Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach

Plant Journal

Volumn 76, Issue 2, 2013, Pages 175-187

  Falchi, Rachele ^a   Vendramin, Elisa ^b   Zanon, Laura ^a   Scalabrin, Simone ^c   Cipriani, Guido ^a,b   Verde, Ignazio ^b   Vizzotto, Giannina ^a   Morgante, Michele ^a,c  

^a UNIVERSITY OF UDINE   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c Istituto di Genomica Applicata (IGA)   (Italy)

Author keywords

allelic variants; carotenoid cleavage dioxygenase; nonsense mediated mRNA decay; Prunus persica L. Batsch; somatic revertants; transposable element

Indexed keywords

ALLELIC VARIANTS; DIOXYGENASES; NONSENSE-MEDIATED MRNA DECAY; PRUNUS PERSICA; SOMATIC REVERTANTS; TRANSPOSABLE ELEMENTS;

COLOR; GENES; PIGMENTS; PLANTS (BOTANY);

FRUITS;

PRUNUS PERSICA;

CAROTENOID CLEAVAGE DIOXYGENASE; DIOXYGENASE;

ALLELE; ALLELIC VARIANTS; AMINO ACID SEQUENCE; ARTICLE; COLOR; ENZYMOLOGY; FRUIT; GENETICS; GENOTYPE; MOLECULAR GENETICS; MUTATION; NONSENSE-MEDIATED MRNA DECAY; PHENOTYPE; PHYLOGENY; PLANT GENE; PRUNUS; PRUNUS PERSICA L. BATSCH; SOMATIC REVERTANTS; TRANSPOSON;

ALLELIC VARIANTS; CAROTENOID CLEAVAGE DIOXYGENASE; NONSENSE-MEDIATED MRNA DECAY; PRUNUS PERSICA L. BATSCH; SOMATIC REVERTANTS; TRANSPOSABLE ELEMENT;

ALLELES; AMINO ACID SEQUENCE; COLOR; DIOXYGENASES; FRUIT; GENES, PLANT; GENOTYPE; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHYLOGENY; PRUNUS;

EID: 84885320323     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12283     Document Type: Article

References (58)

