主要果树重要性状QTL鉴定研究进展

doi:10.16420/j.issn.0513-353x.2021-1102

摘要/Abstract

摘要：

阐述并比较了基于遗传连锁图谱、利用集团分离分析或分离群体分组分析（BSA）以及全基因组关联分析（GWAS）等鉴定主要果树重要性状QTL的方法，综述了近年来果实外观品质和内在品质、生长发育、抗生物和非生物胁迫等重要性状的QTL鉴定的研究成果，对QTL鉴定及定位方法策略等问题进行了讨论与展望，以期为果树QTL鉴定研究以及果树育种提供参考与借鉴。

关键词: 果树, QTL定位, 遗传连锁图谱, BSA, GWAS

Abstract:

The methods for QTL identification of important traits in fruit trees by genetic linkage map，BSA and GWAS are expounded and compared. The current review summarizes advancement on the identification of QTLs associated with important traits of fruit trees，including external appearance，internal quality，growth and development，resistance to biotic and abiotic stress，in recent years. The purpose of this review is to provide clues for understanding the QTL identification and breeding of fruit tree，and to discuss and propose the methods and strategies that can be used for QTL identification and mapping of important characters in fruit trees.

Key words: fruit tree, QTL mapping, genetic linkage map, BSA, GWAS

中图分类号:

方天, 刘继红. 主要果树重要性状QTL鉴定研究进展[J]. 园艺学报, 2022, 49(12): 2622-2640.

FANG Tian, LIU Jihong. Advances in Identification of QTLs Associated with Significant Traits in Major Fruit Trees[J]. Acta Horticulturae Sinica, 2022, 49(12): 2622-2640.

参考文献 133

[1]	Aharoni A, Jongsma M A, Kim T Y, Ri M B, Giri A P, Verstappen F W A, Schwab W, Bouwmeester H J. 2006. Metabolic engineering of terpenoid biosynthesis in plants. Phytochemistry Reviews, 5 (1):49-58. doi: 10.1007/s11101-005-3747-3 URL
[2]	Allard A, Bink M C A M, Martinez S, Kelner J J, Legave J M, Di G M, Di P E A, Laurens F, van de Weg E W, Costes E. 2016. Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. Journal of Experimental Botany, 67 (9):2875-2888. doi: 10.1093/jxb/erw130 pmid: 27034326
[3]	Alonge M, Wang X, Benoit M, Soyk S, Pereira L, Zhang L, Suresh H, Ramakrishnan S, Maumus F, Ciren D, Levy Y, Harel T H, Shalev-Schlosser G, Amsellem Z, Razifard H, Caicedo A L, Tieman D M, Klee H, Kirsche M, Aganezov S, Ranallo-Benavidez T R, Lemmon Z H, Kim J, Robitaille G, Kramer M, Goodwin S, McCombie W R, Hutton S, Van E J, Gillis J, Eshed Y, Sedlazeck F J, van der K E, Schatz M C, Lippman Z B. 2020. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell, 182 (1):145-161. doi: S0092-8674(20)30616-4 pmid: 32553272
[4]	Arús P, Verde I, Sosinski B, Zhebentyayeva T, Abbott A G. 2012. The peach genome. Tree Genetics & Genomes, 8 (3):531-547.
[5]	Asins M J, Bernet G P, Ruiz C, Cambra M, Guerri J, Carbonell E A. 2004. QTL analysis of citrus tristeza virus-citradia interaction. Theoretical and Applied Genetics, 108 (4):603-611. pmid: 14614564
[6]	Bai Y, Dougherty L, Li M, Fazio G, Cheng L, Xu K. 2012. A natural mutation-led truncation in one of the two aluminum-activated malate transporter-like genes at the Ma locus is associated with low fruit acidity in apple. Molecular Genetics and Genomics, 287(8):663-678. doi: 10.1007/s00438-012-0707-7 URL
[7]	Ban S, Xu K N. 2020. Identification of two QTLs associated with high fruit acidity in apple using pooled genome sequencing analysis. Horticulture Research, 7 (1):171. doi: 10.1038/s41438-020-00393-y pmid: 34620842
[8]	Bazakos C, Hanemian M, Trontin C, Jiménez-Gómez J M, Loudet O. 2017. New strategies and tools in quantitative genetics:How to go from the phenotype to the genotype. Annual Review of Plant Biology, 68 (1):435-455. doi: 10.1146/annurev-arplant-042916-040820 URL
[9]	Bernet G P, Margaix C, Jacas J, Carbonell E A, Asins, M J. 2005. Genetic analysis of citrus leafminer susceptibility. Theoretical and Applied Genetics, 110 (8):1393-1400. pmid: 15834698
[10]	Bhat J A, Deshmukh R, Zhao T, Patil G, Deokar A, Shinde S, Chaudhary J. 2020. Harnessing high-throughput phenotyping and genotyping for enhanced drought tolerance in crop plants. Journal of Biotechnology, 324:248-260. doi: 10.1016/j.jbiotec.2020.11.010 pmid: 33186658
[11]	Bohra A, Chand Jha U, Godwin I D, Kumar Varshney R. 2020. Genomic interventions for sustainable agriculture. Plant Biotechnology Journal, 18 (12):2388-2405. doi: 10.1111/pbi.13472 URL
[12]	Cai L, Quero-García J, Barreneche T, Dirlewanger E, Saski C, Iezzoni A. 2019. A fruit firmness QTL identified on linkage group 4 in sweet cherry (Prunus avium L.)is associated with domesticated and bred germplasm. Scientific Reports, 9 (1):1-14. doi: 10.1038/s41598-018-37186-2 URL
[13]	Calle A, Cai L, Iezzoni A, Wünsch A. 2020. Genetic dissection of bloom time in low chilling sweet cherry(Prunus avium L.)using a multi-family QTL approach. Frontiers in Plant Science, 10:1647. doi: 10.3389/fpls.2019.01647 URL
[14]	Calle A, Wünsch A. 2020. Multiple-population QTL mapping of maturity and fruit-quality traits reveals LG4 region as a breeding target in sweet cherry(Prunus avium L.). Horticulture Research, 7 (1):127. doi: 10.1038/s41438-020-00349-2 URL
