Distinguishing two genetic factors that control yellow fruit color in tomato

Abstract

Carotenoids are tetraterpenes (40-carbon isoprenoids) derived from the five-carbon isoprene units, isopentenyl diphosphate (IDP) and its isomer dimethylallyl diphosphate (DMADP). These molecules are the major determinants of fruit pigmentation in many plant species, including tomato. The IDP isomerase (IDI) catalyzes the isomerization of IDP to DMADP. Phytoene synthase (PSY) catalyzes the dimerization of two diterpenes from geranylgeranyl pyrophosphate to phytoene, which is the rate-limiting step in carotenoid biosynthesis. Mutations in the tomato PSY1, yellow flesh, are widely used for breeding yellow tomatoes. We report a series of allelic variations in yellow flesh, and in the newly identified apricot, which has yellow fruit as a result of a mutation in IDI1. In HPLC analysis, both the cultivars showed yellow ripe fruits that lacked carotenoids. However, unlike wild type and yellow flesh, apricot mutants had reduced carotenoid levels in flowers. The allelic variations in yellow flesh were determined to have a deletion in the promoter region and a nonsense mutation in the PSY1 gene, whereas apricot contained a ‘T’ insertion that resulted in premature termination codon in the IDI1 gene. DNA markers to identify allelic variations in two yellow flesh and three apricot mutant lines were developed. These markers and germplasms would be useful for breeding yellow tomatoes.

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References

  1. Aflitos S, Schijlen E, Jong H, Ridder D, Smit S, Finkers R, Wang J, Zhang G, Li N, Mao L, Bakker F, Dirks R, Breit T, Gravendeel B, Huits H, Struss D, Swanson-Wagner R, Leeuwen H, Ham RCHJ, Fito L, Guignier L, Sevilla M, Ellul P, Ganko E, Kapur A, Reclus E, Geus B, Geest H, BtL Hekkert, Haarst J, Smits L, Koops A, Sanchez-Perez G, Heusden AW, Visser R, Quan Z, Min J, Liao L, Wang X, Wang G, Yue Z, Yang X, Xu N, Schranz E, Smets E, Vos R, Rauwerda J, Ursem R, Schuit C, Kerns M, Berg J, Vriezen W, Janssen A, Datema E, Jahrman T, Moquet F, Bonnet J, Peters S (2014) Exploring genetic variation in the tomato (Solanum section Lycopersicon) clade by whole-genome sequencing. Plant J 80:136–148

    Article  PubMed  Google Scholar 

  2. Ballester A-R, Molthoff J, de Vos R, BtL Hekkert, Orzaez D, Fernández-Moreno J-P, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Barry CS, McQuinn RP, Chung MY, Besuden A, Giovannoni JJ (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147:179–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Berthelot K, Estevez Y, Deffieux A, Peruch F (2012) Isopentenyl diphosphate isomerase: a checkpoint to isoprenoid biosynthesis. Biochimie 94:1621–1634

    Article  CAS  PubMed  Google Scholar 

  5. Botella-Pavía P, Besumbes Ó, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188–199

    Article  CAS  PubMed  Google Scholar 

  6. Cheng X, Zhang D, Cheng Z, Keller B, Ling H-Q (2009) A new family of Ty1-copia-like retrotransposons originated in the tomato genome by a recent horizontal transfer event. Genetics 181:1183–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1:581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Durbecq V, Sainz G, Oudjama Y, Clantin B, Bompard-Gilles C, Tricot C, Caillet J, Stalon V, Droogmans L, Villeret V (2001) Crystal structure of isopentenyl diphosphate: dimethylallyl diphosphate isomerase. EMBO J 20:1530–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Egea I, Barsan C, Bian W, Purgatto E, Latche A, Chervin C, Bouzayen M, Pech JC (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51:1601–1611

    Article  CAS  PubMed  Google Scholar 

  10. Eisenreich W, Rohdich F, Bacher A (2001) Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci 6:78–84

    Article  CAS  PubMed  Google Scholar 

  11. Enfissi EMA, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3:17–27

    Article  CAS  PubMed  Google Scholar 

  12. Fantini E, Falcone G, Frusciante S, Giliberto L, Giuliano G (2013) Dissection of tomato lycopene biosynthesis through virus-induced gene silencing. Plant Physiol 163:986–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265

    Article  CAS  PubMed  Google Scholar 

  14. Fraser PD, Enfissi EM, Halket JM, Truesdale MR, Yu D, Gerrish C, Bramley PM (2007) Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19:3194–3211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. Gady AL, Vriezen WH, Van de Wal MH, Huang P, Bovy AG, Visser RG, Bachem CW (2012) Induced point mutations in the phytoene synthase 1 gene cause differences in carotenoid content during tomato fruit ripening. Mol Breed 29:801–812

