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Expansin genes are candidate markers for the control of fruit weight in peach

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Abstract

Fruit weight is an important target trait in peach breeding and culture. Although many studies have investigated quantitative trait loci (QTL) associated with fruit weight and cell wall development, no causal genes have been identified to date. Expansins (EXPs) are plant cell wall-loosening proteins that modulate the enlargement and softening of fruit, but their role in peach development is unknown. To address this issue, we evaluated the expression profiles of all EXP genes in the peach genome. We identified 29 genes that could be classified into six groups according to their temporal expression patterns during fruit development. A genome-wide association analysis showed that six of these genes were located in the confidence intervals of QTL regions of fruit weight. The expression of two of the genes, ppa017982m and ppa010443m, was positively correlated with fruit diameter, suggesting that they control fruit weight by regulating cell enlargement. After screening the single nucleotide polymorphism (SNP) distribution in varieties of peach that bear small or large fruit (n = 30 each), an SNP in chromosome 5 (nucleotide 5,026,380) was identified in the promoter region of ppa017982m. This SNP can serve as a molecular marker in breeding programs designed to eliminate small fruit varieties.

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References

  • Abbott AG, Rajapakse S, SosinskiB LuZX, Sossey-AlaouiK Gannavarapu M, Reighard G, Ballard RE, Baird WV, Scorza R, Callahan A (1997) Construction of saturated linkage maps of peach crosses segregating for characters controlling fruit quality, tree architecture and pest resistance. Acta Hortic 465:41–49

    Google Scholar 

  • Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha S, Scheffler BE, Jenkins JN, Abdukarim A (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92:478–487

    Article  CAS  PubMed  Google Scholar 

  • Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, Li Y, Meng DZ, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I et al (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begum H, Spindel JE, Lalusin A, Borromeo T, Gregorio G, Hernandez J, Virk P, Collard B, McCouch SR (2015) Genome-wide association mapping for yield and other agronomic traits in an elite breeding population of tropical rice (Oryza sativa). PLoS ONE 10(3):e0119873

    Article  PubMed  PubMed Central  Google Scholar 

  • Caderas D, Muster M, Vogler H, Mandel T, Rose JKC, McQueen-Mason S, Kuhlemeier C (2000) Limited correlation between expansin gene expression and elongation growth rate. Plant Physiol 123:1399–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao K, Wang LR, Zhu GR, Fang WC, Chen CW, Luo J (2012) Genetic diversity, linkage disequilibrium, and association mapping analyses of peach (Prunus persica) landraces in China. Tree Genet Genomes 8:975–990

    Article  Google Scholar 

  • Chen F, Dahal P, Bradford KJ (2001) Two tomato expansin genes show divergent expression and localization in embryos during seed development and germination. Plant Physiol 127:928–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin JP, Gévaudant F, Hernould M (2011) Elucidating the functional role of endoreduplication in tomato fruit development. Ann Bot-London 107:1159–1169

    Article  CAS  Google Scholar 

  • Cong B, Liu JP, Tanksley SD (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. PNAS 99:13606–13611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dal Santo S, Vannozzi A, Tornielli GB, Fasoli M, Venturini L, Pezzotti M, Zenoni S (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS ONE 8(4):e62206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Jong M, Wolters-Arts M, Schimmel BCJ, Stultiens CLM, de Groot PFM, Powers SJ, Tikunov YM, Bovy AG, Mariani C, Vriezen WH, Rieu I (2015) Solanum lycopersicum AUXIN RESPONSE FACTOR 9 regulates cell division activity during early tomato fruit development. J Exp Bot 66:3405–3416

    Article  PubMed  PubMed Central  Google Scholar 

  • Devoghalaere F, Doucen T, Guitton B, Keeling J, Payne W, Ling TJ, Ross JJ, Hallett IC, Gunaseelan K, Dayatilake GA, Diak R, Breen KC, Tustin DS, Costes E, Chagné D, Schaffer RJ, David KM (2012) A genomics approach to understanding the role of auxin in apple (Malus × domestica) fruit size control. BMC Plant Biol 12:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dirlewanger E, Moing A, Rothan C, Svanella L, Pronier V, Guye A, Plomion C, Monet R (1999) Mapping QTLs controlling fruit quality in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 98:18–31

    Article  CAS  Google Scholar 

  • Doligez A, Bertrand Y, Farnos M, Grolier M, Romieu C, Esnault F, Dias S, Berger G, François P, Pons T, Ortigosa P, Roux C, Houel C, Laucou V, Bacilieri R, Péros J, This P (2013) New stable QTLs for berry weight do not colocalize with QTLs for seed traits in cultivated grapevine (Vitis vinifera L.). BMC Plant Biol 13:217

    Article  PubMed  PubMed Central  Google Scholar 

  • Eduardo I, Pacheco I, Chietera G, Bassi D, Pozzi C, Vecchietti A, Rossini L (2011) QTL analysis of fruit quality traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genomes 7:323–335

    Article  Google Scholar 

  • Etienne C, Rothan C, Moing A, Plomion C, Bodénès C, Svanella-Dumas L, Cosson P, Pronier V, Monet R, Dirlewanger E (2002) Candidate genes and QTLs for sugar and organic acid content in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 105:145–159

    Article  CAS  PubMed  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu JM, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064

    Article  CAS  PubMed  Google Scholar 

  • Franceschi PD, Stegmeir T, Cabrera A, van der Knaap E, Rosyara UR, Sebolt AM, Dondini L, Dirlewanger E, Quero-Garcia J, Campoy JA, Iezzoni AF (2013) Cell number regulator genes in Prunus provide candidate genes for the control of fruit size in sweet and sour cherry. Mol Breeding 32:311–326

