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Genomic Aspects of Melon Fruit Quality

  • Amit Gur
  • Itay Gonda
  • Vitaly Portnoy
  • Galil Tzuri
  • Noam Chayut
  • Shahar Cohen
  • Yelena Yeselson
  • Ayala Meir
  • Einat Bar
  • Rachel Davidovitz-Rikanati
  • Uzi Saar
  • Harry S. Paris
  • Joseph Burger
  • Yaakov Tadmor
  • Efraim Lewinsohn
  • Arthur A. Schaffer
  • Nurit KatzirEmail author
Chapter
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 20)

Abstract

Fruit quality in melon (Cucumis melo) and in other cucurbit species is primarily determined by sweetness, acidity, aroma, color and shelf-life. During ripening, the mesocarp (fruit flesh), the consumed tissue, generally softens due to degradation of cell walls, and accumulates soluble sugars, organic acids, volatiles and additional secondary metabolites. Flesh and rind color undergo developmental changes, the most noticeable of which are changes in pigmentation. This chapter reviews the current knowledge of genes that regulate, or participate in, the major metabolic pathways affecting sugar and acid metabolism (sweetness), volatile organic compounds (aroma) and pigments (color) of the melon fruit.

Keywords

Transcriptome Sugar metabolism Carotenoids Flavonoids Aroma Volatile organic compounds (VOCs) 

References

  1. Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Domínguez E, Wang Z, De Vos RCH, Jetter R, Schreiber L, Heredia A, Rogachev I, Aharoni A. Fruit-surface flavonoid accumulation in tomato is controlled by a SlMYB12-regulated transcriptional network. PLoS Genet. 2009;5:e1000777.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Aggelis A, John I, Karvouni Z, Grierson D. Characterization of two cDNA clones for mRNAs expressed during ripening of melon (Cucumis melo L.) fruits. Plant Mol Biol. 1997;33:313–22.PubMedCrossRefGoogle Scholar
  3. Araus JL, Cairns JE. Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci. 2014;19:52–61.PubMedCrossRefGoogle Scholar
  4. Argyris JM, Pujol M, Martín-Hernández AM, Garcia-Mas J. Combined use of genetic and genomics resources to understand virus resistance and fruit quality traits in melon. Physiol Plant. 2015;155:4–11.PubMedCrossRefGoogle Scholar
  5. Ayub R, Guis M, Amor MB, Gillot L, Roustan J-P, Latche A, Bouzayen M, Pech J-C. Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nat Biotechnol. 1996;14:862–6.PubMedCrossRefGoogle Scholar
  6. Balague C, Watson CF, Turner AJ, Rouge P, Picton S, Pech JC, Grierson D. Isolation of a ripening and wound-induced cDNA from Cucumis melo L. encoding a protein with homology to the ethylene-forming enzyme. Eur J Biochem. 1993;212:27–34.PubMedCrossRefGoogle Scholar
  7. Ballester A, Molthoff J, De Vos R, Hekkert B, Orzaez D, Fernandez-Moreno J, Tripodi P, Grandillo S, Martin C, Heldens J, Ykema M, Granell A, Bovy A. Biochemical and molecular analysis of pink tomatoes: deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiol. 2009;152:71–84.PubMedCrossRefGoogle Scholar
  8. Bauchot AD, Mottram DS, Dodson AT, John P. Effect of aminocyclopropane-1-carboxylic acid oxidase antisense gene on the formation of volatile esters in cantaloupe Charentais melon (cv. Védrandais). J Agric Food Chem. 1998;46:4787–92.CrossRefGoogle Scholar
  9. Beaulieu JC, Grimm CC. Identification of volatile compounds in cantaloupe at various developmental stages using solid phase microextraction. J Agric Food Chem. 2001;49:1345–52.PubMedCrossRefGoogle Scholar
  10. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V. Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol. 2015;32:76–84.PubMedCrossRefGoogle Scholar
  11. Beyer P, Morell M, Mackay I, Powell W. From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr Opin Plant Biol. 2008;11:215–21.CrossRefGoogle Scholar
  12. Blanca J, Cañizares J, Ziarsolo P, Esteras C, Mir G, Nuez F, Garcia-Mas J, Picó B. Melon transcriptome characterization: SSRs and SNPs discovery for high throughput genotyping across the species. Plant Genome. 2011;4:118–31.CrossRefGoogle Scholar
  13. Blanca J, Esteras C, Ziarsolo P, Pérez D, FernáNdez-Pedrosa V, Collado C, De Pablos R RÃ, Ballester A, Roig C, Cañizares J, Picó B. Transcriptome sequencing for SNP discovery across Cucumis melo. BMC Genomics. 2012;13:1–18.CrossRefGoogle Scholar
  14. Brewer MT, Lang L, Fujimura K, Dujmovic N, Gray S, Van Der Knaap E. Development of a controlled vocabulary and software application to analyze fruit shape variation in tomato and other plant species. Plant Physiol. 2006;141:15–25.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Burger Y, Shen S, Petreikov M, Schaffer AA. The contribution of sucrose to total sugar content in melon. In: VII Eucarpia meeting on cucurbit genetics and breeding. Katzir N, Paris HS, editors. ISHS Acta Hortic. 2000;510:479–85.Google Scholar
