Skip to main content
Log in

Map position and functional allelic diversity of Md-Exp7, a new putative expansin gene associated with fruit softening in apple (Malus × domestica Borkh.) and pear (Pyrus communis)

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Fruit ripening can be considered as a complex set of biochemical and physiological changes occurring at the end of the developmental stage. Ripe fruit texture notably affects overall quality and consumer appreciation. Excessive softening limits shelf-life and storability, thereby increasing disease susceptibility and economic loss. Fruit softening is a process due to the depolymerisation of different polysaccharide classes, an event controlled by a synergic and coordinated action of several enzymes among which expansins play a fundamental role. To date, six expansin genes are known to be expressed during apple fruit ontogeny, from full bloom up to fruit ripening. We identified a novel expansin apple homolog (Md-Exp7) sharing high sequence similarity with specific-ripening expansin genes of other crops. A functional marker (Md-Exp7SSR) based on an SSR motif located within the untranslated region of the gene was developed and mapped on Linkage Group 1 of the apple and pear genomes in a region where one major apple QTL for fruit firmness had been previously identified. The allelic composition of 31 apple varieties for the SSR marker was associated with differences in fruit softening.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bao JS, Corke H, Sun M (2002) Microsatellites in starch-synthesizing genes in relation to starch physicochemical proprieties in waxy rice (Oryza sativa L.). Theor Appl Genet 105:898–905

    Article  PubMed  CAS  Google Scholar 

  • Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    Article  PubMed  CAS  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–340

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2000a) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2000b) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78

    Article  PubMed  CAS  Google Scholar 

  • Costa F, Stella S, Van de Weg WE, Guerra W, Cecchinel M, Dallavia J, Koller B, Sansavini S (2005) Role of the genes Md-ACO1 and Md-ACS1 in ethylene production and shelf life of apple (Malus domestica Borkh). Euphytica 141:181–190

    Article  CAS  Google Scholar 

  • Devic M, Albert S, Delseny M, Roscoe TJ (1997) Efficient PCR walking on plant genomic DNA. Plant Physiol Biochem 35:331–339

    CAS  Google Scholar 

  • Dondini L, Pierantoni L, Gaiotti F, Chiodini R, Tartarini S, Bazzi C, Sansavini S (2004) Identifying QTLs for fire-blight resistance via a European pear (Pyrus communis L.) genetic linkage map. Mol Breed 14:407–418

    Article  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1989) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Fujimori S, Washio T, Higo K, Ohtomo Y, Murakami K, Matsubara K, Kawai J, Carninci P, Hayashizaki Y, Kikuchi S, Tomita M (2003) A novel feature of microsatellites in plants: a distribution gradient along the direction of transcription. FEBS Letters 554:17–22

    Article  PubMed  CAS  Google Scholar 

  • Gao ZS, Van de Weg WE (2006) The Vf gene for scab resistance in apple is linked to sub-lethal genes. Euphytica 153:123–132

    Article  Google Scholar 

  • Gianfranceschi L, Soglio V (2004) The European project HiDRAS: innovative multidisciplinary approaches to breeding high quality disease resistant apples. Acta Hort 663:327–330

    Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol 52:725–49

    Article  PubMed  CAS  Google Scholar 

  • Harada T, Sunako T, Wakasa Y, Soejima J, Satoh T, Niizeki M (2000) An allele of the 1-aminocyclopropane-1-carboxylate synthase gene (Md-ACS1) accounts for the low level of ethylene production in climacteric fruits of some apple cultivars. Theor Appl Genet 101:742–746

    Article  CAS  Google Scholar 

  • Harrison EP, McQueen-Mason SJ, Manning K (2001) Expression of six expansin genes in relation to extension activity in developing strawberry fruit. J Exp Bot 52:1437–1446

    Article  PubMed  CAS  Google Scholar 

  • Hiwasa K, Rose JKC, Nakano R, Inaba A, Kubo Y (2003) Differential expression of seven a-expansin genes during growth and ripening of pear fruit. Physiologia Plantarum 117:564–572