    Article  CAS  PubMed  Google Scholar 

  17. Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J (2006) A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18:1947–1960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Giorio G, Stigliani AL, D’Ambrosio C (2008) Phytoene synthase genes in tomato (Solanum lycopersicum L.)—new data on the structures, the deduced amino acid sequences and the expression patterns. FEBS J 275:527–535

    Article  CAS  PubMed  Google Scholar 

  19. Guil-Guerrero JL, Rebolloso-Fuentes MM (2009) Nutrient composition and antioxidant activity of eight tomato (Lycopersicon esculentum) varieties. J Food Compost Anal 22:123–129

    Article  CAS  Google Scholar 

  20. Horton P, Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56:365–373

    Article  CAS  Google Scholar 

  21. Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 14:333–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kachanovsky DE, Filler S, Isaacson T, 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

    Article  PubMed  Google Scholar 

  23. Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70:191–204

    Article  CAS  PubMed  Google Scholar 

  24. Liu L, Shao Z, Zhang M, Wang Q (2015) Regulation of carotenoid metabolism in tomato. Mol Plant 8:28–39

    Article  CAS  PubMed  Google Scholar 

  25. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:948

    Article  CAS  PubMed  Google Scholar 

  26. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res 37:D205–D210

    Article  CAS  PubMed  Google Scholar 

  27. McQuinn RP, Giovannoni JJ, Pogson BJ (2015) More than meets the eye: from carotenoid biosynthesis, to new insights into apocarotenoid signaling. Curr Opin Plant Biol 27:172–179

    Article  CAS  PubMed  Google Scholar 

  28. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ohmiya A (2011) Diversity of carotenoid composition in flower petals. Jpn Agric Res Q 45:163–171

    Article  CAS  Google Scholar 

  30. Phillips MA, D’Auria JC, Gershenzon J, Pichersky E (2008) The Arabidopsis thaliana type I isopentenyl diphosphate isomerases are targeted to multiple subcellular compartments and have overlapping functions in isoprenoid biosynthesis. Plant Cell 20:677–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pulido P, Perello C, Rodriguez-Concepcion M (2012) New insights into plant isoprenoid metabolism. Mol Plant 5:964–967

    Article  CAS  PubMed  Google Scholar 

  32. Rodriguez-Concepcion M (2010) Supply of precursors for carotenoid biosynthesis in plants. Arch Biochem Biophys 504:118–122

    Article  CAS  PubMed  Google Scholar 

  33. Ronen G, Cohen M, Zamir D, Hirschberg Z (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J 17:341–351

    Article  CAS  PubMed  Google Scholar 

  34. Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107

    Article  CAS  PubMed  Google Scholar 

  35. Shirasawa K, Hirakawa H (2013) DNA marker applications to molecular genetics and genomics in tomato. Breed Sci 63:21–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Aspects Med 24:345–351

    Article  CAS  PubMed  Google Scholar 

  37. Sun J, Zhang Y-Y, Liu H, Zou Z, Zhang C-J, Zhang X-H, Li H-X, Ye Z-B (2010) A novel cytoplasmic isopentenyl diphosphate isomerase gene from tomato (Solanum lycopersicum): cloning, expression, and color complementation. Plant Mol Biol Rep 28:473–480

    Article  CAS  Google Scholar 

  38. The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  CAS  Google Scholar 

  39. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-Box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296:343–346

    Article  CAS  PubMed  Google Scholar 

  40. Yoo HJ, Park WJ, Lee G-M, Oh C-S, Yeam I, Won D-C, Kim CK, Lee JM (2017) Inferring the genetic determinants of fruit colors in tomato by carotenoid profiling. Molecules 22:764

    Article  CAS  PubMed Central  Google Scholar 

  41. Yuan D, Chen J, Shen H, Yang W (2008) Genetics of flesh color and nucleotide sequence analysis of phytoene synthase gene 1 in a yellow-fruited tomato accession PI114490. Sci Hortic 118:20–24

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Research Foundation of Korea (2018R1A2B6002620) and the Golden Seed Project (Center for Horticultural Seed Development) (213007-05-2-SBF20), the Ministry of Agriculture, Food and Rural Affairs, Republic of Korea.

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Correspondence to Je Min Lee.

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Shin, J.H., Yoo, H.J., Yeam, I. et al. Distinguishing two genetic factors that control yellow fruit color in tomato. Hortic. Environ. Biotechnol. 60, 59–67 (2019). https://doi.org/10.1007/s13580-018-0093-0

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Keywords

  • Tomato
  • Carotenoid
  • Fruit color
  • Phytoene synthase
  • Isopentenyl diphosphate isomerase