[15]	Cao K, Zhou Z K, Wang Q, Guo J, Zhao P, Zhu G R, Fang W C, Chen C W, Wang X W, Wang X L, Tian Z X, Wang L R. 2016. Genome-wide association study of 12 agronomic traits in peach. Nature Communications, 7 (1):13246. doi: 10.1038/ncomms13246 URL
[16]	Carrasco-Valenzuela T, Muñoz-Espinoza C, Riveros A, Pedreschi R, Arús P, Campos-Vargas R, Meneses C. 2019. Expression QTL(eQTLs)analyses reveal candidate genes associated with fruit flesh softening rate in peach[Prunus persica(L.)Batsch]. Frontiers in Plant Science, 10:1581. doi: 10.3389/fpls.2019.01581 pmid: 31850046
[17]	Chagné D, Carlisle C M, Blond C, Volz R K, Whitworth C J, Oraguzie N C, Crowhurst R N, Allan A C, Espley R V, Hellens R P, Gardiner S E. 2007. Mapping a candidate gene(MdMYB10)for red flesh and foliage colour in apple. BMC Genomics, 8 (1):212. doi: 10.1186/1471-2164-8-212 URL
[18]	Chagné D, Lin-Wang K, Espley R V, Volz R K, How N M, Rouse S, Brendolise C, Carlisle C M, Kumar S, de Silva N, Micheletti D, McGhie T, Crowhurst R N, Storey R D, Velasco R, Hellens R P, Gardiner S E, Allan A C. 2013. An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiology, 161 (1):225-239. doi: 10.1104/pp.112.206771 pmid: 23096157
[19]	Chagné D, Vanderzande S, Kirk C, Profitt N, Weskett R, Gardiner S E, Peace C P, Volz R K, Bassil N V. 2019. Validation of SNP markers for fruit quality and disease resistance loci in apple(Malus × domestica Borkh.)using the OpenArray^® platform. Horticulture Research, 6 (1):30. doi: 10.1038/s41438-018-0114-2 URL
[20]	Chawla H S, Lee H T, Gabur I, Vollrath P, Tamilselvan-Nattar-Amutha S, Obermeier C, Schiessl S V, Song J M, Liu K, Guo L, Parkin I A P, Snowdon R J. 2021. Long-read sequencing reveals widespread intragenic structural variants in a recent allopolyploid crop plant. Plant Biotechnology Journal, 19 (2):240-250. doi: 10.1111/pbi.13456 URL
[21]	Chang Yuan-sheng, Cheng Lai-liang, Wang Hai-bo, He Ping, Li Hui-feng, Li Lin-guang. 2017. Review of molecular marker and marker assisted breeding of apple. Acta Horticulturae Sinica, 44 (9):1658-1680. (in Chinese)
	常源升, 程来亮, 王海波, 何平, 李慧峰, 李林光. 2017. 苹果分子标记及辅助育种研究进展. 园艺学报, 44 (9):1658-1680.
[22]	Christeller J T, McGhie T K, Johnston J W, Carr B, Chagné D. 2019. Quantitative trait loci influencing pentacyclic triterpene composition in apple fruit peel. Scientific Reports, 9 (1):18501. doi: 10.1038/s41598-019-55070-5 pmid: 31811217
[23]	Cirilli M, Gattolin S, Chiozzotto R, Baccichet I, Pascal T, Quilot-Turion B, Rossini L, Bassi D. 2021. The Di2/pet variant in PETALOSA gene underlies a major heat requirement-related QTL for blooming date in peach(P. persica L. Batsch). Plant and Cell Physiology, 62 (2):356-365. doi: 10.1093/pcp/pcaa166 pmid: 33399872
[24]	Costa F. 2015. MetaQTL analysis provides a compendium of genomic loci controlling fruit quality traits in apple. Tree Genetics & Genomes, 11 (1):1-11.
[25]	Costa F, Cappellin L, Zini E, Patocchi A, Kellerhals M, Komjanc M, Gessler C, Biasioli F. 2013. QTL validation and stability for volatile organic compounds(VOCs)in apple. Plant Science, 211:1-7. doi: 10.1016/j.plantsci.2013.05.018 URL
[26]	Cristofani M, Machado M A, Grattapaglia D. 1999. Genetic linkage maps of Citrus sunki Hort. ex. Tan. and Poncirus trifoliata(L.) Raf. and mapping of citrus tristeza virus resistance gene. Euphytica, 109 (1):25-32. doi: 10.1023/A:1003637116745 URL
[27]	Curtolo M, Cristofani-Yaly M, Gazaffi R, Takita M A, Figueira A, Machado M A. 2017. QTL mapping for fruit quality in citrus using DArTseq markers. BMC Genomics, 18 (1):289. doi: 10.1186/s12864-017-3629-2 pmid: 28403819
[28]	Della Coletta R, Qiu Y, Ou S, Hufford M B, Hirsch C N. 2021. How the pan-genome is changing crop genomics and improvement. Genome Biology, 22 (1):3. doi: 10.1186/s13059-020-02224-8 pmid: 33397434
[29]	de Young B J, Innes R W. 2006. Plant NBS-LRR proteins in pathogen sensing and host defense. Nature Immunology, 7 (12):1243-1249. doi: 10.1038/ni1410 pmid: 17110940
[30]	Di Guardo M, Bink M C A M, Guerra W, Letschka T, Lozano L, Busatto N, Poles L, Tadiello A, Bianco L, Visser R G F, van de Weg E, Costa F. 2017. Deciphering the genetic control of fruit texture in apple by multiple family-based analysis and genome-wide association. Journal of Experimental Botany, 68 (7):1451-1466. doi: 10.1093/jxb/erx017 pmid: 28338805
[31]	Dirlewanger E, Cosson P, Boudehri K, Renaud C, Capdeville G, Tauzin Y, Laigret F, Moing A. 2006. Development of a second-generation genetic linkage map for peach[Prunus persica(L.)Batsch]and characterization of morphological traits affecting flower and fruit. Tree Genetics & Genomes, 3 (1):1-13.