    Article  PubMed  CAS  Google Scholar 

  • Hough LF, Shay JR, Dayton DF (1953) Apple scab resistance from Malus floribunda Sieb. Proc Am Soc Hortic Sci 62:341–347

    Google Scholar 

  • Iglesias AR, Kindlund E, Tammi M, Wadelius C (2004) Some microsatellites may act as novel polymorphic cis-regulatory elements through transcription factor binding. Gene 341:149–165

    Article  PubMed  CAS  Google Scholar 

  • King GJ, Alston FH, Brown LM, Chevreau E, Evans KM, Dunemann F, Janse J, Laurens F, Lynn JR, Maliepaard C, Manganaris AG, Roche P, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink R (1998) Multiple field and glasshouse assessments increase the reliability of linkage mapping of the Vf source of scab resistance in apple. Theor Appl Gen 96:699–708

    Article  CAS  Google Scholar 

  • King GJ, Tartarini S, Brown L, Gennari F, Sansavini S (1999) Introgression of the Vf source of scab resistance and distribution of linked marker alleles within the Malus gene pool. Theor Appl Genet 99:1039–1046

    Article  CAS  Google Scholar 

  • King GJ, Maliepaard C, Lynn JR, Alston FH, Durel CE, Evans KM, Griffon B, Laurens F, Manganars AG, Schrevens E, Tartarini S, Verhaegh J (2000) Quantitative genetics analysis and comparison of physical and sensory descriptors to fruit flesh firmness in apple (Malus pupila Mill.). Theor Appl Genet 100:1074–1084

    Article  Google Scholar 

  • King GJ, Lynn JR, Dover CJ, Evans KM, Seymour GB (2001) Resolution of quantitative trait loci for mechanical measures accounting for genetic variation in fruit texture of apple (Malus pumila Mill.). Theor Appl Genet 102:1227–1235

    Article  CAS  Google Scholar 

  • Li Y, Darley CP, Onagro V, Fleming A, Schipper O, Baldauf SL, Mc-Queen-Mason SJ (2002) Plant expansin are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128:854–864

    Article  PubMed  CAS  Google Scholar 

  • Li YC, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007

    Article  PubMed  CAS  Google Scholar 

  • Maliepaard C, Alston FH, Van Arkel G, Brown LM, Chevreau E, Dunemann F, Evans KM, Gardiner S, Guilford P, Van Heusden AW, Janse J, Laurens F, Lynn JR, Manganaris AG, den Nijs APM, Periam N, Rikkerink E, Roche P, Ryder C, Sansavini S, Schmidt H, Tartarini S, Verhaegh JJ, Vrielink-van Ginkel M, King GJ (1998) Aligning male and female linkage maps of apple (Malus pumila Mill.) using multi-allelic markers. Theor Appl Genet 97:60–73

    Article  CAS  Google Scholar 

  • Maliepaard C, Sillanpaa MJ, van Ooijen JW, Jansen RC, Arjas E (2001) Bayesian versus frequentist analysis of multiple quantitative trait loci with an application to an outbred apple corss. Theor Appl Genet 103:1243–1253

    Article  CAS  Google Scholar 

  • Morgante M, Hanafey M, Powell W (2002) Microsatellite are preferentially associated wit nonrepetitive DNA in plant genomes. Nat Genet 302:194–200

    Article  Google Scholar 

  • Oraguzie NC, Iwanami H, Soejima J, Harada T, Hall A (2004) Inheritance of the Md-ACS1 gene and its relationship to fruit softening in apple (Malus × domestica Borkh.). Theor Appl Genet 108:1526–1533

    Article  PubMed  CAS  Google Scholar 

  • Oraguzie NC, Volz RK, Whitworth CJ, Bassett HCM, Hall AJ, Gardiner SE (2007) Influence of Md-ACS1 allelotype and harvest season within an apple germplasm collection on fruit softening during cold air storage. Postharvest Biol Techn 44:212–219

    Article  CAS  Google Scholar 

  • Pierantoni L, Cho KH, Shin IS, Chiodini R, Tartarini S, Dondini L, Kang SJ, Sansavini S (2004) Characterization and transferability of apple SSRs to two European pear F1 populations. Theor Appl Genet 109:1519–1524

