Abstract
To identify genes involved in the expression of a trait using the candidate gene (CG) approach, the genome positions of the maximum number of genes which potentially cause the observed phenotypic variability needs to be known. This position is compared with that of major genes or quantitative trait loci (QTL) for this character, with the co-location of the CG and major gene or QTL indicating a possible cause and effect relationship. In the present study we selected 273 sequences from expressed sequence tag collections, corresponding to CGs from metabolic pathways affecting fruit growth and maturity, texture, sugar and organic acid content, aroma and color, and mapped them in the Prunus reference map (T × E) based on an interspecific almond × peach F2 population. We used the bin-mapping approach, where only eight plants, six of the T × E progeny plus one of the parents and the F1 hybrid, are used to determine the position of a marker. This strategy was very efficient, with 206 CGs mapped, based mainly on the segregation of one or more single-nucleotide polymorphisms. These CGs were located throughout the Prunus genome and are a resource for genetic analysis in stone fruit (peach, plum, apricot and cherry) and almond. Co-locations between CGs and major genes or QTL responsible for natural variability of fruit quality characters in Prunus were identified using the available information on their positions.
Similar content being viewed by others
References
Abbott AG, Arús P, Scorza R (2008) Genetic engineering and genomics. In: Layne DR, Bassi D (eds) The peach: botany, production and uses. CABI, Cambridge, USA, pp 85–105
Arús P, Yamamoto T, Dirlewanger E, Abbott AG (2005) Synteny in the rosaceae. In: Janick J (ed) Plant breeding reviews. Wiley, USA, pp 175–211
Bassi D, Monet R (2008) Botany and taxonomy. In: Layne DR, Bassi D (eds) The peach: botany, production, and uses. CABI, Cambridge, USA, pp 1–36
Boss PK, Davies C, Robinson SP (1996a) Anthocyanin composition and anthocyanin pathway gene expression in grapevine sports differing in berry skin colour. Aust J Grape Wine Res 2:163–170
Boss PK, Davies C, Robinson SP (1996b) Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Mol Biol 32:565–569
Buddharak P, Chundet R (2009) Isolation and characterization of flavonoid 3′ hydroxylase (F3′H) gene and genetic transformation in butterfly pea (Clitoria ternatea Linn.) via Agrobacterium tumefasciens. Acta Hort 836:247–253
Cabrera A, Kozik A, Howad W, Arus P, Iezzoni A, Knaap E (2009) Development and bin mapping of a rosaceae conserved ortholog set (COS) of markers. BMC Genomics 10:562
Callesen O (2009) ISAFRUIT: the total chain approach. J Hort Sci Biotech ISAFRUIT Supplement:1
Chagné D, Gasic K, Crowhurst RN, Han Y, Bassett HC, Bowatte DR, Lawrence TJ, Rikkerink EHA, Gardiner SE, Korban SS (2008) Development of a set of SNP markers present in expressed genes of the apple. Genomics 92:353–358
Ching A, Caldwell K, Jung M, Dolan M, Smith O, Tingey S, Morgante M, Rafalski A (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3:19
Costa F, Van de Weg W, Stella S, Dondini L, Pratesi D, Musacchi S, Sansavini S (2008) Map position and functional allelic diversity of Md-Exp7, a new putative expansin gene associated with fruit softening in apple (Malus × domestica Borkh.) and pear (Pyrus communis). Tree Genet Genomes 4:575–586
Dirlewanger E, Graziano E, Joobeur T, Garriga-Caldere F, Cosson P, Howad W, Arus P (2004) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. Proc Natl Acad Sci USA 101:9891–9896
Dirlewanger E, Cosson P, Renaud C, Monet R, Poëssel JL, Moing A (2005) New detection of QTLs controlling major fruit quality components in peach. Acta Hort 713:65–72