[32]	Dirlewanger E, Graziano E, Joobeur T, Garriga-caldere F, Cosson P, Howad W, Aru P. 2004. Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proceedings of the National Academy of Sciences of the United States of America, 101 (26):9891-9896.
[33]	Dirlewanger E, Quero-García J, Le Dantec L, Lambert P, Ruiz D, Dondini L, Illa E, Quilot-Turion B, Audergon J M, Tartarini S, Letourmy P, Arús P. 2012. Comparison of the genetic determinism of two key phenological traits,flowering and maturity dates,in three Prunus species:peach,apricot and sweet cherry. Heredity, 109 (5):280-292. doi: 10.1038/hdy.2012.38 pmid: 22828898
[34]	Dong Ling. 2016. The analysis of stomatal traits and QTL mapping under drought condition in‘Qingguan’×‘ Honeycrisp Leaves’[Ph. D. Dissertation]. Yangling:Northwest A & F University. (in Chinese)
	董玲. 2016. 干旱条件下‘秦冠’×‘蜜脆’杂交后代叶片的气孔性状分析及QTL定位[博士论文]. 杨凌:西北农林科技大学.
[35]	Dong O X, Yu S, Jain R, Zhang N, Duong P Q, Butler C, Li Y, Lipzen A, Martin J A, Barry K W, Schmutz J, Tian L, Ronald P C. 2020. Marker-free carotenoid-enriched rice generated through targeted gene insertion using CRISPR-Cas9. Nature Communications, 11 (1):1178. doi: 10.1038/s41467-020-14981-y pmid: 32132530
[36]	Dunemann F, Ulrich D, Boudichevskaia A, Grafe C, Weber W E. 2009. QTL mapping of aroma compounds analysed by headspace solid-phase microextraction gas chromatography in the apple progeny‘Discovery’×‘ Prima’. Molecular Breeding, 23 (3):501-521. doi: 10.1007/s11032-008-9252-9 URL
[37]	Elsadr H, Sherif S, Banks T, Somers D, Jayasankar S. 2019. Refining the genomic region containing a major locus controlling fruit maturity in peach. Scientific Reports, 9 (1):1-12. doi: 10.1038/s41598-018-37186-2 URL
[38]	Falchi R., Vendramin E, Zanon L, Scalabrin S, Cipriani G, Verde I, Vizzotto G, Morgante M. 2013. Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. Plant Journal, 76 (2):175-187. doi: 10.1111/tpj.12283 URL
[39]	Forni C, Duca D, Glick B R. 2017. Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant and Soil, 410 (1-2):335-356. doi: 10.1007/s11104-016-3007-x URL
[40]	Foster T M, Celton J M, Chagne D, Stuart Tustin D, Gardiner S E. 2015. Two quantitative trait loci,Dw1 and Dw2,are primarily responsible for rootstock-induced dwarfing in apple. Horticulture Research, 2 (1):15001. doi: 10.1038/hortres.2015.1 URL
[41]	Frett T J, Reighard G L, Okie W R, Gasic K. 2014. Mapping quantitative trait loci associated with blush in peach[Prunus persica(L.)Batsch]. Tree Genetics & Genomes, 10 (2):367-381.
[42]	Gao C X. 2021. Genome engineering for crop improvement and future agriculture. Cell, 184 (6):1621-1635. doi: 10.1016/j.cell.2021.01.005 pmid: 33581057
[43]	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 (4):1121-1137. doi: 10.1093/genetics/137.4.1121 pmid: 7982566
[44]	Gross B L, Olsen K M. 2010. Genetic perspectives on crop domestication. Trends in Plant Science, 15 (9):529-537. doi: 10.1016/j.tplants.2010.05.008 pmid: 20541451
[45]	Guo Jun, Zhu Jie, Xie Shangqian, Zhang Ye, Ye Beilei, Zheng Liyan, Ling Peng. 2020. Development of SSR molecular markers based on transcriptome and analysis of genetic relationship of germplasm resources in avocado. Acta Horticulturae Sinica, 47 (8):1552-1564. (in Chinese)
	郭俊, 朱婕, 谢尚潜, 张叶, 叶蓓蕾, 郑丽燕, 凌鹏. 2020. 油梨转录组SSR分子标记开发与种质资源亲缘关系分析. 园艺学报, 47 (8):1552-1564.
[46]	Han Guohui, Luo Youjin, Xiang Suqiong, Yang Haijian, Li Xunlan, Cheng Changfeng. 2019. Advances in genetic linkage map construction and QTL mapping associated main traits of citrus. Acta Horticulturae Sinica, 46 (9):1739-1751. (in Chinese)
	韩国辉, 罗友进, 向素琼, 杨海健, 李勋兰, 程昌凤. 2019. 柑橘遗传连锁图谱构建及重要性状QTL的研究进展. 园艺学报, 46 (9):1739-1751.
[47]	Hong Q B, Ma X J, Gong G Z, Peng Z C, He Y R. 2015. QTL mapping of citrus freeze tolerance. Acta Horticulturae, 1065:467-474.