    Article  Google Scholar 

  • Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knaap E, Cong B, Liu JP, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88

    Article  CAS  PubMed  Google Scholar 

  • Harada T, Kurahashi W, Yanai M, Wakasa Y, Satoh T (2005) Involvement of cell proliferation and cell enlargement in increasing the fruit size of Malus species. Sci Hortic 105:447–456

    Article  CAS  Google Scholar 

  • Hayama H, Shimada T, Haji T, Ito A, Kashimura Y, Yoshioka H (2000) Molecular cloning of a ripening-related expansin cDNA in peach: evidence for no relationship between expansin accumulation and change in fruit firmness during storage. J Plant Physiol 157:567–573

    Article  CAS  Google Scholar 

  • Hayama H, Ito A, Moriguchi T, Kashimura Y (2003) Identification of a new expansin gene closely associated with peach fruit softening. Postharvest Biol Tecnol 29:1–10

    Article  CAS  Google Scholar 

  • Hayama H, Shimada T, Fujii H, Ito A, Kashimura Y (2006) Ethylene-regulation of fruit softening and softening-related genes in peach. J Exp Bot 57:4071–4077

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Wei XH, Sang T, Zhao Q, Feng Q, Zhao Y, Li CY, Zhu CR, Lu TT, Zhang ZW, Li M, Fan DL, Guo YL, Wang AH, Wang L (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105

    Article  CAS  PubMed  Google Scholar 

  • Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S, McArtney S, Pichler FB, Snowden KC, Ward S (2008) Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 8:16

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia GQ, Huang XH, Zhi H, Zhao Y, Zhao Q, Li WJ, Chai Y, Yang LF, Liu KY, Lu HY, Zhu CR, Lu YQ, Zhou CC, Fan DL, Weng QJ et al (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45:957–961

    Article  CAS  PubMed  Google Scholar 

  • Lee DK, Ahn JH, Song SK, Choi YD, Lee JS (2003) Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol 131:985–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin CF, Choi HS, Cho HT (2011) Root hair-specific EXPANSIN A7 is required for root hair elongation in Arabidopsis. Mol Cells 31:393–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linge CS, Bassi D, Bianco L, Pacheco I, Pirona R, Rossini L (2015) Genetic dissection of fruit weight and size in an F2 peach (Prunus persica (L.) Batsch) progeny. Mol Breeding 35:71

    Article  Google Scholar 

  • Malladi A, Hirst PM (2010) Increase in fruit size of a spontaneous mutant of ‘Gala’ apple (Malus domestica Borkh.) is facilitated by altered cell production and enhanced cell size. J Exp Bot 61:3003–3013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olmstead JW, Iezzoni AF, Whiting MD (2007) Genotypic differences in sweet cherry fruit size are primarily a function of cell number. JASHS 132:5697–5703

    Google Scholar 

  • Quilot B, Wu BH, Kervella J, Génard M, Foulongne M, Moreau K (2004) QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theor Appl Genet 109:884–897

    Article  CAS  PubMed  Google Scholar 

  • Rose Jocelyn K C, Lee Howard H, Bennett Alan B (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. PNAS 94:5955–5960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scorza R, May LG, Purnell B, Upchurch B (1991) Differences in number and area of mesocarp cells between small- and large-fruited peach cultivars. J Am Soc Hortic Sci 116:861–864

    Google Scholar 

  • Song XJ, Huang W, Shi M, Zhu M, Lin H (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630

    Article  CAS  PubMed  Google Scholar 

  • Sosinski B, Sossey-Alaoui K, Rajapakse S, Glassmoyer K, Ballard RE, Abbott AG, Lu ZX, Baird WV, Reighard G, Tabb A, Scorza R (1998) Use of AFLP and RFLP markers to create a combined linkage map in peach [Prunus persica (L.) Batsch] for use in marker assisted selection. Acta Hort 465:61–68

    Article  CAS  Google Scholar 

  • The International Peach Genome Initiative (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Article  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ESIV (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Article  CAS  PubMed  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu J, Li LT, Li M, Awais Khan M, Li XG, Chen H, Yin H, Zhang SL (2014) High-density genetic linkage map construction and identification of fruit-related QTLs in pear using SNP and SSR markers. J Exp Bot 65:5771–5781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto T, Shimada T, Imai T, Yaegaki H, Haji T, Matsuta N, Yamaguchi M, Hayashi T (2001) Characterization of morphological traits based on a genetic linkage map in peach. Breeding Sci 51:271–278

    Article  CAS  Google Scholar 

  • Yang XY, Wang Y, Jiang WJ, Liu XL, Zhang XM, Yu HJ, Huang SW, Liu GQ (2013) Characterization and expression profiling of cucumber kinesin genes during early fruit development: revealing the roles of kinesins in exponential cell production and enlargement in cucumber fruit. J Exp Bot 64:4541–4557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang GR, Sebolt AM, Sooriyapathirana SS, Wang DH, Bink MC, Olmstead JW, Iezzoni AF (2010) Fruit size QTL analysis of an F1 population derived from a cross between a domesticated sweet cherry cultivar and a wild forest sweet cherry. Tree Genet Genomes 6:25–36

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Key Technology R&D Program of the Ministry of Science and Technology of China (2013BAD01B04-19) and the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2015-ZFRI-01).

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Correspondence to Lirong Wang.

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Cao, K., Zhao, P., Zhu, G. et al. Expansin genes are candidate markers for the control of fruit weight in peach. Euphytica 210, 441–449 (2016). https://doi.org/10.1007/s10681-016-1711-5

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