Dirlewanger E, Cosson P, Boudehri K, Renaud C, Capdeville G, Tauzin Y, Laigret F, Moing A (2006a) 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 3:1–13
Dirlewanger E, Le Dantec L, Cosson P, Renaud C, Etienne C, Laigret F, Howad W, Arús P, Moing A, Rothan C, Carcia V (2006b) Peach fruit ESTs—annotation and mapping. Acta Hort 713:151–160
Etienne C, Rothan C, Moing A, Plomion C, Bodenes 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
Feltus FA, Singh HP, Lohithaswa HC, Schulze SR, Silva TD, Paterson AH (2006) A Comparative genomics strategy for targeted discovery of single-nucleotide polymorphisms and conserved-noncoding sequences in orphan crops. Plant Physiol 140:1183–1191
Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826
Granot D (2008) Putting plant hexokinases in their proper place. Phytochemistry 69:2649–2654
Grimplet J, Romieu C, Audergon J-M, Marty I, Albagnac G, Lambert P, Bouchet J-P, Terrier N (2005) Transcriptomic study of apricot fruit (Prunus armeniaca) ripening among 13006 expressed sequence tags. Physiol Plantarum 125:281–292
Howad W, Yamamoto T, Dirlewanger E, Testolin R, Cosson P, Cipriani G, Monforte AJ, Georgi L, Abbott AG, Arus P (2005) Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305–1309
Joobeur T, Viruel MA, de Vicente MC, Jáuregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Messeguer R, Batlle I, Quarta R, Dirlewanger E, Arús P (1998) Construction of a saturated linkage map for Prunus using an almond × peach F2 progeny. Theor Appl Genet 97:1034–1041
Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. Plant J 37:104–114
Lalli DA, Decroocq V, Blenda AV, Schurdi-Levraud V, Garay L, Le Gall O, Damsteegt V, Reighard GL, Abbott AG (2005) Identification and mapping of resistance gene analogs (RGAs) in Prunus: a resistance map for Prunus. Theor Appl Genet 111:1504–1513
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181
Larsen ES, Alfenito MR, Briggs WR, Walbot V (2003) A carnation anthocyanin mutant is complemented by the glutathione S-transferases encoded by maize Bz2 and petunia An9. Plant Cell Rep 21:900–904
Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429
Lester DR, Sherman WB, Atwell BJ (1996) Endopolygalacturonase and the melting flesh (M) locus in Peach. J Am Soc Hort Sci 121:231–235
Masoudi-Nejad A, Goto S, Endo TR, Kanehisa M (2007) KEGG bioinformatics resource for plant genomics research. Plant Bioinform 437–458
Nishitani C, Kimura T, Ueda E, Howad W, Arús P, Yamamoto T (2007) Tri-/hexanucleotide microsatellite markers in peach derived from enriched genomic libraries and their application in Rosaceae. Breed Sci 57:289–296
Ogundiwin E, Peace C, Gradziel T, Dandekar AM, Bliss F, Crisosto C (2007) Molecular genetic dissection of chilling injury in peach fruit. Acta Hort 738:633–638
Ogundiwin E, Peace C, Nicolet C, Rashbrook V, Gradziel T, Bliss F, Parfitt D, Crisosto C (2008) Leucoanthocyanidin dioxygenase gene (PpLDOX): a potential functional marker for cold storage browning in peach. Tree Genet Genomes 4:543–554
Ogundiwin E, Peace C, Gradziel T, Parfitt D, Bliss F, Crisosto C (2009) A fruit quality gene map of Prunus. BMC Genomics 10:587
Peace CP, Crisosto CH, Gradziel TM (2005) Endopolygalacturonase: a candidate gene for freestone and melting flesh in peach. Mol Breed 16:21–31
Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291
Quilot B, Wu BH, Kervella J, Genard 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
Remay A, Lalanne D, Thouroude T, Le Couviour F, Hibrand-Saint Oyant L, Foucher F (2009) A survey of flowering genes reveals the role of gibberellins in floral control in rose. Theor Appl Genet 119:767–781
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
Sánchez-Pérez R, Howad W, Dicenta F, Arús P, Martínez-Gómez P (2007) Mapping major genes and quantitative trait loci controlling agronomic traits in almond. Plant Breed 126:310–318
