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Theoretical and Applied Genetics

, Volume 116, Issue 4, pp 589–602 | Cite as

Candidate genes and QTLs for fruit ripening and softening in melon

  • Eduard Moreno
  • Javier M. Obando
  • Noelia Dos-Santos
  • J. Pablo Fernández-Trujillo
  • Antonio J. Monforte
  • Jordi Garcia-Mas
Original Paper

Abstract

Different factors affect the quality of melon fruit and among them long shelf life is critical from the consumer’s point of view. In melon, cultivars showing both climacteric and non-climacteric ripening types are found. In this study we have investigated climacteric ripening and fruit softening using a collection of near-isogenic lines (NILs) derived from the non-climacteric melon parental lines PI 161375 (SC) and “Piel de Sapo” (PS). Surprisingly, we found that QTL eth3.5 in NIL SC3-5b induced a climacteric-ripening phenotype with increased respiration and ethylene levels. Data suggest that the non-climacteric phenotypes from PI 161375 and “Piel de Sapo” may be the result of mutations in different genes. Several QTLs for fruit flesh firmness were also detected. Candidate genes putatively involved in ethylene regulation, biosynthesis and perception and cell wall degradation were mapped and some colocations with QTLs were observed. These results may provide additional data towards understanding of non-climacteric ripening in melon.

Keywords

Bacterial Artificial Chromosome Melon Ethylene Production Bacterial Artificial Chromosome Library Cleave Amplify Polymorphic Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Montserrat Saladié for critically reading the manuscript. This work was funded by grants AGL2003-09175-C02-01 and AGL2003-09175-C02-02 from the Spanish “Ministerio de Educación y Ciencia” (MEC). EM was supported by an AGAUR fellowship (Generalitat de Catalunya). JO was supported by a MAE-AECI fellowship from the Spanish Ministry of Foreigner Affairs. NDS was supported by two consecutive fellowships from FPI (Fundación Séneca de la Región de Murcia) and FPU (MEC AP2006-01565). We are indebted to Michel Pitrat (INRA, Montfavet, France) for the “Védrantais” seeds; to Fuensanta García, Claudia Miranda and María José Ferrer for technical assistance; to Plácido Varó and his team (CIFEA-Torre Pacheco, Consejería de Agricultura de la Región de Murcia) and Antoni Ortigosa for crop management.