  16. Burger Y, Saar U, Katzir N, Paris HS, Yeselson Y, Levin I, Schaffer AA. A single recessive gene for sucrose accumulation in Cucumis melo fruit. J Am Soc Hortic Sci. 2002;127:938–43.Google Scholar
  17. Burger Y, Sa’ar U, Distelfeld A, Katzir N, Yeselson Y, Shen S, Schaffer AA. Development of sweet melon (Cucumis melo) genotypes combining high sucrose and organic acid content. J Am Soc Hortic Sci. 2003;128:537–40.Google Scholar
  18. Burger Y, Sa’ar U, Paris HS, Lewinsohn E, Katzir N, Tadmor Y, Schaffer AA. Genetic variability for valuable fruit quality traits in Cucumis melo. Israel J Plant Sci. 2006;54:233–42.CrossRefGoogle Scholar
  19. Burger Y, Schaffer AA. The contribution of sucrose metabolism enzymes to sucrose accumulation in Cucumis melo. J Am Soc Hortic Sci. 2007;132:704–12.Google Scholar
  20. Burger Y, Paris H, Cohen R, Katzir N, Tadmor Y, Lewinsohn E, Schaffer AA. Genetic diversity of Cucumis melo. Hortic Rev. 2009;36:165–98.Google Scholar
  21. Cao S, Chen H, Zhang C, Tang Y, Liu J, Qi H. Heterologous expression and biochemical characterization of two lipoxygenases in Oriental melon Cucumis melo var. makuwa Makino. PLoS ONE. 2016;11:e0153801.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Carmi N, Zhang G, Petreikov M, Gao Z, Eyal Y, Granot D, Schaffer AA. Cloning and functional expression of alkaline α-galactosidase from melon fruit: similarity to plant SIP proteins uncovers a novel family of plant glycosyl hydrolases. Plant J. 2003;33:97–106.PubMedCrossRefGoogle Scholar
  23. Cazzonelli CI, Pogson BJ. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 2010;15:266–74.PubMedCrossRefGoogle Scholar
  24. Chayut N, Yuan H, Ohali S, Meir A, Yeselson Y, Portnoy V, Zheng Y, Fei Z, Lewinsohn E, Katzir N, Schaffer AA, Gepstein S, Burger J, Li L, Tadmor Y. A bulk segregant transcriptome analysis reveals metabolic and cellular processes associated with orange allelic variation and fruit β-carotene accumulation in melon fruit. BMC Plant Biol. 2015;15:274.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chen S, Zhang R, Hao L, Chen W, Cheng S. Profiling of volatile compounds and associated gene expression and enzyme activity during fruit development in two cucumber cultivars. PLoS ONE. 2015;10:e0119444.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clayberg CD. Interaction and linkage test of flesh colour genes in Cucumis melo L. Cucurbit Genet Coop. 1992;15:53.Google Scholar
  27. Clepet C, Joobeur T, Zheng Y, Jublot D, Huang M, Truniger V, Boualem A, Hernandez-Gonzalez ME, Dolcet-Sanjuan R, Portnoy V, Mascarell-Creus A, Caño-Delgado AI, Katzir N, Bendahmane A, Giovannoni JJ, Aranda MA, Garcia-Mas J, Fei Z. Analysis of expressed sequence tags generated from full-length enriched cDNA libraries of melon. BMC Genomics. 2011;12:1–12.CrossRefGoogle Scholar
  28. Cohen S, Itkin M, Yeselson Y, Tzuri G, Portnoy V, Harel-Baja R, Lev S, Sa’ar U, Davidovitz-Rikanati R, Baranes N, Bar E, Wolf D, Petreikov M, Shen S, Ben-Dor S, Rogachev I, Aharoni A, Ast T, Schuldiner M, Belausov E, Eshed R, Ophir R, Sherman A, Frei B, Neuhaus HE, Xu Y, Fei Z, Giovannoni J, Lewinsohn E, Tadmor Y, Paris HS, Katzir N, Burger Y, Schaffer AA. The PH gene determines fruit acidity and contributes to the evolution of sweet melons. Nat Commun. 2014;5:4026.PubMedCrossRefGoogle Scholar
  29. Cuevas HE, Staub JE, Simon PW, Zalapa JE, Mccreight JD. Mapping of genetic loci that regulate quantity of beta-carotene in fruit of US Western Shipping melon (Cucumis melo L.). Theor Appl Genet. 2008;117:1345–59.PubMedCrossRefGoogle Scholar
  30. Cuevas HE, Staub JE, Simon PW, Zalapa JE. A consensus linkage map identifies genomic regions controlling fruit maturity and beta-carotene-associated flesh color in melon (Cucumis melo L.). Theor Appl Genet. 2009;119:741–56.PubMedCrossRefGoogle Scholar
  31. Dai N, Petreikov M, Portnoy V, Katzir N, Pharr DM, Schaffer AA. Cloning and expression analysis of a UDP-galactose/glucose pyrophosphorylase from melon fruit provides evidence for the major metabolic pathway of galactose metabolism in raffinose oligosaccharide metabolizing plants. Plant Physiol. 2006;142:294–304.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Dai N, Cohen S, Portnoy V, Tzuri G, Harel-Beja R, Pompan-Lotan M, Carmi N, Zhang G, Diber A, Pollock S, Karchi H, Yeselson Y, Petreikov M, Shen S, Sahar U, Hovav R, Lewinsohn E, Tadmor Y, Granot D, Ophir R, Sherman A, Fei Z, Giovannoni J, Burger Y, Katzir N, Schaffer A. Metabolism of soluble sugars in developing melon fruit: a global transcriptional view of the metabolic transition to sucrose accumulation. Plant Mol Biol. 2011;76:1–18.PubMedCrossRefGoogle Scholar
