The art of tartness: the genetics of organic acid content in fresh fruits

Abstract

Organic acids are major determinants of fruit flavor and a primary focus of fruit crop breeding. The accumulation of organic acids is determined by their synthesis, degradation, and transport, all of which are manipulated by sophisticated genetic mechanisms. Constant exploration of the genetic basis of organic acid accumulation, especially through linkage analysis, association analysis, and evolutionary analysis, have identified numerous loci in recent decades. In this review, the genetic loci and genes responsible for malate and citrate contents in fruits are discussed from the genetic perspective. Technologies such as gene transformation and genome editing as well as efficient breeding using marker-assisted selection (MAS) and genomic selection (GS) are expected to break the bottleneck of traditional fruit crop breeding and promote fruit quality improvement.

Acknowledgements

This work was supported by the Shaanxi Science and Technology Innovation Team Project (2022TD-12) and the Young Elite Scientists Sponsorship Program by CAST (2023QNRC001).

Author contributions

S.M. and M.L. conceived this review. S.M. wrote original draft. X.W., L.Z., B.M., and M.L. revised the manuscript. All authors approved the final manuscript.

Data availability statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

Conflict of interests

The authors declare no conflict of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1] Zhao J, Sauvage C, Zhao J. et al. Meta-analysis of genome-wide association studies provides insights into genetic control of tomato flavor. Nat Commun. 2019; 10 :1534

[2] Li Y, Cao K, Zhu G. et al. Genomic analyses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history. Genome Biol. 2019; 20 :36

[3] Lin Q, Chen J, Liu X. et al. A metabolic perspective of selection for fruit quality related to apple domestication and improvement. Genome Biol. 2023; 24 :95

[4] Baccichet I, Tagliabue GA, Da Silva LC. et al. Sensory perception of citrate and malate and their impact on the overall taste in apricot (Prunus armeniaca L.) fruits. Sci Hortic. 2023; 321 :112266

[5] Drkenda P, ´ Culah A, Spaho N. et al. How do consumers receive sensory attributes of apple? Food Secur. 2021; 10 :2667

[6] Colaric M, Veberic R, Stampar F. et al. Evaluation of peach and nectarine fruit quality and correlations between sensory and chemical attributes. J Sci Food Agric. 2005; 85 :2611-6

[7] Esti M, Messia MC, Sinesio F. et al. Quality evaluation of peaches and nectarines by electrochemical and multivariate analyses: relationships between analytical measurements and sensory attributes. Food Chem. 1997; 60 :659-66

[8] Liebhard R, Kellerhals M, Pfammatter W. et al. Mapping quantitative physiological traits in apple (Malus × domestica Borkh.). Plant Mol Biol. 2003; 52 :511-26

[9] Huang X-Y, Wang C-K, Zhao Y-W. et al. Mechanisms and regulation of organic acid accumulation in plant vacuoles. Hortic Res. 2021; 8 :227

[10] Etienne A, Génard M, Lobit P. et al. What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J Exp Bot. 2013; 64 :1451-69

[11] Ma B, Chen J, Zheng H. et al. Comparative assessment of sugar and malic acid composition in cultivated and wild apples. Food Chem. 2015; 172 :86-91

[12] Wang L, He F, Huang Y. et al. Genome of wild mandarin and domestication history of mandarin. Mol Plant. 2018; 11 :1024-37

[13] Zhou J, Yang S, Ma Y. et al. Soluble sugar and organic acid composition and flavor evaluation of Chinese cherry fruits. Food Chem X. 2023; 20 :100953

[14] Xu K, Wang A, Brown S. Genetic characterization of the Ma locus with pH and titratable acidity in apple. Mol Breeding. 2012; 30 :899-912

[15] Ma B, Zhao S, Wu B. et al. 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 Genet Genomes. 2016; 12 :1

[16] Jia D, Shen F, Wang Y. et al. Apple fruit acidity is genetically diversified by natural variations in three hierarchical epistatic genes: MdSAUR37, MdPP2CH and MdALMTII. Plant J. 2018; 95 :427-43

[17] Cao K, Zhou Z, Wang Q. et al. Genome-wide association study of 12 agronomic traits in peach. Nat Commun. 2016; 7 :13246

[18] Zhang M-Y, Xue C, Hu H. et al. Genome-wide association studies provide insights into the genetic determination of fruit traits of pear. Nat Commun. 2021; 12 :1144