1. Ampomah-Dwamena, C., Dejnoprat, S., Lewis, D., Sutherland, P., Volz, R.K., and, Allan, A.C., (2012) Metabolic and gene expression analysis of apple (Malus × domestica) carotenogenesis. J. Exp. Bot. 63, 4497-4511.
2. Andersson, L.S., Larhammar, M., Memic, F., et al. (2012) Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature, 488, 642-646.
3. Auldridge, M.E., Block, A., Vogel, J.T., Dabney-Smith, C., Mila, I., Bouzayen, M., Magallanes-Lundback, M., DellaPenna, D., McCarty, D.R., and, Klee, H.J., (2006) Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J. 45, 982-993.
4. Bailey, J.S., and, French, A.P., (1949) The Inheritance of Certain Fruit and Foliage Characters in the Peach. Amherst, MA: University of Massachusetts Press.
5. Ballester, A.R., Molthoff, J., de Vos, R., et al. (2010) Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol. 152, 71-84.
6. Blas, A.L., Ming, R., Liu, Z., Veatch, O.J., Paull, R.E., Moore, P.H., and, Yu, Q., (2010) Cloning of the papaya chromoplast-specific lycopene β-cyclase, CpCYC-b, controlling fruit flesh color reveals conserved microsynteny and a recombination hot spot. Plant Physiol. 152, 2013-2022.
7. Bliss, F.A., Arulsekar, S., Foolad, M.R., Becerra, V., Gillen, A.M., Warburton, M.L., Dandekar, A.M., Kocsisne, G.M., and, Mydin, K.K., (2002) An expanded genetic linkage map of Prunus based on an interspecific cross between almond and peach. Genome, 45, 520-529.
8. Bramley, P.M., (2002) Regulation of carotenoid formation during tomato fruit ripening and development. J. Exp. Bot. 53, 2107-2113.
9. Brand, A., Borovsky, Y., Meir, S., Rogachev, I., Aharoni, A., and, Paran, I., (2012) pc8.1, a major QTL for pigment content in pepper fruit, is associated with variation in plastid compartment size. Planta, 235, 579-588.
10. Brandi, F., Bar, E., Mourgues, F., Horváth, G., Turcsi, E., Giuliano, G., Liverani, A., Tartarini, S., Lewinsohn, E., and, 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.
11. Butelli, E., Licciardello, C., Zhang, Y., Liu, J., Mackay, S., Bailey, P., Reforgiato-Recupero, G., and, Martin, C., (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 24, 1242-1255.
12. Byrne, D., Raseira, M., Bassi, D., Piagnani, M., Gasic, K., Reighard, G., Moreno, M., and, Pérez, S., (2012) Peach. In Fruit Breeding (, Badenes, M.L., and, Byrne, D.H., eds). New York: Springer Verlag, pp. 505-569.
13. Campbell, R., Ducreux, L.J.M., Morris, W.L., Morris, J.A., Suttle, J.C., Ramsay, G., Bryan, G.J., Hedley, P.E., and, Taylor, M.A., (2010) The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato. Plant Physiol. 154, 656-664.
14. Cazzonelli, C.I., and, Pogson, B.J., (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 15, 266-274.
15. Connors, C.H., (1920) Some notes on the inheritance of unit characters in the peach. Proc. Am. Soc. Hortic. Sci. 16, 24-36.
16. Dermen, H., (1956) Histogenetic factors in color and fuzzless peach sports. J. Hered. 47, 64-76.
17. Falchi, R., Cipriani, G., Marrazzo, T., Nonis, A., Vizzotto, G., and, Ruperti, B., (2010) Identification and differential expression dynamics of peach small GTPases encoding genes during fruit development and ripening. J. Exp. Bot. 61, 2829-2842.
18. Fray, R.G., and, 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.
19. García-Limones, C., Schnäbele, K., Blanco-Portales, R., Luz Bellido, M., Caballero, J.L., Schwab, W., and, Muñoz-Blanco, J., (2008) Functional characterization of FaCCD1: a carotenoid cleavage dioxygenase from strawberry involved in lutein degradation during fruit ripening. J. Agric. Food Chem. 56, 9277-9285.
20. Gil, M.I., Tomás-Barberán, F.A., Hess-Pierce, B., and, Kader, A.A., (2002) Antioxidant capacities, phenolic compounds, carotenoids, and vitamin C contents of nectarine, peach, and plum cultivars from California. J. Agric. Food Chem. 50, 4976-4982.
21. Giuliano, G., Al-Babili, S., and, von Lintig, J., (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci. 8, 145-149.
22. Harjes, C.E., Rocheford, T.R., Bai, L., et al. (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science, 319, 330-333.
23. Havecker, E.R., Gao, X., and, Voytas, D.F., (2004) The diversity of LTR retrotransposons. Genome Biol. 5, 225.
24. van Hoof, A., and, Green, P.J., (2006) NMD in plants. In Nonsense-Mediated mRNA Decay. (, Maquat, L.E., ed). New York: Landes Bioscience, pp. 167-172.
25. Huang, X., Lu, G., Zhao, Q., Liu, X., and, Han, B., (2008) Genome-wide analysis of transposon insertion polymorphisms reveals intraspecific variation in cultivated rice. Plant Physiol. 148, 25-40.
26. Huang, F.C., Molnár, P., and, Schwab, W., (2009) Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J. Exp. Bot. 60, 3011-3022.
27. Illa, E., Eduardo, I., Audergon, J., et al. (2011) Saturating the Prunus (stone fruits) genome with candidate genes for fruit quality. Mol. Breed. 28, 667-682.
28. Kachanovsky, D.E., Filler, S., Isaacson, T., and, Hirschberg, J., (2012) Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc. Natl Acad. Sci. USA 109, 19021-19026.
29. Kato, M., Matsumoto, H., Ikoma, Y., Okuda, H., and, Yano, M., (2006) The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit. J. Exp. Bot. 57, 2153-2164.