Sargent D, Marchese A, Simpson D, Howad W, Fernández-Fernández F, Monfort A, Arús P, Evans K, Tobutt K (2009) Development of “universal” gene-specific markers from Malus spp. cDNA sequences, their mapping and use in synteny studies within Rosaceae. Tree Genet Genomes 5:133–145
Sosinski B, Shulaev V, Dhingra A, Kalyanaraman A, Bumgarner R, Rokhsar D, Verde I, Velasco R, Abbott AG (2009) Rosaceaous genome sequencing: perspectives and progress. In: Folta KM, Gardiner SE (eds) Genetics and genomics of rosaceae. Springer, New York, pp 601–615
Stevens R, Buret M, Duffe P, Garchery C, Baldet P, Rothan C, Causse M (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 143:1943–1953
Suliman-Pollatschek S, Kashkush K, Shats H, Hillel J, Lavi U (2002) Generation and mapping of AFLP, SSRs and SNPs in Lycopersicon esculentum. Cell Mol Biol Lett 7:583–597
Sun J, Loboda T, Sung S-JS, Black CC Jr (1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiol 98:1163–1169
Tanaka Y, Brugliera F (2006) Flower colour. In: Ainsworth C (ed) Flowering and its manipulation. Wiley-Blackwell, Oxford, pp 201–239
Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781
Varshney R, Beier U, Khlestkina E, Kota R, Korzun V, Graner A, Börner A (2007) Single nucleotide polymorphisms in rye (Secale cereale L.): discovery, frequency, and applications for genome mapping and diversity studies. Theor Appl Genet 114:1105–1116
Viruel MA, Messeguer R, Vicente MC, Garcia-Mas J, Puigdomènech P, Vargas F, Arús P (1995) A linkage map with RFLP and isozyme markers for almond. Theor Appl Genet 91:964–971
Wu S-B, Wirthensohn M, Hunt P, Gibson J, Sedgley M (2008) High resolution melting analysis of almond SNPs derived from ESTs. Theor Appl Genet 118:1–14
Yamamoto T, Yamaguchi M, Hayashi T (2005) An integrated genetic linkage map of peach by SSR, STS, AFLP and RAPD. J Jpn Soc Hort Sci 74:204–213
Yang W, Bai X, Kabelka E, Eaton C, Kamoun S, van der Knaap E, David F (2004) Discovery of single nucleotide polymorphisms in Lycopersicon esculentum by computer aided analysis of expressed sequence tags. Mol Breed 14:21–34
Yang L, Jin G, Zhao X, Zheng Y, Xu Z, Wu W (2007) PIP: a database of potential intron polymorphism markers. Bioinformatics 23:2174–2177
Zrenner R, Salanoubat M, Willmitzer L, Sonnewald U (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J 7:97–107
Acknowledgments
This study was supported in part by the ISAFRUIT Integrated Project. The ISAFRUIT Project is funded by the European Commission under Thematic Priority 5 – Food Quality and Safety of the 6th Framework Programme of RTD (Contract No. FP6-FOOD-CT-2006-016279). Disclaimer: Opinions expressed in this publication may not be regarded as stating an official position of the European Commission.
Funding from the Zhejiang University group comes from the China Natural Science Foundation (30771496). The group of IRTA is a member of the CONSOLIDER Center for Basic Genomics and Agro-food Orientation (CSD2007-00036) funded by the Spanish Ministry of Science and Innovation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Eudald Illa and Iban Eduardo contributed equally to this paper.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11032_2010_9518_MOESM1_ESM.xls
Supplementary Table 1: Features of 273 candidate genes involved in fruit quality and their primer sequences. (XLS 2226 kb)
Rights and permissions
About this article
Cite this article
Illa, E., Eduardo, I., Audergon, J.M. et al. Saturating the Prunus (stone fruits) genome with candidate genes for fruit quality. Mol Breeding 28, 667–682 (2011). https://doi.org/10.1007/s11032-010-9518-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-010-9518-x