[19] Liao L, Zhang W, Zhang B. et al. Unraveling a genetic roadmap for improved taste in the domesticated apple. Mol Plant. 2021; 14 :1454-71

[20] Wang Q, Cao K, Cheng L. et al. Multi-omics approaches identify a key gene, PpTST1, for organic acid accumulation in peach. Hortic Res. 2022; 9 :uhac026

[21] Yamaki S. Isolation of vacuoles from immature apple fruit flesh and compartmentation of sugars, organic acids, phenolic compounds and amino acids. Plant Cell Physiol. 1984; 25 :151-66

[22] Moing A, Svanella L, Rolin D. et al. Compositional changes during the fruit development of two peach cultivars differing in juice acidity. J Am Soc Hortic Sci. 1998; 123 :770-5

[23] Deng H, Li X, Wang Y. et al. Organic acid accumulation and associated dynamic changes in enzyme activity and gene expression during fruit development and ripening of common loquat and its interspecific hybrid. Food Secur. 2023; 12 :911

[24] Usenik V, Fabčič J, Štampar F. Sugars, organic acids, phenolic composition and antioxidant activity of sweet cherry (Prunus avium L.). Food Chem. 2008; 107 :185-92

[25] Yamaki YT. Organic acids in the juice of citrus fruits. J Jpn Soc Hortic Sci. 1989; 58 :587-94

[26] Sweetman C, Deluc LG, Cramer GR. et al. Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry. 2009; 70 :1329-44

[27] Miller SS, Driscoll BT, Gregerson RG. et al. Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J. 1998; 15 :173-84

[28] Diakou P, Svanella L, Raymond P. et al. Phosphoenolpyruvate carboxylase during grape berry development: protein level, enzyme activity and regulation. Funct Plant Biol. 2000; 27 :221

[29] Yao Y-X, Li M, Zhai H. et al. Isolation and characterization of an apple cytosolic malate dehydrogenase gene reveal its function in malate synthesis. J Plant Physiol. 2011; 168 :474-80

[30] Caburatan L, Park J. Differential expression, tissue-specific distribution, and posttranslational controls of phosphoenolpyruvate carboxylase. Plants (Basel). 2021; 10 :1887

[31] Leegood RC, Walker RP. Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Biochem Biophys. 2003; 414 :204-10

[32] Famiani F, Cultrera NGM, Battistelli A. et al. Phosphoenolpyruvate carboxykinase and its potential role in the catabolism of organic acids in the flesh of soft fruit during ripening. J Exp Bot. 2005; 56 :2959-69

[33] Yao Y-X, Li M, Liu Z. et al. Molecular cloning of three malic acid related genes MdPEPC, MdVHA-A, MdcyME and their expression analysis in apple fruits. Sci Hortic. 2009; 122 :404-8

[34] Sadka A, Dahan E, Cohen L. et al. Aconitase activity and expression during the development of lemon fruit. Physiol Plant. 2000; 108 :255-62

[35] Lin Q, Wang C, Dong W. et al. Transcriptome and metabolome analyses of sugar and organic acid metabolism in ponkan (Citrus reticulata ) fruit during fruit maturation. Gene. 2015; 554 :64-74

[36] Zhu L, Li B, Wu L. et al. MdERDL6-mediated glucose efflux to the cytosol promotes sugar accumulation in the vacuole through up-regulating TSTs in apple and tomato. Proc Natl Acad Sci USA. 2021; 118 :e2022788118

[37] Zhu L, Li Y, Wang C. et al. The SnRK2.3-AREB1-TST1/ 2 cascade activated by cytosolic glucose regulates sugar accumulation across tonoplasts in apple and tomato. Nat Plants. 2023; 9 :951-64

[38] Liu Z, Mao Z, Li M. et al. Vacuole: a repository to control fruit flavor quality. Fruit Res. 2023; 3 :12

[39] Ye J, Wang X, Hu T. et al. An InDel in the promoter of ALUMINUM-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell. 2017; 29 :2249-68

[40] Bai Y, Dougherty L, Li M. et al. 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. Mol Gen Genomics. 2012; 287 :663-78

[41] Li C, Dougherty L, Coluccio AE. et al. Apple ALMT9 requires a conserved C-terminal domain for malate transport underlying fruit acidity. Plant Physiol. 2020; 182 :992-1006