30. Kijima, T.E., and, Innan, H., (2010) On the estimation of the insertion time of LTR retrotransposable elements. Mol. Biol. Evol. 27, 896-904.
31. Kim, J.M., Vanguri, S., Boeke, J.D., Gabriel, A., and, Voytas, D.F., (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8, 464-478.
32. Kobayashi, S., Goto-Yamamoto, N., and, Hirochika, H., (2004) Retrotransposon-induced mutations in grape skin color. Science, 304, 982.
33. Kuzin, A., Lyubomirskaya, N., Khudaibergenova, B., Ilyin, Y., and, Kim, A., (1994) Precise excision of the retrotransposon gypsy from the forked and cut loci in a genetically unstable Drosophila melanogaster strain. Nucleic Acids Res. 22, 4641-4645.
34. Lewinsohn, E., Sitrit, Y., Bar, E., Azulay, Y., Ibdah, M., Meir, A., Yosef, E., Zamir, D., and, Tadmor, Y., (2005) Not just colors-carotenoid degradation as a link between pigmentation and aroma in tomato and watermelon fruit. Trends Food Sci. Technol. 16, 407-415.
35. Li, F., Vallabhaneni, R., Yu, J., Rocheford, T., and, Wurtzel, E.T., (2008) The maize phytoene synthase gene family: overlapping roles for carotenogenesis in endosperm, photomorphogenesis, and thermal stress tolerance. Plant Physiol. 147, 1334-1346.
36. Martinez-Garcia, P., Parfitt, D., Ogundiwin, E., Fass, J., Chan, H., Ahmad, R., Lurie, S., Dandekar, A., Gradziel, T., and, Crisosto, C., (2013) High density SNP mapping and QTL analysis for fruit quality characteristics in peach (Prunus persica L.). Tree Genet. Genomes 9, 19-36.
37. Mathieu, S., Terrier, N., Procureur, J., Bigey, F., and, Günata, Z., (2005) A carotenoid cleavage dioxygenase from Vitis vinifera L.: functional characterization and expression during grape berry development in relation to C13-norisoprenoid accumulation. J. Exp. Bot. 56, 2721-2731.
38. Moise, A.R., von Lintig, J., and, Palczewski, K., (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci. 10, 178-186.
39. Ohmiya, A., Kishimoto, S., Aida, R., Yoshioka, S., and, Sumitomo, K., (2006) Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in Chrysanthemum petals. Plant Physiol. 142, 1193-1201.
40. Palaisa, K.A., Morgante, M., Williams, M., and, Rafalski, A., (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell, 15, 1795-1806.
41. Parker, H.G., VonHoldt, B.M., Quignon, P., et al. (2009) An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science, 325, 995-998.
42. Pfaffl, M.W., (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
43. Rodriguez-Uribe, L., Guzman, I., Rajapakse, W., Richins, R.D., and, O'Connell, M.A., (2012) Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels. J. Exp. Bot. 63, 517-526.
44. Rodriguez-Villalon, A., Gas, E., and, Rodriguez-Concepcion, M., (2009) Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in dark-grown Arabidopsis seedlings. Plant J. 60, 424-435.
45. de la Rosa, L.A., Alvarez-Parrilla, E., and, Gonzalez-Aguilar, G.A., (2009) Fruit and Vegetable Phytochemicals: Chemistry, Nutritional Value and Stability. Ames, IA: John Wiley & Sons.
46. Rubio, A., Rambla, J.L., Santaella, M., Gómez, M.D., Orzaez, D., Granell, A., and, 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.
47. Salvi, S., Sponza, G., Morgante, M., et al. (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc. Natl Acad. Sci. USA 104, 11376-11381.
48. Shimazaki, M., Fujita, K., Kobayashi, H., and, Suzuki, S., (2011) Pink-colored grape berry is the result of short insertion in intron of color regulatory gene. PLoS ONE, 6, 8.
49. Tamura, K., Dudley, J., Nei, M., and, Kumar, S., (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
50. Vendramin, E., Dettori, M.T., Giovinazzi, J., Micali, S., Quarta, R., and, Verde, I., (2007) A set of EST-SSRs isolated from peach fruit transcriptome and their transportability across Prunus species. Mol. Ecol. Notes 7, 307-310.
51. Verde, I., Bassil, N., Scalabrin, S., et al. (2012) Development and evaluation of a 9K SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PLoS ONE 7, e35668.
52. Verde, I., Abbott, A.G., Scalabrin, S., et al. (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.
53. Vezzi, F., Del Fabbro, C., Tomescu, A.I., and, Policriti, A., (2012) rNA: a fast and accurate short reads numerical aligner. Bioinformatics, 28, 123-124.
54. Vizzotto, M., Cisneros-Zevallos, L., Byrne, D.H., Ramming, D.W., and, Okie, W.R., (2007) Large variation found in the phytochemical and antioxidant activity of peach and plum germplasm. J. Am. Soc. Hortic. Sci., 132, 334-340.
55. Walker, A.R., Lee, E., and, Robinson, S.P., (2006) Two new grape cultivars, bud sports of Cabernet Sauvignon bearing pale-coloured berries, are the result of deletion of two regulatory genes of the berry colour locus. Plant Mol. Biol. 62, 623-635.
56. Williamson, J., Peace, C., Bliss, F., Garner, D., and, Crisosto, C., (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.
57. Yeager, A.F., and, Meader, E.M., (1956) A flesh-color chimera in the peach. J. Hered. 47, 77-78.
58. Zhang, H.-B., Zhao, X., Ding, X., Paterson, A.H., and, Wing, R.A., (1995) Preparation of megabase-size DNA from plant nuclei. Plant J. 7, 175-184.