    Article  PubMed  CAS  Google Scholar 

  • Powell ALT, Kalamaki MS, Kurien PA, Guerrieri S, Bennett AB (2003) Simultaneous transgeninc suppression of LePG and LeExp1 influences fruit texture and juice viscosity in a fresh market tomato variety. J Agric Food Chem 51:7450–7455

    Article  PubMed  CAS  Google Scholar 

  • Rose JKC, Lee HH, Bennett AB (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. PNAS 94:5955–5960

    Article  PubMed  CAS  Google Scholar 

  • Rose JKC, Hadfield KA, Labavitch JM, Bennett AB (1998) Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol 117:345–361

    Article  PubMed  CAS  Google Scholar 

  • Seymour GB, Manning K, Eriksson EM, Popovich AH, King GJ (2002) Genetic identification and genomic organization of factors affecting fruit texture. J Ex Bot 53:2065–2071

    Article  CAS  Google Scholar 

  • Silfverberg-Dilworth E, Matasci C, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.). Tree Genet Gen 2:202–224

    Article  Google Scholar 

  • Sunako T, Sakuraba W, Senda M, Akada S, Ishikawa R, Niizeki M, Harada T (1999) An allele of the ripening-specific 1-amino-cyclopropane-1-carboxylic acid synthase gene (ACS1) in apple fruit with a long storage life. Plant Physiol 119:1297–1303

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW, Voorrips RE (2001) JoinMapÒ Version 3.0, Software for the calculation of genetic linkage maps. Plant Research International, Wageningen, The Netherlands

    Google Scholar 

  • Van Ooijen JW (2004) MapQTL®5, Software for the mapping of quantitative trait loci in experimental populations. Kyazma, Wageningen, The Netherlands

    Google Scholar 

  • Voorrips RE (2001) MapChart version 2.0: Windows software for the graphical presentation of linkage maps and QTLs. Plant Research International, Wageningen, The Netherlands

    Google Scholar 

  • Wakasa Y, Hatsuyama Y, Takahashi A, Sato T, Niizeki M, Harada T (2003) Divergent expression of six expansin genes during apple fruit ontogeny. Eur. J. Hort. Sci. 68:253–259

    CAS  Google Scholar 

  • Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:1–18

    Google Scholar 

  • Yamamoto T, Saito T, Kotobuki K, Matsuta N, Liebhard R, Gessler C, Van de Weg WE, Hayashi T (2004) Genetic linkage maps of Japanese and European pears aligned to the apple consensus map. Acta Hort 663:51–56

    CAS  Google Scholar 

  • Zhang L, Yuan D, Yu S, Li Z, Cao Y, Miao Z, Qian H, Tang K (2004) Preference of simple sequence repeats in coding and non-coding regions of Arabidopsis thaliana. Bioinformatics 20:1081–1086

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Zuo K, Zhang F, Cao Y, Wang J, Zhang Y, Sun X, Tang K (2006) Conservation of noncoding microsatellites in plants: implication for gene regulation. BMC Genomics 7:323–337

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study has been carried out with financial support from the Commission of the European Communities, specific research program “Quality of Life and Management of Living Resource”, QLK5-2002-01492 “High quality Disease Resistant Apple for a Sustainable Agriculture”. This manuscript does not necessarily reflect the Commission’s views and in no way anticipates its future policy in this area. Its content is the sole responsibility of the publishers.

We acknowledge C. Maliepaard for making available fruit firmness data of the cross Prima × Fiesta. The author wishes to thank the anonymous reviewers for providing stimulating, thoughtful and constructive comments to this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Costa.

Additional information

Communicated by P. Arús

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costa, F., Van de Weg, W.E., Stella, S. et al. Map position and functional allelic diversity of Md-Exp7, a new putative expansin gene associated with fruit softening in apple (Malus × domestica Borkh.) and pear (Pyrus communis). Tree Genetics & Genomes 4, 575–586 (2008). https://doi.org/10.1007/s11295-008-0133-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-008-0133-5

Keywords

Navigation