  33. Danin-Poleg Y, Tadmor Y, Tzuri G, Reis N, Hirschberg J, Katzir N. Construction of a genetic map of melon with molecular markers and horticultural traits, and localization of genes associated with ZYMV resistance. Euphytica. 2002;125:373–84.CrossRefGoogle Scholar
  34. Deleu W, Esteras C, Roig C, Gonzalez-To M, Fernandez-Silva I, Gonzalez-Ibeas D, Blanca J, Aranda MA, Arus P, Nuez F, Monforte AJ, Pico MB, Garcia-Mas J. A set of EST-SNPs for map saturation and cultivar identification in melon. BMC Plant Biol. 2009;9.Google Scholar
  35. Diallinas G, Kanellis AK. A phenylalanine ammonia-lyase gene from melon fruit: cDNA cloning, sequence and expression in response to development and wounding. Plant Mol Biol. 1994;26:473–9.PubMedCrossRefGoogle Scholar
  36. Diaz A, Fergany M, Formisano G, Ziarsolo P, Blanca J, Fei Z, Staub J, Zalapa J, Cuevas H, Dace G, Oliver M, Boissot N, Dogimont C, Pitrat M, Hofstede R, Van Koert P, Harel-Beja R, Tzuri G, Portnoy V, Cohen S, Schaffer A, Katzir N, Xu Y, Zhang H, Fukino N, Matsumoto S, Garcia-Mas J, Monforte A. A consensus linkage map for molecular markers and Quantitative Trait Loci associated with economically important traits in melon (Cucumis melo L.). BMC Plant Biol. 2011;11:111.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dickinson J, Salgado L, Hewlins M. The catabolism of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J Biol Chem. 2003;278:8028–34.PubMedCrossRefGoogle Scholar
  38. Dudareva N, Klempien A, Muhlemann JK, Kaplan I. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 2013;198:16–32.PubMedCrossRefGoogle Scholar
  39. El-Sharkawy I, Manriquez D, Flores F, Regad F, Bouzayen M, Latche A, Pech J. Functional characterization of a melon alcohol acyl-transferase gene family involved in the biosynthesis of ester volatiles. Identification of the crucial role of a threonine residue for enzyme activity. Plant Mol Biol. 2005;59:345–62.PubMedCrossRefGoogle Scholar
  40. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. 2011;6:e19379.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Esteras C, Nuez F, Picó B. Genetic diversity studies in Cucurbits using molecular tools. In: Behera TK, Wang Y, Kole C, editors. Genetics, genomics and breeding of Cucurbits. Enfield: Science Publishers Inc; 2012.Google Scholar
  42. Falcone Ferreyra ML, Rius SP, Casati P. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci. 2012;3:222.PubMedPubMedCentralGoogle Scholar
  43. Farré G, Sanahuja G, Naqvi S, Al E. Travel advice on the road to carotenoids in plants. Plant Sci. 2010;179:28–48.CrossRefGoogle Scholar
  44. Feder A, Burger J, Gao S, Lewinsohn E, Katzir N, Schaffer AA, Meir A, Davidovich-Rikanati R, Portnoy V, Gal-On A, Fei Z, Kashi Y, Tadmor Y. A Kelch domain-containing F-box coding gene negatively regulates flavonoid accumulation in Cucumis melo L. Plant Physiol. 2015. doi: 10.1104/pp.15.01008.PubMedPubMedCentralGoogle Scholar
  45. Flores F, Ben Amor M, Jones B, Pech JC, Bouzayen M, Latché A, Romojaro F. The use of ethylene-suppressed lines to assess differential sensitivity to ethylene of the various ripening pathways in Cantaloupe melons. Physiol Plant. 2001a;113:128–33.CrossRefGoogle Scholar
  46. Flores FB, Martínez-Madrid MC, Sánchez-Hidalgo FJ, Romojaro F. Differential rind and pulp ripening of transgenic antisense ACC oxidase melon. Plant Physiol Biochem. 2001b;39:37–43.CrossRefGoogle Scholar
  47. Fraser PD, Bramley PM. The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res. 2004;43:228–65.PubMedCrossRefGoogle Scholar
  48. Freilich S, Lev S, Gonda I, Reuveni E, Portnoy V, Oren E, Lohse M, Galpaz N, Bar E, Tzuri G, Wissotsky G, Meir A, Burger J, Tadmor Y, Schaffer AA, Fei Z, Giovannoni J, Lewinsohn E, Katzir N. Systems approach for exploring the intricate associations between sweetness, color and aroma in melon fruits. BMC Plant Biol. 2015;15:71.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Galliard T, Phillips D. The enzymic cleavage of linoleic acid to C9 carbonyl fragments in extracts of cucumber (Cucumis sativus) fruit and the possible role of lipoxygenase. Biochim Biophys Acta. 1976;431:278–87.PubMedCrossRefGoogle Scholar
  50. Gao Z, Petreikov M, Burger Y, Shen S, Schaffer A. Stachyose to sucrose metabolism in sweet melon (Cucumis melo) fruit mesocarp during the sucrose accumulation stage. In: Lebeda A, Paris HS, editors. Progress in Cucurbit genetics and breeding research: proceedings of Cucurbitaceae 2004, the 8th EUCARPIA meeting on Cucurbit genetics and breeding. olomouc: Palacký University in Olomouc; 2004. p. 471–5.Google Scholar