[48]	Huang M, Roose M L, Yu Q B, Du D L, Yu Y, Zhang Y, Deng Z N, Stover E, Gmitter F G. 2018. Construction of high-density genetic maps and detection of QTLs associated with Huanglongbing tolerance in citrus. Frontiers in Plant Science, 9:1694. doi: 10.3389/fpls.2018.01694 pmid: 30542355
[49]	Huang Y F, Bertrand Y, Guiraud J L, Vialet S, Launay A, Cheynier V, Terrier N, This P. 2013. Expression QTL mapping in grapevine-revisiting the genetic determinism of grape skin colour. Plant Science, 207:18-24. doi: 10.1016/j.plantsci.2013.02.011 URL
[50]	Jaiswal S, Gautam R K, Singh R K, Krishnamurthy S L, Ali S, Sakthivel K, Iquebal M A, Rai A, Kumar D. 2019. Harmonizing technological advances in phenomics and genomics for enhanced salt tolerance in rice from a practical perspective. Rice, 12 (1):89. doi: 10.1186/s12284-019-0347-1 pmid: 31802312
[51]	Jia D J, Shen F, Wang Y, Wu T, Xu X F, Zhang X Z, Han Z H. 2018. Apple fruit acidity is genetically diversified by natural variations in three hierarchical epistatic genes:MdSAUR37,MdPP2CH and MdALMTII. Plant Journal, 95 (3):427-443. doi: 10.1111/tpj.13957 URL
[52]	Jia D J, Wu P, Shen F, Li W, Zheng X D, Wang Y Z, Yuan Y B, Zhang X Z, Han Z H. 2021. Genetic variation in the promoter of an R2R3-MYB transcription factor determines fruit malate content in apple(Malus domestica Borkh.). Plant Physiology, 186 (1):549-568. doi: 10.1093/plphys/kiab098 URL
[53]	Jiang Shuang, Zhang Xueying, An Haishan, Xu Fangjie, Zhang Jiaying. 2021. Development and analysis of polymorphism of SSR markers in the whole genome of loquat. Acta Horticulturae Sinica, 48 (5):1013-1022. (in Chinese)
	蒋爽, 张学英, 安海山, 徐芳杰, 章加应. 2021. 枇杷全基因组SSR标记开发及其多态性研究. 园艺学报, 48 (5):1013-1022.
[54]	Kostick S A, Teh S L, Norelli J L, Vanderzande S, Peace C, Evans K M. 2021. Fire blight QTL analysis in a multi-family apple population identifies a reduced-susceptibility allele in‘Honeycrisp’. Horticulture Research, 8 (1):28. doi: 10.1038/s41438-021-00466-6 pmid: 33518709
[55]	Kumar S, Kirk C, Deng C H, Wiedow C, Qin M, Espley R, Wu J, Brewer L. 2019. Fine-mapping and validation of the genomic region underpinning pear red skin colour. Horticulture Research, 6 (1):29. doi: 10.1038/s41438-018-0112-4 URL
[56]	Lambert P, Campoy J A, Pacheco I, Mauroux J B, Da S L C, Micheletti D, Bassi D, Rossini L, Dirlewanger E, Pascal T, Troggio M, Aranzana M J, Patocchi A, Arús P. 2016. Identifying SNP markers tightly associated with six major genes in peach[Prunus persica(L.)Batsch]using a high-density SNP array with an objective of marker-assisted selection(MAS). Tree Genetics & Genomes, 12 (6):121.
[57]	Li Na, Shang Jianli, Li Nannan, Zhou Dan, Kong Shengnan, Wang Jiming, Ma Shuangwu. 2021. Accurate molecular identification for fruit shape in watermelon(Citrullus lanatus). Acta Horticulturae Sinica, 48 (7):1386-1396. (in Chinese)
	李娜, 尚建立, 李楠楠, 周丹, 孔胜楠, 王吉明, 马双武. 2021. 西瓜果实形状的分子精准鉴定. 园艺学报, 48 (7):1386-1396.
[58]	Liao L, Zhang W H, Zhang B, Fang T, Wang X F, Cai Y M, Ogutu C, Gao L, Chen G, Nie X Q, Xu J S, Zhang Q Y, Ren Y R, Yu J Q, Wang C K, Deng C H, Ma B Q, Zheng B B, You C X, Hu D G, Espley R, Wang K L, Yao J L, Allan A C, Khan A, Korban S S, Fei Z J, Ming R, Hao Y J, Li L, Han Y P. 2021. Unraveling a genetic roadmap for improved taste in the domesticated apple. Molecular Plant, 14 (9):1454-1471. doi: 10.1016/j.molp.2021.05.018 pmid: 34022440
[59]	Lima R P M, Curtolo M, Merfa M V, Cristofani-Yaly M, Machado M A. 2018. QTLs and eQTLs mapping related to citrandarins’ resistance to citrus gummosis disease. BMC Genomics, 19 (1):1-17. doi: 10.1186/s12864-017-4368-0 URL
[60]	Liu J, Shen F, Xiao Y, Fang H C, Qiu C P, Li W, Wu T, Xu X F, Wang Y, Zhang X Z, Han Z H. 2020. Genomics-assisted prediction of salt and alkali tolerances and functional marker development in apple rootstocks. BMC Genomics, 21 (1):550. doi: 10.1186/s12864-020-06961-9 pmid: 32778069
[61]	Liu Sheng-rui. 2016. High-density genetic map construction and identification of QTLs controlling deciduous trait in citrus[Ph. D. Dissertation]. Wuhan:Huazhong Agricultural University. (in Chinese)
	刘升锐. 2016. 柑橘高密度遗传连锁图谱的构建及落叶性状的QTL定位[博士论文]. 武汉:华中农业大学.