[42] De Angeli A, Baetz U, Francisco R. et al. The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera. Planta. 2013; 238 :283-91

[43] Alabd A, Cheng H, Ahmad M. et al. ABRE-BINDING FACTOR3-WRKY DNA-BINDING PROTEIN44 module promotes salinity-induced malate accumulation in pear. Plant Physiol. 2023; 192 :1982-96

[44] Fu B, Wang W, Li X. et al. A dramatic decline in fruit citrate induced by mutagenesis of a NAC transcription factor, AcNAC1. Plant Biotechnol J. 2023; 21 :1695-706

[45] Liu S, Liu X, Gou B. et al. The interaction between CitMYB52 and CitbHLH2 negatively regulates citrate accumulation by activating CitALMT in citrus fruit. Front Plant Sci. 2022; 13 :848869

[46] Hurth MA, Suh SJ, Kretzschmar T. et al. Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiol. 2005; 137 :901-10

[47] Yao Y-X, Dong Q-L, You C-X. et al. Expression analysis and functional characterization of apple MdVHP1 gene reveals its involvement in Na ⁺, malate and soluble sugar accumulation. Plant Physiol Biochem. 2011; 49 :1201-8

[48] Shimada T, Nakano R, Shulaev V. et al. Vacuolar citrate/H ⁺ symporter of citrus juice cells. Planta. 2006; 224 :472-80

[49] Maliepaard C, Alston FH, Van Arkel G. et al. Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet. 1998; 97 :60-73

[50] Kenis K, Keulemans J, Davey MW. Identification and stability of QTLs for fruit quality traits in apple. Tree Genet Genomes. 2008; 4 :647-61

[51] Khan SA, Beekwilder J, Schaart JG. et al. Differences in acidity of apples are probably mainly caused by a malic acid transporter gene on LG16. Tree Genet Genomes. 2013; 9 :475-87

[52] Verma S, Evans K, Guan Y. et al. Two large-effect QTLs, Ma and Ma3, determine genetic potential for acidity in apple fruit: breeding insights from a multi-family study. Tree Genet Genomes. 2019; 15 :18

[53] Rymenants M, Van De Weg E, Auwerkerken A. et al. Detection of QTL for apple fruit acidity and sweetness using sensorial evaluation in multiple pedigreed full-sib families. Tree Genet Genomes. 2020; 16 :71

[54] Peng Y, Yuan Y, Chang W. et al. Transcriptional repression of MdMa1 by MdMYB21 in Ma locus decreases malic acid content in apple fruit. Plant J. 2023; 115 :1231-42

[55] Zhang Q, Ma B, Li H. et al. Identification, characterization, and utilization of genome-wide simple sequence repeats to identify a QTL for acidity in apple. BMC Genomics. 2012; 13 :537

[56] Sun R, Chang Y, Yang F. et al. A dense SNP genetic map constructed using restriction site-associated DNA sequencing enables detection of QTLs controlling apple fruit quality. BMC Genomics. 2015; 16 :747

[57] Jia D, Wu P, Shen F. et al. Genetic variation in the promoter of an R2R3-MYB transcription factor determines fruit malate content in apple (Malus domestica Borkh.). Plant Physiol. 2021; 186 :549-68

[58] Ban S, Xu K. Identification of two QTLs associated with high fruit acidity in apple using pooled genome sequencing analysis. Hortic Res. 2020; 7 :171

[59] Gao M, Yang N, Shao Y. et al. An insertion in the promoter of a malate dehydrogenase gene regulates malic acid content in apple fruit. Plant Physiol. 2024;kiae303

[60] Fu W, Zhao L, Qiu W. et al. Whole-genome resequencing identifies candidate genes and allelic variation in the MdNADP-ME promoter that regulate fruit malate and fructose contents in apple. Plant Commun. 2024; 100973 :

[61] Kumar S, Molloy C, Hunt M. et al. GWAS provides new insights into the genetic mechanisms of phytochemicals production and red skin colour in apple. Hortic Res. 2022; 9 :uhac218

[62] Duan N, Bai Y, Sun H. et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun. 2017; 8 :249

[63] Sun X, Jiao C, Schwaninger H. et al. Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nat Genet. 2020; 52 :1423-32

[64] Ma B, Liao L, Fang T. et al. A Ma10 gene encoding P-type ATPase is involved in fruit organic acid accumulation in apple. Plant Biotechnol J. 2019; 17 :674-86

