Abstract
Peach flesh color is a monogenic trait with the white phenotype being dominant over the yellow; its expression has been reported to be determined by a carotenoid degradative enzyme. In the present study, a carotenoid cleavage dioxygenase (ccd4) gene was analyzed to test whether it can be responsible for the flesh color determinism. The analysis was conducted on chimeric mutants with white and yellow sectors of the fruit mesocarp; it was then extended to a pool of cultivars and a segregating F1 population. A ccd4 functional allele is consistently associated with the ancestral white flesh color; on the other hand, the yellow phenotype originated from at least three independent mutations disrupting ccd4 function, thus preventing carotenoid degradation. In addition, retro-mutations recovering ccd4 function and re-establishing the ancestral white flesh color were detected. Our results show that ccd4 is the gene controlling flesh color in peach; its expression results in the degradation of carotenoids in white-fleshed genotypes, while the yellow color arises as a consequence of its inactivation.
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References
Bian W, Barsan C, Egea I, Purgatto E, Chervin C, Zouine M, Latché A, Bouzayen M, Pech J-C (2011) Metabolic and molecular events occurring during chromoplast biogenesis. J Bot 2011:1–13. doi:10.1155/2011/289859
Brandi F, Bar E, Mourgues F, Horváth G, Turcsi E, Giuliano G, Liverani A, Tartarini S, Lewinsohn E, Rosati C (2011) Study of “Redhaven” peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol 11:24. doi:10.1186/1471-2229-11-24
Brendel V, Xing L, Zhu W (2004) Gene structure prediction from consensus spliced alignment of multiple ESTs matching the same genomic locus. Bioinform (Oxford, England) 20:1157–1169. doi:10.1093/bioinformatics/bth058
Brody JR, Kern SE (2004) Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques 36:214–216
Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP (2007) Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 8:762–775. doi:10.1038/nrg2193
Connors CH (1920) Some notes on the inheritance of unit characters in the peach. P Am Soc Hortic Sci 16:24–36
Decroocq V, Favé MG, Hagen L, Bordenave L, Decroocq S (2003) Development and transferability of apricot and grape EST microsatellite markers across taxa. Theor Appl Genet 106:912–922. doi:10.1007/s00122-002-1158-z
Dermen H, Stewart R (1973) Ontogenetic study of floral organs of peach (Prunus persica) utilizing cytochimeral plants. Am J Bot 60:283–291
Diretto G, Welsch R, Tavazza R, Mourgues F, Pizzichini D, Beyer P, Giuliano G (2007) Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol 7:11. doi:10.1186/1471-2229-7-11
Faust M, Timon B (1995) Origin and dissemination of peach. In: Jules J (ed) Hortic Rev. Wiley, New York, pp 331–379
Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22:589–602. doi:10.1007/BF00047400
Gómez-Gómez L, Rubio-Moraga Á, Ahrazem O (2010) Understanding carotenoid metabolism in saffron stigmas: unravelling aroma and colour formation. Func Plant Sci Biotech 4:56–63
Gorbunova V, Levy A (1999) How plants make ends meet: DNA double-strand break repair. Trends Plant Sci 4:263–269
Hayden MJ, Tabone T, Mather DE (2009) Development and assessment of simple PCR markers for SNP genotyping in barley. Theor Appl Genet 119:939–951. doi:10.1007/s00122-009-1101-7
Hormaza JI, Dollo L, Polito VS (1994) Identification of a RAPD marker linked to sex determination in Pistacia vera using bulked segregant analysis. Theor Appl Genet 89:9–13. doi:10.1007/BF00226975
Huang F-CC, Molnár P, Schwab W, Molnar P (2009) Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J Exp Bot 60:3011–3022. doi:10.1093/jxb/erp137
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59. doi:10.1146/annurev-genet-110410-132507
Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinforma 7:474
Kuzin AB, Lyubomirskaya NV, Khudaibergenova BM, Ilyin YV, Kim AI (1994) Precise excision of the retrotransposon gypsy from the forked and cut loci in a genetically unstable D. melanogaster strain. Nucleic Acids Res 22:4641–4645