[62]	Luedeling E. 2012. Climate change impacts on winter chill for temperate fruit and nut production:a review. Scientia Horticulturae, 144:218-229. doi: 10.1016/j.scienta.2012.07.011 URL
[63]	Lu Y M, Tian Y F, Shen R D, Yao Q, Wang M G, Chen M, Dong J S, Zhang T E, Li F, Lei M G, Zhu J K. 2020. Targeted efficient sequence insertion and replacement in rice. Nature Biotechnology, 38 (12):1402-1407. doi: 10.1038/s41587-020-0581-5 URL
[64]	Lye Z N, Purugganan M D. 2019. Copy number variation in domestication. Trends in Plant Science, 24 (4):352-365. doi: S1360-1385(19)30015-9 pmid: 30745056
[65]	Ma B Q, Zhao S, Wu B H, Wang D M, Peng Q, Owiti A, Fang T, Liao L, Ogutu C, Korban S S, Li S H, Han Y P. 2016. Construction of a high density linkage map and its application in the identification of QTLs for soluble sugar and organic acid components in apple. Tree Genetics & Genomes, 12 (1):1.
[66]	Ma Xi-jun. 2012. Citrus genetic linkage map extension and cold resistance analysis and QTL mapping[M. D. Dissertation]. Chongqing: Southwest University. (in Chinese)
	马喜军. 2012. 柑橘遗传图谱的延伸加密以及抗寒性遗传分析和QTL定位[硕士论文]. 重庆: 西南大学.
[67]	Mares-Perlman J A, Millen A E, Ficek T L, Hankinson S E. 2002. The body of evidence to support a protective role for lutein and zeaxanthin in delaying chronic disease. Overview. Journal of Nutrition, 132 (3):518-524.
[68]	McClure K A, Gong Y H, Song J, Vinqvist-Tymchuk M, Campbell P L, Fan L, Burgher-MacLellan K, Zhang Z Q, Celton J M, Forney C F, Migicovsky Z, Myles S. 2019. Genome-wide association studies in apple reveal loci of large effect controlling apple polyphenols. Horticulture Research, 6 (1):107. doi: 10.1038/s41438-019-0190-y URL
[69]	McDowell J M, Simon S A. 2006. Recent insights into R gene evolution. Molecular Plant Pathology, 7 (5):437-448. doi: 10.1111/j.1364-3703.2006.00342.x pmid: 20507459
[70]	McHale L, Tan X, Koehl P, Michelmore R W. 2006. Plant NBS-LRR proteins: adaptable guards. Genome Biology, 7 (4):212. doi: 10.1186/gb-2006-7-4-212 pmid: 16677430
[71]	Michelmore R W, Paran I, Kesseli R V. 1991. Identification of markers linked to disease-resistance genes by bulked segregant analysis:a rapid method to detect markers in specific genomic regions by using segregating populations. Proceedings of the National Academy of Sciences of the United States of America, 88 (21):9828-9832.
[72]	Montanari S, Perchepied L, Renault D, Frijters L, Velasco R, Horner M, Gardiner S E, Chagné D, Bus V G M, Durel C E, Malnoy M. 2016. A QTL detected in an interspecific pear population confers stable fire blight resistance across different environments and genetic backgrounds. Molecular Breeding, 36 (4):47. doi: 10.1007/s11032-016-0473-z URL
[73]	Moriya S, Iwanami H, Haji T, Okada K, Yamada M, Yamamoto T, Abe K. 2015. Identification and genetic characterization of a quantitative trait locus for adventitious rooting from apple hardwood cuttings. Tree Genetics & Genomes, 11 (3):59.
[74]	Mou J L, Zhang Z H, Qiu H J, Lu Y, Zhu X, Fan Z Q, Zhang Q H, Ye J L, Fernie A R, Cheng Y J, Deng X X, Wen W W. 2021. Multiomics-based dissection of citrus flavonoid metabolism using a Citrus reticulata × Poncirus trifoliata population. Horticulture Research, 8 (1):56. doi: 10.1038/s41438-021-00472-8 URL
[75]	Nishio S, Hayashi T, Shirasawa K, Saito T, Terakami S, Takada N, Takeuchi Y, Moriya S, Itai A. 2021. Genome-wide association study of individual sugar content in fruit of Japanese pear(Pyrus spp.). BMC Plant Biology, 21 (1):1-19. doi: 10.1186/s12870-020-02777-7 URL
[76]	Nocker S V, Gardiner S E. 2014. Breeding better cultivars,faster: applications of new technologies for the rapid deployment of superior horticultural tree crops. Horticulture Research, 1 (1):14022. doi: 10.1038/hortres.2014.22 URL
[77]	Nordborg M, Weigel D. 2008. Next-generation genetics in plants. Nature, 456 (7223):720-723. doi: 10.1038/nature07629 URL
[78]	Nuñez-Lillo G, Cifuentes-Esquivel A, Troggio M, Micheletti D, Infante R, Campos-Vargas R, Orellana A, Blanco-Herrera F, Meneses C. 2015. Identification of candidate genes associated with mealiness and maturity date in peach[Prunus persica (L.) Batsch]using QTL analysis and deep sequencing. Tree Genetics & Genomes, 11 (4):86.
[79]	Ogundiwin E A, Peace C P, Gradziel T M, Parfitt D E, Bliss F A, Crisosto C H. 2009. A fruit quality gene map of Prunus. BMC Genomics, 10 (1):587. doi: 10.1186/1471-2164-10-587 URL
[80]	Pei M S, Cao S H, Wu L, Wang G M, Xie Z H, Gu C, Zhang S L. 2020. Comparative transcriptome analyses of fruit development among pears,peaches,and strawberries provide new insights into single sigmoid patterns. BMC Plant Biology, 20 (1):108. doi: 10.1186/s12870-020-2317-6 URL
[81]	Peil A, Hübert C, Wensing A, Horner M, Emeriewen O F, Richter K, Wöhner T, Chagné D, Orellana-Torrejon C, Saeed M, Troggio M, Stefani E, Gardiner S E, Hanke M V, Flachowsky H, Bus V G M. 2019. Mapping of fire blight resistance in Malus × robusta 5 flowers following artificial inoculation. BMC Plant Biology, 19 (1):532. doi: 10.1186/s12870-019-2154-7 URL
[82]	Peng Q, Cai Y M, Lai E, Nakamura M, Liao L, Zheng B B, Ogutu C, Cherono S, Han Y P. 2020. The sucrose transporter MdSUT4.1 participates in the regulation of fruit sugar accumulation in apple. BMC Plant Biology, 20 (1):191. doi: 10.1186/s12870-020-02406-3 pmid: 32375636
[83]	Pichersky E, Gershenzon J. 2002. The formation and function of plant volatiles:perfumes for pollinator attraction and defense. Current Opinion in Plant Biology, 5 (3):237-243. doi: 10.1016/s1369-5266(02)00251-0 pmid: 11960742
[84]	Pichersky E, Raguso R A. 2018. Why do plants produce so many terpenoid compounds? New Phytologist, 220 (3):692-702. doi: 10.1111/nph.14178 pmid: 27604856
[85]	Pierantoni L, Dondini L, Cho K H, Shin I S, Gennari F, Chiodini R, Tartarini S, Kang S J, Sansavini S. 2007. Pear scab resistance QTLs via a European pear(Pyrus communis)linkage map. Tree Genetics & Genomes, 3 (4):311-317.