[65] Zheng L, Liao L, Duan C. et al. Allelic variation of MdMYB123 controls malic acid content by regulating MdMa1 and MdMa11 expression in apple. Plant Physiol. 2023; 192 :1877-91

[66] Velasco R, Zharkikh A, Affourtit J. et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet. 2010; 42 :833-9

[67] Li C, Krishnan S, Zhang M. et al. Alternative splicing underpins the ALMT9 transporter function for vacuolar malic acid accumulation in apple. Adv Sci. 2024; 11 :e2310159

[68] Canel C, Bailey-Serres JN, Roose ML. In vitro [ 14 C]citrate uptake by tonoplast vesicles of acidless citrus juice cells. J Am Soc Hortic Sci. 1995; 120 :510-4

[69] Strazzer P, Spelt CE, Li S. et al. Hyperacidification of citrus fruits by a vacuolar proton-pumping P-ATPase complex. Nat Commun. 2019; 10 :744

[70] He J, Xu Y, Huang D. et al. TRIPTYCHON-LIKE regulates aspects of both fruit flavor and color in citrus. J Exp Bot. 2022; 73 :3610-24

[71] Verweij W, Spelt C, Di Sansebastiano G-P. et al. An H ⁺ P-ATPase on the tonoplast determines vacuolar pH and flower colour. Nat Cell Biol. 2008; 10 :1456-62

[72] Faraco M, Spelt C, Bliek M. et al. Hyperacidification of vacuoles by the combined action of two different P-ATPases in the tonoplast determines flower color. Cell Rep. 2014; 6 :32-43

[73] Quattrocchio F, Verweij W, Kroon A. et al. PH4 of petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell. 2006; 18 :1274-91

[74] Butelli E, Licciardello C, Ramadugu C. et al. Noemi controls production of flavonoid pigments and fruit acidity and illustrates the domestication routes of modern citrus varieties. Curr Biol. 2019; 29 :158-164.e2

[75] Huang Y, He J, Xu Y. et al. Pangenome analysis provides insight into the evolution of the orange subfamily and a key gene for citric acid accumulation in citrus fruits. Nat Genet. 2023; 55 :1964-75

[76] Wu GA, Terol J, Ibanez V. et al. Genomics of the origin and evolution of citrus. Nature. 2018; 554 :311-6

[77] Minamikawa MF, Nonaka K, Kaminuma E. et al. Genome-wide association study and genomic prediction in citrus: potential of genomics-assisted breeding for fruit quality traits. Sci Rep. 2017; 7 :4721

[78] Khefifi H, Dumont D, Costantino G. et al. Mapping of QTLs for citrus quality traits throughout the fruit maturation process on clementine (Citrus reticulata × C. sinensis ) and mandarin (C. reticulata Blanco) genetic maps. Tree Genet Genomes. 2022; 18 :40

[79] Lu X, Cao X, Li F. et al. Comparative transcriptome analysis reveals a global insight into molecular processes regulating citrate accumulation in sweet orange (Citrus sinensis ). Physiol Plant. 2016; 158 :463-82

[80] Asins MJ, Raga V, Bernet GP. et al. Genetic analysis of reproductive, vegetative and fruit quality traits to improve citrus varieties. Tree Genet Genomes. 2015; 11 :117

[81] Yu Y, Chen C, Gmitter FG. QTL mapping of mandarin (Citrus reticulata ) fruit characters using high-throughput SNP markers. Tree Genet Genomes. 2016; 12 :77

[82] Curtolo M, Cristofani-Yaly M, Gazaffi R. et al. QTL mapping for fruit quality in citrus using DArTseq markers. BMC Genomics. 2017; 18 :289

[83] Bastías A, López-Climent M, Valcárcel M. et al. Modulation of organic acids and sugar content in tomato fruits by an abscisic acid-regulated transcription factor. Physiol Plant. 2011; 141 :215-26

[84] Schauer N, Zamir D, Fernie AR. Metabolic profiling of leaves and fruit of wild species tomato: a survey of the Solanum lycopersicum complex. J Exp Bot. 2004; 56 :297-307

[85] Sauvage C, Segura V, Bauchet G. et al. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 2014; 165 :1120-32