References

  1. Altschul SF, Gish SF, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  2. Ayub R, Guis M, BenAmor M, Gillot L, Roustan JP, Latché A, Bouzayen M, Pech JC (1996) Expression of ACC oxidase antisense gene inhibits ripening of cantaloupe melon fruits. Nat Biotechnol 14:862–866CrossRefGoogle Scholar
  3. Barry C, Giovanonni J (2006) Ripening inhibition in the tomato Green-ripe mutant results from ectopic expression of a novel protein which disrupts ethylene signal transduction. Proc Natl Acad Sci USA 103:7923–7928PubMedCrossRefGoogle Scholar
  4. Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340PubMedCrossRefGoogle Scholar
  5. Causse M, Saliba-Colombani V, Lecomte L, Duffé P, Rousselle P, Buret M (2002) QTL analysis of fruit quality in fresh market tomato: a few chromosome regions control the variation of sensory and instrumental traits. J Exp Bot 53:2089–2098PubMedCrossRefGoogle Scholar
  6. Chaïb J, Devaux M-F, Grotte M-G, Robini K, Causse M, Lahaye M, Marty I (2007) Physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. J Exp Bot 58:1915–1925PubMedCrossRefGoogle Scholar
  7. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  8. Dunnet CW (1955) A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assn 50:1096–1121CrossRefGoogle Scholar
  9. Eduardo I, Arús P, Monforte AJ (2005) Development of a genomic library of near isogenic lines (NILs) in melon (Cucumis melo L.) from the exotic accession PI 161375. Theor Appl Genet 6:1–10Google Scholar
  10. Eduardo I, Obando J, Martínez JA, Alarcón AL, Arús P, Álvarez JM, van der Knaap E, Fernández-Trujillo JP, Monforte AJ (2007) Estimating the genetic architecture of fruit quality traits in melon (Cucumis melo L.) using a genomic library of near-isogenic lines. J Am Soc Hortic Sci 132:80–89Google Scholar
  11. Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162PubMedGoogle Scholar
  12. Fernández-Trujillo JP, Obando J, Martínez JA, Alarcón A, Eduardo I, Arús P, Monforte AJ (2005) Quality management of experiments with a collection of near-isogenic lines of melon. In: Atienza J, Rabasseda J (eds). Proceedings of third virtual Iberoamerican Congress of laboratory quality management. III IBEROLAB, Madrid, pp 149–158Google Scholar
  13. Fernández-Silva I, Blanca J, Picó MB, Nuez F, Arús P, Monforte AJ (2006) Mapeo de marcadores microsatélites a partir de librerías de ESTs de melón (Cucumis melo) mediante genotipado selectivo. Actas de Horticultura 45:109–110Google Scholar
  14. Garcia-Mas J, Oliver M, Gómez H, de Vicente MC (2000) AFLP, RAPD and RFLP markers to measure genetic diversity in melon. Theor Appl Genet 101:860–864CrossRefGoogle Scholar
  15. Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10:1–7CrossRefGoogle Scholar
  16. 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 (2007) MELOGEN: an EST database for melon functional genomics. BMC Genomics 8:306PubMedCrossRefGoogle Scholar
  17. Gonzalo MJ, Oliver M, Garcia-Mas J, Monfort A, Dolcet-Sanjuan R, Katzir N, Arús P, Monforte AJ (2005) Simple-sequence repeat (SSR) markers used in merging linkage maps of melon (Cucumis melo L.). Theor Appl Genet 110:802–811PubMedCrossRefGoogle Scholar
  18. Guis M, Botondi R, Ben Amor M, Ayub R, Bouzayen M, Pech JC, Latche A (1997) Ripening-associated biochemical traits of cantaloupe Charentais melons expressing antisense ACC oxidase transgene. J Am Soc Hortic Sci 122:748–751Google Scholar
  19. Hadfield KA, Rose JK, Yaver DS, Berka RM, Bennett AB (1998) Polygalacturonase gene expression in ripe melon fruit supports a role for polygalacturonase in ripening-associated pectin disassembly. Plant Physiol 117:363–373PubMedCrossRefGoogle Scholar
  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  21. Harker FR, Redgwell RJ, Hallett IC, Murray SH, Carter G (1997) Texture of fresh fruit. Hortic Rev 20:121–224Google Scholar
  22. Howad W, Yamamoto T, Dirlewanger E, Testolin R, Cosson P, Cipriani G, Monforte AJ, Georgi L, Abbott AG, Arus P (2006) Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305–1309CrossRefGoogle Scholar
  23. Ishiki Y, Oda A, Yaegashi Y, Orihara Y, Arai T, Hirabayashi T, Nakagawa H, Sato T (2000) 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. Asian J Plant Sci 159:173–181Google Scholar
  24. Kader AA (2000) Methods of gas mixing, sampling and analysis. In: Kader AA (ed) Postharvest technology of horticultural crops. Pub no 3311. Division of agriculture and natural resources, 3a edn. University of California, pp 145–148Google Scholar
  25. Lasserre E, Bouquin T, Hernández JA, Bull J, Pech JC, Balague C (1996) Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.). Mol Gen Genet 251:81–90PubMedGoogle Scholar
  26. Liebhard R, Kellerhals M, Pfammatter W, Jertmini M, Gessler C (2003) Mapping quantitative physiological traits in apple (Malus x domestica Borkh.). Plant Mol Biol 52:511–526PubMedCrossRefGoogle Scholar
  27. Lin YT, Pitt RE (1986) Rheology of apple and potato tissue as affected by cell turgor pressure. J Text Stud 17:291–313CrossRefGoogle Scholar