[86]	Pieruschka R, Schurr U. 2019. Plant phenotyping: past,present,and future. Plant Phenomics, 1 (1):6.
[87]	Pirona R, Eduardo I, Pacheco I, da Silva Linge C, Miculan M, Verde I, Tartarini S, Dondini L, Pea G, Bassi D, Rossini L. 2013. Fine mapping and identification of a candidate gene for a major locus controlling maturity date in peach. BMC Plant Biology, 13 (1):166. doi: 10.1186/1471-2229-13-166 URL
[88]	Price A H. 2006. Believe it or not,QTLs are accurate. Trends in Plant Science, 11 (5):213-216. doi: 10.1016/j.tplants.2006.03.006 pmid: 16617032
[89]	Raga V, Intrigliolo D S, Bernet G P, Carbonell E A, Asins M J. 2016. Genetic analysis of salt tolerance in a progeny derived from the citrus rootstocks cleopatra mandarin and trifoliate orange. Tree Genetics & Genomes, 12 (3):34.
[90]	Rawandoozi Z J, Hartmann T P, Carpenedo S, Gasic K, da Silva Linge C, Cai L, van de Weg E, Byrne D H. 2020. Identification and characterization of QTLs for fruit quality traits in peach through a multi-family approach. BMC Genomics, 21 (1):522. doi: 10.1186/s12864-020-06927-x pmid: 32727362
[91]	Ruiz D, Lambert P, Audergon J M, Dondini L, Tartarini S, Adami M, Gennari F, Cervellati C, De Franceschi P, Sansavini S, Testolin R, Bureau S, Gouble B, Reich M, Renard C M G C, Bassi D. 2010. Identification of QTLs for fruit quality traits in apricot. Acta Horticulturae,(862):587-592.
[92]	Salazar J A, Ruiz D, Campoy J A, Sánchez-Pérez R, Crisosto C H, Martínez-García P J, Blenda A, Jung S, Main D, Martínez-Gómez P, Rubio M. 2014. Quantitative trait loci(QTL)and mendelian trait loci(MTL)analysis in Prunus:a breeding perspective and beyond. Plant Molecular Biology Reporter, 32 (1):1-18. doi: 10.1007/s11105-013-0643-7 URL
[93]	Serra O, Giné-Bordonaba J, Eduardo I, Bonany J, Echeverria G, Larrigaudière C, Arús P. 2017. Genetic analysis of the slow-melting flesh character in peach. Tree Genetics & Genomes, 13 (4):77.
[94]	Shen F, Huang Z Y, Zhang B G, Wang Y, Zhang X, Wu T, Xu X F, Zhang X Z, Han Z H. 2019. Mapping gene markers for apple fruit ring rot disease resistance using a multi-omics approach. G3:Genes,Genomes,Genetics, 9 (5):1663-1678.
[95]	Shi P, Xu Z, Zhang S Y, Wang X J, Ma X F, Zheng J C, Xing L B, Zhang D, Ma J J, Han M Y, Zhao C P. 2020. Construction of a high-density SNP-based genetic map and identification of fruit-related QTLs and candidate genes in peach[Prunus persica(L.)Batsch]. BMC Plant Biology, 20 (1):438. doi: 10.1186/s12870-020-02557-3 URL
[96]	Siviero A, Cristofani M, Furtado E L, Garcia A A F, Coelho A S G, Machado M A. 2006. Identification of QTLs associated with citrus resistance to phytophthora gummosis. Journal of Applied Genetics, 47 (1):23-28. pmid: 16424605
[97]	Souleyre E J F, Bowen J K, Matich A J, Tomes S, Chen X, Hunt M B, Wang M Y, Ileperuma N R, Richards K, Rowan D D, Chagné D, Atkinson R G. 2019. Genetic control of α-farnesene production in apple fruit and its role in fungal pathogenesis. Plant Journal, 100 (6):1148-1162. doi: 10.1111/tpj.14504
[98]	Sugiyama A, Omura M, Matsumoto H, Shimada T, Fujii H, Endo T, Shimizu T, Nesumi H, Ikoma Y. 2011. Quantitative trait loci (QTL) analysis of carotenoid content in citrus fruit. Journal of the Japanese Society for Horticultural Science, 80 (2):136-144. doi: 10.2503/jjshs1.80.136 URL
[99]	Sun M Y, Zhang M Y, Singh J, Song B B, Tang Z K, Liu Y Y, Wang R Z, Qin M F, Li J M, Khan A, Wu J. 2020. Contrasting genetic variation and positive selection followed the divergence of NBS-encoding genes in Asian and European pears. BMC Genomics, 21 (1):809. doi: 10.1186/s12864-020-07226-1 pmid: 33213380
[100]	Sun R, Chang Y S, Yang F Q, Wang Y, Li H, Zhao Y B, Chen D M, Wu T, Zhang X Z, Han Z H. 2015. A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality. BMC Genomics, 16 (1):747. doi: 10.1186/s12864-015-1946-x URL
[101]	Sun Rui. 2015. High-density genetic linkage map construction and QTL identification for important fruit quality traits in apple[Ph. D. Dissertation]. Beijing:China Agricultural University. (in Chinese)
	孙瑞. 2015. 苹果高密度遗传连锁图谱构建与重要果实品质性状QTL定位[博士论文]. 北京:中国农业大学.