  51. Gao ZF, Schaffer AA. A novel alkaline alpha-galactosidase from melon fruit with a substrate preference for raffinose. Plant Physiol. 1999;119:979–87.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González VM, Hénaff E, Câmara F, Cozzuto L, Lowy E, Alioto T, Capella-Gutiérrez S, Blanca J, Cañizares J, Ziarsolo P, Gonzalez-Ibeas D, Rodríguez-Moreno L, Droege M, L D, Alvarez-Tejado M, Lorente-Galdos B, Melé M, Yang L, Weng Y, Navarro A, Marques-Bonet T, Aranda MA, Nuez F, Picó B, Gabaldón T, Roma G, Guigó R, Casacuberta JM, Arús P, Puigdomènech P. The genome of melon (Cucumis melo L.). Proc Natl Acad Sci. 2012;109:11872–7.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Giovannoni JJ. Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol. 2001;52:725–49.PubMedCrossRefGoogle Scholar
  54. Giovannoni JJ. Genetic regulation of fruit development and ripening. Plant Cell Online. 2004;16:S170–80.CrossRefGoogle Scholar
  55. Giovannoni JJ. Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol. 2007;10:283–9.PubMedCrossRefGoogle Scholar
  56. Giuliano G, Tavazza R, Diretto G. Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol. 2008;26:139–45.PubMedCrossRefGoogle Scholar
  57. Goff SA, Klee HJ. Plant volatile compounds: Sensory cues for health and nutritional value? Science. 2006;311:815–9.PubMedCrossRefGoogle Scholar
  58. Gonda I, Bar E, Portnoy V, Lev S, Burger J, Schaffer AA, Tadmor Y, Gepstein S, Giovannoni J, Katzir N, Lewinsohn E. Branched-chain and aromatic amino acid catabolism into aroma volatiles in Cucumis melo L. fruit. J Exp Bot. 2010;61:1111–23.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Gonda I, Lev S, Bar E, Sikron N, Portnoy V, Davidovich-Rikanati R, Burger J, Schaffer AA, Tadmor Y, Giovannonni J, Huang M, Fei Z, Katzir N, Fait A, Lewinsohn E. Catabolism of L-methionine in the formation of sulfur and other volatiles in melon (Cucumis melo L.) fruit. Plant J. 2013;74:458–72.PubMedCrossRefGoogle Scholar
  60. Gonda I, Burger Y, Schaffer AA, Ibdah M, Tadmor Y, Katzir N, Fait A, Lewinsohn E. Biosynthesis and perception of melon aroma. In: Havkin-Frenkel D, Dudai N, editors. Biotechnology in flavor production. Oxford: Wiley-Blackwell Publishing Ltd.; 2016.Google Scholar
  61. Gonzalez-Ibeas D, Blanca J, Roig C, González-To M, Picó B, Truniger V, Gómez P, Deleu W, Caño-Delgado A, Arús P, Nuez F, Garcia-Mas J, Puigdomènech P, Aranda MA. MELOGEN: an EST database for melon functional genomics. BMC Genomics. 2007;8:1–17.CrossRefGoogle Scholar
  62. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, Mcmullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES. A first-generation haplotype map of maize. Science. 2009;326:1115–7.PubMedCrossRefGoogle Scholar
  63. Graham RD, Welch RM, Bouis HE. Addressing micronutrient malnutrition through enhancing the nutritional quality of staple foods: principles, perspectives and knowledge gaps. In: Advances in agronomy. Academic Press, Cambridge, Massachusetts; 2001, p. 77–142.Google Scholar
  64. Granier C, Vile D. Phenotyping and beyond: modelling the relationships between traits. Curr Opin Plant Biol. 2014;18:96–102.PubMedCrossRefGoogle Scholar
  65. Grumet R, Katzir N, Little HA, Portnoy V, Burger Y. New insights into reproductive development in melon (Cucumis melo L.). Int J Plant Dev Biol. 2007;1:253–64.Google Scholar
  66. Guis M, Botondi R, Ben-Amor M, Ayub R, Bouzayen M, Pech J-C, Latché A. Ripening-associated biochemical traits of cantaloupe Charentais melons expressing an antisense ACC oxidase transgene. J Am Soc Hortic Sci. 1997;122:748–51.Google Scholar
  67. Hadfield KA, Rose JKC, Yaver DS, Berka RM, Bennett AB. Polygalacturonase gene expression in ripe melon fruit supports a role for polygalacturonase in ripening-associated pectin disassembly. Plant Physiol. 1998;117:363–73.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hadfield KA, Dang T, Guis M, Pech J-C, Bouzayen M, Bennett AB. Characterization of ripening-regulated cDNAs and their expression in ethylene-suppressed Charentais melon fruit. Plant Physiol. 2000;122:977–84.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hao J, Niu Y, Yang B, Gao F, Zhang L, Wang J, Hasi A. Transformation of a marker-free and vector-free antisense ACC oxidase gene cassette into melon via the pollen-tube pathway. Biotechnol Lett. 2011;33:55–61.PubMedCrossRefGoogle Scholar
  70. Harel-Beja R, Tzuri G, Portnoy V, Lotan-Pompan M, Lev S, Cohen S, Dai N, Yeselson L, Meir A, SE L, Avisar E, Melame T, Van Koert P, Verbakel H, Hofstede R, Volpin H, Oliver M, Fougedoire A, Stalh C, Fauve J, Copes B, Fei Z, Giovannoni J, Ori N, Lewinsohn E, Sherman A, Burger J, Tadmor Y, AA S, Katzir N. A genetic map of melon highly enriched with fruit quality QTLs and EST markers, including sugar and carotenoid metabolism genes. Theor Appl Genet. 2010;121:511–33.PubMedCrossRefGoogle Scholar
  71. Hirschberg J. Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol. 2001;4:210–8.PubMedCrossRefGoogle Scholar