Li J, Dudas B, Webster MA, Cook HE, Davies BH, Gilmartin PM (2010) Hose in Hose, an S locus-linked mutant of Primula vulgaris, is caused by an unstable mutation at the Globosa locus. Proc Natl Acad Sci U S A 107:5664–5668. doi:10.1073/pnas.0910955107
Li Y-C, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007. doi:10.1093/molbev/msh073
Moehs CP, Tian L, Osteryoung KW, Dellapenna D (2001) Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Mol Biol 45:281–293. doi:10.1023/A:1006417009203
Nefedova LN, Ljubomirskaya NV, Ilyin YV, Kim AI (2006) Precise excision of long terminal repeats of the gypsy (mdg4) retrotransposon of Drosophila melanogaster detected in Escherichia coli cells is explained by its integrase function. Russ J Genet 42:1398–1404. doi:10.1134/S1022795406120064
Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol 142:1193–1201. doi:10.1104/pp. 106.087130
Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. doi:10.1038/nmeth.1701
Rubio A, Rambla JL, Santaella M, Gómez MD, Orzaez D, Granell A, Gómez-Gómez L (2008) Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem 283:24816–24825. doi:10.1074/jbc.M804000200
Sanzol J (2009) Pistil-function breakdown in a new S-allele of European pear, S21*, confers self-compatibility. Plant Cell Rep 28:457–467. doi:10.1007/s00299-008-0645-3
Shewmaker CK, Sheehy JA, Daley M, Colburn S, Ke DY (1999) Seed-specific overexpression of phytoene synthase: increase in carotenoids and other metabolic effects. Plant J 20:401–412. doi:10.1046/j.1365-313x.1999.00611.x
Sosinski B, Gannavarapu M, Hager LD, Beck LE, King GJ, Ryder CD, Rajapakse S, Baird WV, Ballard RE, Abbott AG (2000) Characterization of microsatellite markers in peach [Prunus persica (L.) Batsch]. Theor Appl Genet 101:421–428. doi:10.1007/s001220051499
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:1530–1534. doi:10.1093/molbev/msr121
Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0, software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands
Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692. doi:10.1039/c0np00036a
Wang ML, Barkley NA, Jenkins TM (2009) Microsatellite markers in plants and insects. Part I: applications of biotechnology. Genes Genomes Genomics 3:54–67
Williamson JD, Peace CP, Bliss FA, Garner DT, Crisosto CH (2006) Evidence for a single locus controlling flesh color, senescent leaf color, and hypanthium color in peach. J Am Soc Hortic Sci 131:256–260
Yoshioka S, Aida R, Yamamizo C, Shibata M, Ohmiya A (2011) The carotenoid cleavage dioxygenase 4 (CmCCD4a) gene family encodes a key regulator of petal color mutation in chrysanthemum. Euphytica 184:377–387. doi:10.1007/s10681-011-0602-z
Ytterberg A, Peltier J, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984–997. doi:10.1104/pp. 105.076083.984
Zamboni A, Pierantoni L, De Franceschi P (2008) Total RNA extraction from strawberry tree (Arbutus unedo) and several other woody-plants. iForest - Biogeosciences and Forestry 1:122–125. doi:10.3832/ifor0465-0010122
Zhou X, Van Eck J, Li L (2008) Use of the cauliflower Or gene for improving crop nutritional quality. Biotechnol Annu Rev 14:171–190. doi:10.1016/S1387-2656(08)00006-9
Acknowledgments
The International Peach Genome Initiative (IPGI) is acknowledged for early online access to the draft genome sequence. Authors are grateful to Dr. Xenija Gasic from the University of Clemson (SC) and to the National Clonal Germplasm Repository for Fruit and Nut Crops, Davis (CA), for kindly providing leaf samples of the 10 US breeding founders analyzed in this study. This research was funded by the Project ALISAL from the Italian Ministry of Agriculture and Forestry. MA’s PhD fellowship was funded by CRA-FRF (Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Unità di Ricerca per la Frutticoltura di Forlì).
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Adami, M., De Franceschi, P., Brandi, F. et al. Identifying a Carotenoid Cleavage Dioxygenase (ccd4) Gene Controlling Yellow/White Fruit Flesh Color of Peach. Plant Mol Biol Rep 31, 1166–1175 (2013). https://doi.org/10.1007/s11105-013-0628-6
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DOI: https://doi.org/10.1007/s11105-013-0628-6