[86] Tieman D, Zhu G, Resende MFR. et al. A chemical genetic roadmap to improved tomato flavor. Science. 2017; 355 :391-4

[87] Bauchet G, Grenier S, Samson N. et al. Identification of major loci and genomic regions controlling acid and volatile content in tomato fruit: implications for flavor improvement. New Phytol. 2017; 215 :624-41

[88] Gai W, Yang F, Yuan L. et al. Multiple-model GWAS identifies optimal allelic combinations of quantitative trait loci for malic acid in tomato. Hortic Res. 2023; 10 :uhad021

[89] Razifard H, Ramos A, Della Valle AL. et al. Genomic evidence for complex domestication history of the cultivated tomato in Latin America. Mol Biol Evol. 2020; 37 :1118-32

[90] Gai W, Yuan L, Yang F. et al. Genome-wide variants and optimal allelic combinations for citric acid in tomato. Hortic Res. 2024; 11 :uhae070

[91] Ruggieri V, Francese G, Sacco A. et al. An association mapping approach to identify favourable alleles for tomato fruit quality breeding. BMC Plant Biol. 2014; 14 :337

[92] Zhao J, Xu Y, Ding Q. et al. Association mapping of main tomato fruit sugars and organic acids. Front Plant Sci. 2016; 7 :1286

[93] Çolak NG, Eken NT, Ülger M. et al. Exploring wild alleles from Solanum pimpinellifolium with the potential to improve tomato flavor compounds. Plant Sci. 2020; 298 :110567

[94] Fulton TM, Bucheli P, Voirol E. et al. Quantitative trait loci (QTL) affecting sugars, organic acids and other biochemical properties possibly contributing to flavor, identified in four advanced backcross populations of tomato. Euphytica. 2002; 127 :163-77

[95] Toubiana D, Semel Y, Tohge T. et al. Metabolic profiling of a mapping population exposes new insights in the regulation of seed metabolism and seed, fruit, and plant relations. PLoS Genet. 2012; 8 :e1002612

[96] Causse M, Duffe P, Gomez MC. et al. A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot. 2004; 55 :1671-85

[97] Capel C, Fernández Del Carmen A, Alba JM. et al. Wide-genome QTL mapping of fruit quality traits in a tomato RIL population derived from the wild-relative species Solanum pimpinellifolium L. Theor Appl Genet. 2015; 128 :2019-35

[98] Tieman DM, Zeigler M, Schmelz EA. et al. Identification of loci affecting flavour volatile emissions in tomato fruits. J Exp Bot. 2006; 57 :887-96

[99] Schauer N, Semel Y, Roessner U. et al. Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol. 2006; 24 :447-54

[100] Wang L, Jiang X, Zhao L. et al. A candidate PpRPH gene of the D locus controlling fruit acidity in peach. Plant Mol Biol. 2021; 105 :321-32

[101] Yu Y, Guan J, Xu Y. et al. Population-scale peach genome analyses unravel selection patterns and biochemical basis underlying fruit flavor. Nat Commun. 2021; 12 :3604

[102] Reshef N, Karn A, Manns DC. et al. Stable QTL for malate levels in ripe fruit and their transferability across Vitis species. Hortic Res. 2022; 9 :uhac009

[103] Bayo-Canha A, Costantini L, Fernández-Fernández JI. et al. QTLs related to berry acidity identified in a wine grapevine population grown in warm weather. Plant Mol Biol Rep. 2019; 37 :157-69

[104] Alahakoon D, Fennell A, Helget Z. et al. Berry anthocyanin, acid, and volatile trait analyses in a grapevine-interspecific F2 population using an integrated GBS and rhAmpSeq genetic map. Plants (Basel). 2022; 11 :696

[105] Wu J, Wang Y, Xu J. et al. Diversification and independent domestication of Asian and European pears. Genome Biol. 2018; 19 :77

[106] Cohen S, Itkin M, Yeselson Y. et al. The PH gene determines fruit acidity and contributes to the evolution of sweet melons. Nat Commun. 2014; 5 :4026

[107] Zhao G, Lian Q, Zhang Z. et al. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat Genet. 2019; 51 :1607-15

[108] Zhang C, Geng Y, Liu H. et al. Low-acidity ALUMINUM-DEPENDENT MALATE TRANSPORTER4 genotype determines malate content in cultivated jujube. Plant Physiol. 2023; 191 :414-27