  72. Hoen PC, Friedlander MR, Almlof J, Sammeth M, Pulyakhina I, Anvar SY, Laros JFJ, Buermans HPJ, Karlberg O, Brannvall M, Consortium TG, Dunnen JTD, Ommen G-JBV, Gut IG, Guigo R, Estivill X, Syvanen A-C, Dermitzakis ET, Lappalainen T. Reproducibility of high-throughput mRNA and small RNA sequencing across laboratories. Nat Biotechnol. 2013;31:1015–22.PubMedCrossRefGoogle Scholar
  73. Hubbard NL, Huber SC, Pharr DM. Sucrose phosphate synthase and acid invertase as determinants of sucrose concentration in developing muskmelon (Cucumis melo L.) fruits. Plant Physiol. 1989;91:1527–34.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Hughes M. The inheritance of two characters of Cucumis melo and their interrelationship. Proc Am Soc Horticult Sci. 1948;59:399–402.Google Scholar
  75. Ibdah M, Azulay Y, Portnoy V, Wasserman B, Bar E, Meir A, Burger Y, Hirschberg J, Schaffer AA, Katzir N, Tadmor Y, Lewinsohn E. Functional characterization of CmCCD1, a carotenoid cleavage dioxygenase from melon. Phytochemistry. 2006;67:1579–89.PubMedCrossRefGoogle Scholar
  76. Ignat T, Schmilovitch Z, Fefoldi J, Steiner B, Alkalai-Tuvia S. Non-destructive measurement of ascorbic acid content in bell peppers by VIS-NIR and SWIR spectrometry. Postharvest Biol Technol. 2012;74:91–9.CrossRefGoogle Scholar
  77. Imperato F. Five plants of the family Cucurbitaeeae with flavonoid patterns of pollens different from those of corresponding stigmas. Experientia. 1980;36:1136–7.CrossRefGoogle Scholar
  78. Ishiki Y, Oda A, Yaegashi Y, Orihara Y, Arai T, Hirabayashi T, Nakagawa H, Sato T. Cloning of an auxin-responsive 1-aminocyclopropane-1-carboxylate synthase gene (CMe-ACS2) from melon and the expression of ACS genes in etiolated melon seedlings and melon fruits. Plant Sci. 2000;159:173–81.PubMedCrossRefGoogle Scholar
  79. Jordan MJ, Shaw PE, Goodner KL. Volatile components in aqueous essence and fresh fruit of Cucumis melo cv. athena (muskmelon) by GC-MS and GC-O. J Agric Food Chem. 2001;49:5929–33.PubMedCrossRefGoogle Scholar
  80. Karvouni Z, John I, Taylor JE, Watson CF, Turner AJ, Grierson D. Isolation and characterisation of a melon cDNA clone encoding phytoene synthase. Plant Mol Biol. 1995;27:1153–62.PubMedCrossRefGoogle Scholar
  81. Kourkoutas D, Elmore JS, Mottram DS. Comparison of the volatile compositions and flavour properties of cantaloupe, Galia and honeydew muskmelons. Food Chem. 2006;97:95–102.CrossRefGoogle Scholar
  82. Kover PX, Valdar W, Trakalo J, Scarcelli N, Ehrenreich IM, Purugganan MD, Durrant C, Mott R. A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genet. 2009;5:e1000551.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Krauze-Baranowska M, Cisowski W. Flavonoids from some species of the genus Cucumis. Biochem Syst Ecol. 2001;29:321–4.PubMedCrossRefGoogle Scholar
  84. Kubicki S. Polyploidy in melons (Cucumis melo L.) and cucumbers (Cucumis sativus L.). Genet Polonica. 1962;2-3:161–79.Google Scholar
  85. Lasserre E, Bouquin T, Hernandez JA, Pech J-C, Balagué C, Bull J. Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.). Mol Gen Genet. 1996;251:81–90.PubMedGoogle Scholar
  86. Leida C, Moser C, Esteras C, Sulpice R, Lunn JE, De Langen F, Monforte AJ, Picó B. Variability of candidate genes, genetic structure and association with sugar accumulation and climacteric behavior in a broad germplasm collection of melon (Cucumis melo L.). BMC Genet. 2015;16:1–17.CrossRefGoogle Scholar
  87. Lewinsohn E, Gijzen M. Phytochemical diversity: the sounds of silent metabolism. Plant Sci. 2009;176:161–9.CrossRefGoogle Scholar
  88. Li L, Yuan H. Chromoplast biogenesis and carotenoid accumulation. Arch Biochem Biophys. 2013;539:102–9.PubMedCrossRefGoogle Scholar
  89. Lignou S, Parker JK, Baxter C, Mottram DS. Sensory and instrumental analysis of medium and long shelf-life Charentais cantaloupe melons (Cucumis melo L.) harvested at different maturities. Food Chem. 2014;148:218–29.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Liu L, Shao Z, Zhang M, Wang Q. Regulation of carotenoid metabolism in tomato. Mol Plant. 2015;8:28–39.PubMedCrossRefGoogle Scholar
  91. Lu S, Van Eck J, Zhou X, Lopez AB, O’halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, Kochian LV, Küpper H, Earle ED, Cao J, Li L. The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell. 2006;18:3594–605.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Lucchetta L, Manriquez D, El-Sharkawy I, Flores FB, Sanchez-Bel P, Zouine M, Ginies C, Bouzayen M, Rombaldi C, Pech JC, Latche A. Biochemical and catalytic properties of three recombinant alcohol acyltransferases of melon. Sulfur-containing ester formation, regulatory role of CoA-SH in activity, and sequence elements conferring substrate preference. J Agric Food Chem. 2007;55:5213–20.PubMedCrossRefGoogle Scholar