  28. Manning K, Tor M, Poole M, Hong Y, Thompson A, King G, Giovannoni J, Seymour G (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38:949–952CrossRefGoogle Scholar
  29. Miki T, Yamamoto M, Nakagawa H, Ogura N, Mori H, Imaseki H, Sato T (1995) Nucleotide sequence of a cDNA for 1-aminocyclopropane-1-carboxylate synthase from melon fruits. Plant Physiol 107:297–298PubMedCrossRefGoogle Scholar
  30. Mizuno S, Hirasawa Y, Sonoda M, Nakagawa H, Sato T (2006) Isolation and characterization of three DREB/ERF-type transcription factors from melon (Cucumis melo). Plant Sci 170:1156–1163CrossRefGoogle Scholar
  31. Monforte AJ, Oliver M, Gonzalo MJ, Álvarez JM, Dolcet-Sanjuan R, Arús P (2004) Identification of quantitative trait loci involved in fruit quality traits in melon (Cucumis melo L.). Theor Appl Genet 108:750–758PubMedCrossRefGoogle Scholar
  32. Moore S, Vrebalob J, Giovannoni J (2002) Use of genomic tools to isolate key ripening genes and analyse fruit maturation in tomato. J Exp Bot 53:2023–2030PubMedCrossRefGoogle Scholar
  33. Morales M, Roig E, Monforte AJ, Arus P, Garcia-Mas J (2004) Single-nucleotide polymorphisms detected in expressed sequence tags of melon (Cucumis melo L.). Genome 47:352–360PubMedCrossRefGoogle Scholar
  34. Nishiyama K, Guis M, Rose JKC, Kubo Y, Bennett KA, Wangjin L, Kato K, Ushijima K, Inaba A, Bouzayen M, Latche A, Pech JC, Bennett AB (2007) Ethylene regulation of fruit softening and cell wall disassembly in Charentais melon. J Exp Bot 58:1281–1290PubMedCrossRefGoogle Scholar
  35. Obando J, Fernández-Trujillo JP, Martínez JA, Alarcón AL, Eduardo I, Arús P, Monforte AJ (2007) Identification of melon fruit quality quantitative trait loci using near-isogenic lines. J Am Soc Hortic Sci (in press)Google Scholar
  36. Oliver M, Garcia-Mas J, Cardus M, Pueyo N, Lopez-Sese AL, Arroyo M, Gomez-Paniagua H, Arus P, de Vicente MC (2001) Construction of a reference linkage map for melon. Genome 44:836–845PubMedCrossRefGoogle Scholar
  37. Périn C, Gómez-Jiménez M, Hagen L, Dogimont C, Pech JC, Latché A, Pitrat M, Leliévre JM (2002) Molecular and genetic characterization of a non-climacteric phenotype in melon reveals two loci conferring altered ethylene response in fruit. Plant Physiol 129:300–309PubMedCrossRefGoogle Scholar
  38. Rose JKC, Catalá C, Gonzalez-Carranza ZH, Roberts J (2003) Plant cell wall disassembly. In: Rose JKC (ed). The plant cell wall: annual plant reviews series, vol 8. Blackwell Publishing Ltd, Oxford, pp 264–324Google Scholar
  39. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Meth Mol Biol 132:365–386Google Scholar
  40. Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272CrossRefGoogle Scholar
  41. Sato-Nara K, Yuhashi KI, Higashi K, Hosoya K, Kubota M, Ezura H (1999) Stage- and tissue-specific expression of ethylene receptor homolog genes during fruit development in muskmelon. Plant Physiol 120:321–330PubMedCrossRefGoogle Scholar
  42. Shackel KA, Greve C, Labavitch JM, Ahmadi H (1991) Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiol 97:814–816PubMedCrossRefGoogle Scholar
  43. Shiomi S, Yamamoto M, Nakamura R, Inaba A (1999) Expression of ACC synthase and ACC oxidase genes in melons harvested at different stages of maturity. J Japan Soc Hortic Sci 68:10–17CrossRefGoogle Scholar
  44. Solano R, Stepanova A, Chao Q, Ecker JR (2006) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714CrossRefGoogle Scholar
  45. van Leeuwen H, Monfort A, Zhang HB, Puigdomenech P (2003) Identification and characterisation of a melon genomic region containing a resistance gene cluster from a constructed BAC library. Microcolinearity between Cucumis melo and Arabidopsis thaliana. Plant Mol Biol 51:703–718PubMedCrossRefGoogle Scholar
  46. Vicente AR, Saladié M, Rose JKC, Labavitch JM (2007) The linkage between cell wall metabolism and fruit softening: looking to the future. J Sci Food Agric 87:1435–1448CrossRefGoogle Scholar
  47. 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 296:343–346PubMedCrossRefGoogle Scholar
  48. Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis AJ (2003) Biochemichal diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. Biol Chem 278:49102–49112CrossRefGoogle Scholar
  49. Yamasaki S, Fujii N, Takahashi H (2000) The ethylene-regulated expression of CS-ETR2 and CS-ERS genes in cucumber plants and their possible involvement with sex expression in flowers. Plant Cell Physiol 41:608–616PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Eduard Moreno
    • 1
  • Javier M. Obando
    • 2
  • Noelia Dos-Santos
    • 2
  • J. Pablo Fernández-Trujillo
    • 2
  • Antonio J. Monforte
    • 1
  • Jordi Garcia-Mas
    • 1
  1. 1.IRTA, Centre de Recerca en Agrigenòmica CSIC-IRTA-UABCabrilsSpain
  2. 2.Department of Agricultural and Food EngineeringTechnical University of Cartagena (UPCT), ETSIA and Institute of Plant BiotechnologyCartagena, MurciaSpain

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