[102]	Tan Mei-lian. 2007. Creation of sexual hybrid populations and construction of molecular genetic linkage framework map in citrus[Ph. D. Dissertation]. Wuhan: Huazhong Agricultural University. (in Chinese)
	谭美莲. 2007. 柑橘有性杂种群体的获得及分子遗传连锁框架图的构建[博士论文]. 武汉: 华中农业大学.
[103]	Tang Yu-qing, Zheng Xiong-jie, Wang Nan, Yang Hong-bin, Deng Xiu-xin. 2017. QTL analysis of carotenoid content in hybrid populations from red tangerine × trifoliate orange. Acta Horticulturae Sinica, 44 (S1):2516. (in Chinese)
	汤雨晴, 郑雄杰, 王楠, 杨宏斌, 邓秀新. 2017. 红橘 × 枳壳杂交群体果肉类胡萝卜素代谢的QTL分析. 园艺学报, 44 (S1):2516.
[104]	Thapa R, Singh J, Gutierrez B, Arro J, Khan A. 2021. Genome-wide association mapping identifies novel loci underlying fire blight resistance in apple. The Plant Genome, 14 (2):e20087.
[105]	van Ooijen G, van de Burg H A, Cornelissen B J C, Takken F L W. 2008. Structure and function of resistance proteins in solanaceous plants. Annual Review of Phytopathology, 45:43-72. doi: 10.1146/annurev.phyto.45.062806.094430 URL
[106]	Vendramin E, Pea G, Dondini L, Pacheco I, Dettori M T, Gazza L, Scalabrin S, Strozzi F, Tartarini S, Bassi D, Verde I, Rossini L. 2014. A unique mutation in a MYB gene cosegregates with the nectarine phenotype in peach. PLoS ONE, 9 (3):e90574. doi: 10.1371/journal.pone.0090574 URL
[107]	Verma S, Evans K, Guan Y, Luby J J, Rosyara U R, Howard N P, Bassil N, Bink M C A M, van de Weg W E, Peace C P. 2019. Two large-effect QTLs,Ma and Ma3,determine genetic potential for acidity in apple fruit:breeding insights from a multi-family study. Tree Genetics and Genomes, 15 (2):18. doi: 10.1007/s11295-019-1324-y URL
[108]	Wang Hai-bo. 2018. Mapping QTLs for traits related to water use efficiency in apple under drought stress and identification of candidate genes[Ph. D. Dissertation]. Yangling:Northwest A & F University. (in Chinese)
	王海波. 2018. 干旱条件下苹果水分利用效率相关性状的QTL定位和候选基因的筛选与鉴定[博士论文]. 杨凌:西北农林科技大学.
[109]	Wang Lei, Li Xiu-gen, Xue Hua-bai, Wang Long, Li Jiang. 2016. Mapping QTLs for fruit related traits in pear. Acta Horticulturae Sinica, 43 (12):2431-2441. (in Chinese)
	王磊, 李秀根, 薛华柏, 王龙, 李疆. 2016. 梨果实相关性状QTL定位分析. 园艺学报, 43 (12):2431-2441.
[110]	Wang Lirong, Wu Jinlong. 2021. Review for the research of fruit tree germplasm and breeding of new varieties in the past seven decades in China. Acta Horticulturae Sinica, 48 (4):749-758. (in Chinese)
	王力荣, 吴金龙. 2021. 中国果树种质资源研究与新品种选育70年. 园艺学报, 48 (4):749-758.
[111]	Weber C A, Moore G A, Deng Z, Gmitter F G. 2003. Mapping freeze tolerance quantitative trait loci in a Citrus grandis × Poncirus trifoliata F₁ pseudo-testcross using molecular markers. Journal of the American Society for Horticultural Science, 128 (4):508-514. doi: 10.21273/JASHS.128.4.0508 URL
[112]	Weeden N F, Hemmatt M, Lawson D M, Lodhi M, Bell R L, Manganaris A G, Reischs B I, Brown S K, Ye G N. 1994. Development and application of molecular marker linkage maps in woody fruit crops. Euphytica, 77 (12):71-75. doi: 10.1007/BF02551464 URL
[113]	Wu B, Shen F, Chen C J, Liu L, Wang X, Zheng W Y, Deng Y, Wang T, Huang Z Y, Xiao C, Zhou Q, Wang Y, Wu T, Xu X F, Han Z H, Zhang X Z. 2021. Natural variations in a pectin acetylesterase gene,MdPAE10,contribute to prolonged apple fruit shelf life. The Plant Genome, 14 (1):e20084.