  93. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, Richardson MF, Anholt RRH, Barron M, Bess C, Blankenburg KP, Carbone MA, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan JC, Jhangiani SN, Jordan KW, Lara F, Lawrence F, Lee SL, Librado P, Linheiro RS, Lyman RF, Mackey AJ, Munidasa M, Muzny DM, Nazareth L, Newsham I, Perales L, Pu L-L, Qu C, Ramia M, Reid JG, Rollmann SM, Rozas J, Saada N, Turlapati L, Worley KC, Wu Y-Q, Yamamoto A, Zhu Y, Bergman CM, Thornton KR, Mittelman D, Gibbs RA. The Drosophila melanogaster genetic reference panel. Nature. 2012, 482, 173-178.asxGoogle Scholar
  94. Manríquez D, El-Sharkawy I, Flores F, El-Yahyaoui F, Regad F, Bouzayen M, Latché A, Pech J-C. Two highly divergent alcohol dehydrogenases of melon exhibit fruit ripening-specific expression and distinct biochemical characteristics. Plant Mol Biol. 2006;61:675–85.PubMedCrossRefGoogle Scholar
  95. Mascarell-Creus A, Cañizares J, Vilarrasa-Blasi J, Mora-García S, Blanca J, Gonzalez-Ibeas D, Saladié M, Roig C, Deleu W, Picó-Silvent B, López-Bigas N, Aranda MA, Garcia-Mas J, Nuez F, Puigdomènech P, Caño-Delgado AI. An oligo-based microarray offers novel transcriptomic approaches for the analysis of pathogen resistance and fruit quality traits in melon (Cucumis melo L.). BMC Genomics. 2009;10:1–15.CrossRefGoogle Scholar
  96. Mcquinn RP, Giovannoni JJ, Pogson BJ. More than meets the eye: from carotenoid biosynthesis, to new insights into apocarotenoid signaling. Curr Opin Plant Biol. 2015;27:172–9.PubMedCrossRefGoogle Scholar
  97. Miki T, Yamamoto M, Nakagawa H, Ogura N, Mori H, Imaseki H, Sato T. Nucleotide sequence of a cDNA for 1-aminocyclopropane-1-carboxylate synthase from melon fruits. Plant Physiol. 1995;107:297–8.PubMedPubMedCentralCrossRefGoogle Scholar
  98. Minervini M, Abdelsamea MM, Tsaftaris SA. Image-based plant phenotyping with incremental learning and active contours. Eco Inform. 2014;23:35–48.CrossRefGoogle Scholar
  99. Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A, Aharoni A. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol. 2008;147:823–51.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Monforte AJ, Oliver M, Gonzalo MJ, Alvarez JM, Dolcet-Sanjuan R, Arus P. Identification of quantitative trait loci involved in fruit quality traits in melon (Cucumis melo L.). Theor Appl Genet. 2004;108:750–8.PubMedCrossRefGoogle Scholar
  101. Mussinan CJ, Keelan ME. Sulfur compounds in foods. In: Sulfur compounds in foods. American Chemical Society, Washington, D.C.; 1994. p. 1–6.Google Scholar
  102. Nisar N, Li L, Lu S, Khin NC, Pogson BJ. Carotenoid metabolism in plants. Mol Plant. 2015;8:68–82.PubMedCrossRefGoogle Scholar
  103. Nuñez-Palenius H, Cantliffe D, Huber D, Ciardi J, Klee H. Transformation of a muskmelon ‘Galia’ hybrid parental line (Cucumis melo L. var. reticulatus; Ser.) with an antisense ACC oxidase gene. Plant Cell Rep. 2006;25:198–205.PubMedCrossRefGoogle Scholar
  104. Nuñez-Palenius HG, Gomez-Lim M, Ochoa-Alejo N, Grumet R, Lester G, Cantliffe DJ. Melon fruits: genetic diversity, physiology, and biotechnology features. Crit Rev Biotechnol. 2008;28:13–55.PubMedCrossRefGoogle Scholar
  105. Ogura T, Busch W. From phenotypes to causal sequences: using genome wide association studies to dissect the sequence basis for variation of plant development. Curr Opin Plant Biol. 2015;23:98–108.PubMedCrossRefGoogle Scholar
  106. Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S. Characterization of phloem-sap transcription profile in melon plants. J Exp Bot. 2007;58:3645–56.PubMedCrossRefGoogle Scholar
  107. Paris HS, Amar Z, Lev E. Medieval emergence of sweet melons, Cucumis melo (Cucurbitaceae). Ann Bot. 2012;110:23–33.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Paris MK, Zalapa JE, Mccreight JD, Staub JE. Genetic dissection of fruit quality components in melon (Cucumis melo L.) using a RIL population derived from exotic x elite US Western Shipping germplasm. Mol Breed. 2008;22:405–19.CrossRefGoogle Scholar
  109. Pascual L, Desplat N, Huang BE, Desgroux A, Bruguier L, Bouchet JP, Le QH, Chauchard B, Verschave P, Causse M. Potential of a tomato MAGIC population to decipher the genetic control of quantitative traits and detect causal variants in the resequencing era. Plant Biotechnol J. 2015;13:565–77.PubMedCrossRefGoogle Scholar
  110. Pech JC, Bouzayen M, Latche A. Climacteric fruit ripening: ethylene-dependent and independent regulation of ripening pathways in melon fruit. Plant Sci. 2008;175:114–20.CrossRefGoogle Scholar
  111. Perin C, Hagen LS, De Conto V, Katzir N, Danin-Poleg Y, Portnoy V, Baudracco-Arnas S, Chadoeuf J, Dogimont C, Pitrat M. A reference map of Cucumis melo based on two recombinant inbred line populations. Theor Appl Genet. 2002;104:1017–34.PubMedCrossRefGoogle Scholar