[109] Liu H, Zhao X, Bi J. et al. A natural mutation in the promoter of the aconitase gene ZjACO3 influences fruit citric acid content in jujube. Hortic Res. 2024; 11 :uhae003

[110] Burger Y, Sa’ar U, Distelfeld A. et al. Development of sweet melon (Cucumis melo ) genotypes combining high sucrose and organic acid content. J Am Soc Hortic Sci. 2003; 128 :537-40

[111] Li M, Su J, Yang H. et al. Grape tartaric acid: chemistry, function, metabolism, and regulation. Horticulturae. 2023; 9 :1173

[112] Houel C, Chatbanyong R, Doligez A. et al. Identification of stable QTLs for vegetative and reproductive traits in the microvine (Vitis vinifera L.) using the 18 K Infinium chip. BMC Plant Biol. 2015; 15 :205

[113] Duchêne É, Dumas V, Butterlin G. et al. Genetic variations of acidity in grape berries are controlled by the interplay between organic acids and potassium. Theor Appl Genet. 2020; 133 :993-1008

[114] Negus KL, Chen L-L, Fresnedo-Ramírez J. et al. Identification of QTLs for berry acid and tannin in a Vitis aestivalis -derived ‘Norton’-based population. Fruit Res. 2021; 1 :8

[115] Dirlewanger E, Pronier V, Parvery C. et al. Genetic linkage map of peach [ Prunus persica (L.) Batsch] using morphological and molecular markers. Theor Appl Genet. 1998; 97 :888-95

[116] Dirlewanger E, Moing A, Rothan C. et al. Mapping QTLs controlling fruit quality in peach (Prunus persica (L.) Batsch). Theor Appl Genet. 1999; 98 :18-31

[117] Etienne C, Rothan C, Moing A. et al. Candidate genes and QTLs for sugar and organic acid content in peach [ Prunus persica (L.) Batsch]. Theor Appl Genet. 2002; 105 :145-59

[118] Dirlewanger E, Cosson P, Boudehri K. et al. Development of a second-generation genetic linkage map for peach [ Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genomes. 2006; 3 :1-13

[119] Boudehri K, Bendahmane A, Cardinet G. et al. Phenotypic and fine genetic characterization of the D locus controlling fruit acidity in peach. BMC Plant Biol. 2009; 9 :59

[120] Eduardo I, López-Girona E, Batlle I. et al. Development of diagnostic markers for selection of the subacid trait in peach. Tree Genet Genomes. 2014; 10 :1695-709

[121] Hickey LT, Hafeez AN, Robinson H. et al. Breeding crops to feed 10 billion. Nat Biotechnol. 2019; 37 :744-54

[122] Chagné D, Vanderzande S, Kirk C. et al. Validation of SNP markers for fruit quality and disease resistance loci in apple (Malus × domestica Borkh.) using the OpenArray® platform. Hortic Res. 2019; 6 :30

[123] Kumar S, Garrick DJ, Bink MC. et al. Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics. 2013; 14 :393

[124] Alemu A, Åstrand J, Montesinos-López OA. et al. Genomic selection in plant breeding: key factors shaping two decades of progress. Mol Plant. 2024; 17 :552-78

[125] Kumar S, Chagné D, Bink MCAM. et al. Genomic selection for fruit quality traits in apple (Malus × domestica Borkh.). PLoS One. 2012; 7 :e36674

[126] Kostick SA, Bernardo R, Luby JJ. Genomewide selection for fruit quality traits in apple: breeding insights gained from prediction and postdiction. Hortic Res. 2023; 10 :uhad088

[127] Chen K, Wang Y, Zhang R. et al. CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol. 2019; 70 :667-97

[128] Gao C. Genome engineering for crop improvement and future agriculture. Cell. 2021; 184 :1621-35

[129] Holme IB, Gregersen PL, Brinch-Pedersen H. Induced genetic variation in crop plants by random or targeted mutagenesis: convergence and differences. Front Plant Sci. 2019; 10 :1468

[130] Zsögön A, Cermak T, Voytas D. et al. Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: case study in tomato. Plant Sci. 2017; 256 :120-30

[131] Li T, Yang X, Yu Y. et al. Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol. 2018; 36 :1160-3

[132] Zsögön A, Čermák T, Naves ER. et al. De novo domestication of wild tomato using genome editing. Nat Biotechnol. 2018; 36 :1211-6