[114]	Wu B, Shen F, Wang X, Zheng W Y, Xiao C, Deng Y, Wang T, Huang Z Y, Zhou Q. 2020. Role of MdERF3 and MdERF118 natural variations in apple flesh firmness/crispness retainability and development of QTL-based genomics-assisted prediction. Plant Biotechnology Journal, 19 (5):1022-1037. doi: 10.1111/pbi.13527 URL
[115]	Wu J, Li L T, Li M, Khan M A, Li X G, Chen H, Yin H, Zhang S L. 2014. High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. Journal of Experimental Botany, 65 (20):5771-5781. doi: 10.1093/jxb/eru311 pmid: 25129128
[116]	Wu L M, Han L Q, Li Q, Wang G Y, Zhang H W, Li L. 2021. Using interactome big data to crack genetic mysteries and enhance future crop breeding. Molecular Plant, 14 (1):77-94. doi: 10.1016/j.molp.2020.12.012 pmid: 33340690
[117]	Xu K N, Wang A D, Brown S. 2012. Genetic characterization of the Ma locus with pH and titratable acidity in apple. Molecular Breeding, 30 (2):899-912. doi: 10.1007/s11032-011-9674-7 URL
[118]	Xue H B, Shi T, Wang F F, Zhou H K, Yang J, Wang L, Wang S K, Su Y L, Zhang Z, Qiao Y S, Li X G. 2017. Interval mapping for red/green skin color in Asian pears using a modified QTL-seq method. Horticulture Research, 4 (1):17053. doi: 10.1038/hortres.2017.53 URL
[119]	Yang C Q, Sha G Y, Wei T, Ma B Q, Li C Y, Li P M, Zou Y J, Xu L F, Ma F W. 2021. Linkage map and QTL mapping of red flesh locus in apple using a R1R1 × R6R6 population. Horticultural Plant Journal, 7 (5):393-400. doi: 10.1016/j.hpj.2020.12.008 URL
[120]	Yang Z M, Li G X, Tieman D, Zhu G T. 2019. Genomics approaches to domestication studies of horticultural crops. Horticultural Plant Journal, 5 (6):240-246. doi: 10.1016/j.hpj.2019.11.001
[121]	Yao G F, Ming M L, Allan A C, Gu C, Li L T, Wu X, Wang R Z, Chang Y J, Qi K J, Zhang S L, Wu J. 2017. Map-based cloning of the pear gene MYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis. The Plant Journal, 92 (3):437-451. doi: 10.1111/tpj.13666 URL
[122]	Yu Y, Bai J H, Chen C X, Plotto A, Yu Q B, Baldwin E A, Gmitter F G. 2017. Identification of QTLs controlling aroma volatiles using a‘Fortune’×‘Murcott’(Citrus reticulata)population. BMC Genomics, 18 (1):646. doi: 10.1186/s12864-017-4043-5 URL
[123]	Zhang J C, Zhang D J, Fan Y W, Li C C, Xu P K, Li W, Sun Q, Huang X D, Zhang C Y, Wu L Y, Yang H Z, Wang S Y, Su X M, Li X X, Song Y Y, Wu M E, Lian X M, Li Y B. 2021a. The identification of grain size genes by RapMap reveals directional selection during rice domestication. Nature Communications, 12 (1):5673. doi: 10.1038/s41467-021-25961-1 URL
[124]	Zhang M Y, Xue C, Hu H J, Li J M, Xue Y S, Wang R Z, Fan J, Zou C, Tao S T, Qin M F, Bai B, Li X L, Gu C, Wu S, Chen X, Yang G Y, Liu Y Y, Sun M Y, Fei Z J, Zhang S L, Wu J. 2021b. Genome-wide association studies provide insights into the genetic determination of fruit traits of pear. Nature Communications, 12 (1):1144. doi: 10.1038/s41467-021-21378-y URL
[125]	Zhang Xiao-li, Ai Sha-jiang·Mai Mai-ti, Xue Hua-bai, Yan Peng, Wang Ji-xun. 2018. Recent advances in research on the genetic linkage maps in pears. Journal of Fruit Science, 35 (S1):3-10. (in Chinese)
	张校立, 艾沙江 · 买买提, 薛华柏, 闫鹏, 王继勋. 2018. 梨遗传连锁图谱研究进展. 果树学报, 35 (S1):3-10.
[126]	Zhao Keke, Cui Lulu, Li Chunxiu, Dang Jiangbo, Liang Guolu, Xiang Suqiong. 2021. Research advances on parthenocarpy in Citrus. Acta Horticulturae Sinica, 48 (4):811-824. (in Chiense)
	赵科科, 崔璐璐, 李春秀, 党江波, 梁国鲁, 向素琼. 2021. 柑橘单性结实研究进展. 园艺学报, 48 (4):811-824.
[127]	Zheng C X, Shen F, Wang Y, Wu T, Xu X F, Zhang X Z, Han Z H. 2020a. Intricate genetic variation networks control the adventitious root growth angle in apple. BMC Genomics, 21 (1):852. doi: 10.1186/s12864-020-07257-8 URL
[128]	Zheng W Y, Shen F, Wang W Q, Wu B, Wang X, Xiao C, Tian Z D, Yang X L, Yang J, Wang Y, Wu T, Xu X F, Han Z H, Zhang X Z. 2020b. Quantitative trait loci-based genomics-assisted prediction for the degree of apple fruit cover color. Plant Genome, 13 (3):e20047.
[129]	Zheng X J, Tang Y Q, Ye J L, Pan Z Y, Tan M L, Xie Z Z, Chai L J, Xu Q, Fraser P D, Deng X X. 2019. SLAF-based construction of a high-density genetic map and its application in QTL mapping of carotenoids content in citrus fruit. Journal of Agricultural and Food Chemistry, 67 (3):994-1002. doi: 10.1021/acs.jafc.8b05176 pmid: 30589260
[130]	Zhou H, Lin-Wang K, Wang H L, Gu C, Dare A P, Espley R V, He H P, Allan A C, Han Y P. 2015. Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant Journal, 82 (1):105-121. doi: 10.1111/tpj.12792 URL
[131]	Zhu H C, Li C, Gao C X. 2020. Applications of CRISPR-Cas in agriculture and plant biotechnology. Nature Reviews Molecular Cell Biology, 21 (11):661-677. doi: 10.1038/s41580-020-00288-9 URL
[132]	Zhu Jun. 2007. Genetics. Beijing: China Agriculture Press:324-325. (in Chinese)
	朱军. 2007. 遗传学. 北京: 中国农业出版社:324-325.
[133]	Zou C, Wang P X, Xu Y B. 2016. Bulked sample analysis in genetics,genomics and crop improvement. Plant Biotechnology Journal, 14 (10):1941-1955. doi: 10.1111/pbi.12559 URL