  112. Perry PL, Wang Y, Lin J. Analysis of honeydew melon (Cucumis melo var. inodorus) flavour and GC–MS/MS identification of (E,Z)-2,6-nonadienyl acetate. Flavour Fragr J. 2009;24:341–7.CrossRefGoogle Scholar
  113. Phillips DR, Galliard T. Flavour biogenesis. Partial purification and properties of a fatty acid hydroperoxide cleaving enzyme from fruits of cucumber. Phytochemistry. 1978;17:355–8.CrossRefGoogle Scholar
  114. Pitrat M, Hanelt P, Hammer K. Some comments on infraspecific classification of cultivars of melon. In: Katzir N, Paris HS, editors. VII Eucarpia meeting on Cucurbit genetics and breeding. ISHS Acta Hortic. 2000;510:29–36.Google Scholar
  115. Poland JA, Rife TW. Genotyping-by-sequencing for plant breeding and genetics. Plant Gen. 2012;5:92–102.CrossRefGoogle Scholar
  116. Portnoy V, Benyamini Y, Bar E, Harel-Beja R, Gepstein S, Giovannoni JJ, Schaffer AA, Burger J, Tadmor Y, Lewinsohn E, Katzir N. The molecular and biochemical basis for varietal variation in sesquiterpene content in melon (Cucumis melo L.) rinds. Plant Mol Biol. 2008;66:647–61.PubMedCrossRefGoogle Scholar
  117. Portnoy V, Diber A, Pollock S, Karchi H, Lev S, Tzuri G, Harel-Beja R, Forer R, Portnoy VH, Lewinsohn E, Tadmor Y, Burger J, Schaffer A, Katzir N. Use of non-normalized, non-amplified cDNA for 454-based RNA sequencing of fleshy melon fruit. Plant Genome. 2011;4:36–46.CrossRefGoogle Scholar
  118. Rosa JT. Change in composition during ripening and storage of melons. Hilgardia. 1928;3:421–43.CrossRefGoogle Scholar
  119. Rose JKC, Hadfield KA, Labavitch JM, Bennett AB. Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol. 1998;117:345–61.PubMedPubMedCentralCrossRefGoogle Scholar
  120. Saladié M, Cañizares J, Phillips MA, Rodriguez-Concepcion M, Larrigaudière C, Gibon Y, Stitt M, Lunn JE, Garcia-Mas J. Comparative transcriptional profiling analysis of developing melon (Cucumis melo L.) fruit from climacteric and non-climacteric varieties. BMC Genomics. 2015;16:440.PubMedPubMedCentralCrossRefGoogle Scholar
  121. Schaffer AA, Aloni B, Fogelman E. Sucrose metabolism and accumulation in developing fruit of Cucumis. Phytochemistry. 1987;26:1883–7.CrossRefGoogle Scholar
  122. Schaffer AA, Pharr DM, Madore M. Cucurbits. In: Zamski E, Schaffer AA, editors. Photoassimilate distribution in plants and crops. New York: Marcel Dekker; 1996. p. 729–57.Google Scholar
  123. Schieberle P, Ofner S, Grosch W. Evaluation of potent odorants in cucumbers (Cucumis sativus) and muskmelons (Cucumis melo) by aroma extract dilution analysis. J Food Sci. 1990;55:193–5.CrossRefGoogle Scholar
  124. Schmilovitch ZE, Ignat T, Alchanatis V, Gatker J, Ostrovsky V, Felföldi J. Hyperspectral imaging of intact bell peppers. Biosyst Eng. 2014;117:83–93.CrossRefGoogle Scholar
  125. Schwab W, Davidovich-Rikanati R, Lewinsohn E. Biosynthesis of plant-derived flavor compounds. Plant J. 2008;54:712–32.PubMedCrossRefGoogle Scholar
  126. Serres-Giardi L, Dogimont C.  Cucurbitaceae: proceedings of the Xth Eucarpia meeting on genetics and breeding of Cucurbitaceae. In: Sari N, Solmaz I, Aras V (eds.). Adana: Cukurova University; 2012. p. 254–63.Google Scholar
  127. Shalit M, Katzir N, Tadmor Y, Larkov O, Burger Y, Shalekhet F, Lastochkin E, Ravid U, Amar O, Edelstein M, Karchi Z, Lewinsohn E. Acetyl-CoA: alcohol acetyltransferase activity and aroma formation in ripening melon fruits. J Agric Food Chem. 2001;49:794–9.PubMedCrossRefGoogle Scholar
  128. Shumskaya M, Bradbury LMT, Monaco RR, Wurtzel ET. Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. Plant Cell. 2012;24:3725–41.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Simkin AJ, Schwartz SH, Auldridge M, Taylor MG, Klee HJ. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J. 2004;40:882–92.PubMedCrossRefGoogle Scholar
  130. Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F. An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS ONE. 2013;8:e54603.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Stepansky A, Kovalski I, Schaffer AA, Perl-Treves R. Variation in sugar levels and invertase activity in mature fruit representing a broad spectrum of Cucumis melo genotypes. Genet Resour Crop Evol. 1999;46:53–62.CrossRefGoogle Scholar
  132. Sweeney JP, Chapman VJ, Hepner PA. Sugar, acid, and flavor in fresh fruits. J Am Diet Assoc. 1970;57:432–5.PubMedGoogle Scholar
  133. Tadmor Y, Burger J, Yaakov I, Feder A, Libhaber SE, Portnoy V, Meir A, Tzuri G, Sa’ar U, Rogachev I, Aharoni A, Abeliovich H, Schaffer AA, Lewinsohn E, Katzir N. Genetics of flavonoid, carotenoid, and chlorophyll pigments in melon fruit rinds. J Agric Food Chem. 2010;58:10722–8.PubMedCrossRefGoogle Scholar
