.A., Pressoir G., Tuinstra M.R., Kresovich S., Todhunter R.J., Buckler E.S. Simulation appraisal of the adequacy of number of background markers for relationship estimation in association mapping. Plant Genome. 2009; 2(1):6377. doi 10.3835/plantgenome2008.09.0009
127. Yu Y., Fu J., Xu Y., Zhang J., Ren F., Zhao H., Tian S., … Wang G., Ma R., Jiang Q., Wei J., Xie H. Genome resequencing reveals the evolutionary history of peach fruit edibility. Nat Commun. 2018; 9(1):5404. doi 10.1038/s41467018077443
128. Zhao Q., Feng Q., Lu H., Li Y., Wang A., Tian Q., Zhan Q, ... Xu Q., Wang Z.X., Wei X., Han B., Huang X. Pangenome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet. 2018;50(2):278284. doi 10.1038/s415880180041z
129. Zurn J.D., Nyberg A., Montanari S., Postman J., Neale D., Bassil N. A new SSR fingerprinting set and its comparison to existing SSR and SNPbased genotyping platforms to manage Pyrus germplasm resources. Tree Genet Genomes. 2020;16:72. doi 10.1007/s11295020014677