  134. Tanabata T, Shibaya T, Hori K, Ebana K, Yano M. SmartGrain: high-throughput phenotyping software for measuring seed shape through image analysis. Plant Physiol. 2012;160:1871–80.PubMedPubMedCentralCrossRefGoogle Scholar
  135. Tang Y, Zhang C, Cao S, Wang X, Qi H. The effect of CmLOXs on the production of volatile organic compounds in four aroma types of melon (Cucumis melo). PLoS ONE. 2015;10:e0143567.PubMedPubMedCentralCrossRefGoogle Scholar
  136. The International Hapmap C. A haplotype map of the human genome. Nature. 2005;437:1299–320.CrossRefGoogle Scholar
  137. Tzuri G, Zhou X, Chayut N, Yuan H, Portnoy V, Meir A, Sa’ar U, Baumkoler F, Mazourek M, Lewinsohn E, Fei Z, Schaffer AA, Li L, Burger J, Katzir N, Tadmor Y. A ‘golden’ SNP in CmOr governs the fruit flesh color of melon (Cucumis melo). Plant J. 2015;82:267–79.PubMedCrossRefGoogle Scholar
  138. Ulrich JI. In: The biochemistry of fruits and their products. Hulme AC, editor. London/New York: Academic Press;. 1971, p. 89–117.Google Scholar
  139. Wan X-H, Chen S-X, Wang C-Y, Zhang R-R, Cheng S-Q, Meng H-W, Shen X-Q. Isolation, expression, and characterization of a hydroperoxide lyase gene from cucumber. Int J Mol Sci. 2013;14:22082–101.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Wang Y, Lin J. Gas chromatography–olfactometry and gas chromatography–tandem mass spectrometry analysis of fresh cantaloupe (Cucumis melo L. var. cantalupensis Naudin) aroma. Flavour Fragr J. 2014;29:87–94.CrossRefGoogle Scholar
  141. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10:57–63.PubMedPubMedCentralCrossRefGoogle Scholar
  142. Weigel D, Mott R. The 1001 genomes project for Arabidopsis thaliana. Genome Biol. 2009;10:1–5.CrossRefGoogle Scholar
  143. Whitaker BD, Lester GE. Cloning of phospholipase and lipoxygenase Genes CmPLDa1 and CmLOX1 and their expression in fruit, floral, and vegetative tissues of ‘Honey Brew’ hybrid honeydew melon. J Am Soc Hortic Sci. 2006;131:544–50.Google Scholar
  144. Yahyaoui FEL, Wongs-Aree C, Latche A, Hackett R, Grierson D, Pech JC. Molecular and biochemical characteristics of a gene encoding an alcohol acyl-transferase involved in the generation of aroma volatile esters during melon ripening. Eur J Biochem. 2002;269:2359–66.PubMedCrossRefGoogle Scholar
  145. Yamaguchi M, Hughes DL, Yabumoto K, Jennings WG. Quality of cantaloupe muskmelons – variability and attributes. Sci Hortic. 1977;6:59–70.CrossRefGoogle Scholar
  146. Yamamoto M, Miki T, Ishiki Y, Fujinami K, Yanagisawa Y, Nakagawa H, Ogura N, Hirabayashi T, Sato T. The synthesis of ethylene in melon fruit during the early stage of ripening. Plant Cell Physiol. 1995;36:591–6.Google Scholar
  147. Yu J, Holland JB, Mcmullen MD, Buckler ES. Genetic design and statistical power of nested association mapping in maize. Genetics. 2008;178.Google Scholar
  148. Yuan H, Owsiany K, Sheeja TE, Zhou X, Rodriguez C, Li Y, Welsch R, Chayut N, Yang Y, Thannhauser TW, Parthasarathy MV, Xu Q, Deng X, Fei Z, Schaffer A, Katzir N, Burger J, Tadmor Y, Li L. A single amino acid substitution in an ORANGE protein promotes carotenoid overaccumulation in Arabidopsis. Plant Physiol. 2015a;169:421–31.PubMedPubMedCentralCrossRefGoogle Scholar
  149. Yuan H, Zhang J, Nageswaran D, Li L. Carotenoid metabolism and regulation in horticultural crops. Horm Res. 2015b;2:15036.CrossRefGoogle Scholar
  150. Zhang C, Jin Y, Liu J, Tang Y, Cao S, Qi H. The phylogeny and expression profiles of the lipoxygenase (LOX) family genes in the melon (Cucumis melo L.) genome. Sci Hortic. 2014;170:94–102.CrossRefGoogle Scholar
  151. Zhang H, Wang H, Yi H, Zhai W, Wang G, Fu Q. Transcriptome profiling of Cucumis melo fruit development and ripening. Horm Res. 2016;3:16014.CrossRefGoogle Scholar
  152. Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci. 2015;112:3558–63.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  • Amit Gur
    • 1
  • Itay Gonda
    • 1
  • Vitaly Portnoy
    • 1
  • Galil Tzuri
    • 1
  • Noam Chayut
    • 1
  • Shahar Cohen
    • 2
  • Yelena Yeselson
    • 2
  • Ayala Meir
    • 1
  • Einat Bar
    • 1
  • Rachel Davidovitz-Rikanati
    • 1
  • Uzi Saar
    • 1
  • Harry S. Paris
    • 1
  • Joseph Burger
    • 1
  • Yaakov Tadmor
    • 1
  • Efraim Lewinsohn
    • 1
  • Arthur A. Schaffer
    • 2
  • Nurit Katzir
    • 1
    Email author
  1. 1.Center for the Genetic Enhancement of Cucurbit Fruit Quality, Department of Vegetable Research, Newe Ya‘ar Research CenterAgricultural Research OrganizationRamat YishayIsrael
  2. 2.Center for the Genetic Enhancement of Cucurbit Fruit Quality, Department of Vegetable Research, Volcani CenterAgricultural Research OrganizationRishon Le-ZiyyonIsrael

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