Skip to main content
SpringerLink
Log in

The peach HECATE3-like gene FLESHY plays a double role during fruit development

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Tight control of cell/tissue identity is essential for a correct and functional organ patterning, an important component of overall fruit development and eventual maturation and ripening. Despite many investigations regarding the molecular determinants of cell identity in fruits of different species, a useful model able to depict the regulatory networks governing this relevant part of fruit development is still missing. Here we described the peach fruit as a system to link the phenotype of a slow ripening (SR) selection to an altered transcriptional regulation of genes involved in determination of mesocarp cell identity providing insight toward molecular regulation of fruit tissue formation. Morpho-anatomical observations and metabolomics analyses performed during fruit development on the reference cultivar Fantasia, compared to SR, revealed that the mesocarp of SR maintained typical immaturity traits (e.g. small cell size, high amino acid contents and reduced sucrose) throughout development, along with a strong alteration of phenylpropanoid contents, resulting in accumulation of phenylalanine and lignin. These findings suggest that the SR mesocarp is phenotypically similar to a lignifying endocarp. To test this hypothesis, the expression of genes putatively involved in determination of drupe tissues identity was assessed. Among these, the peach HEC3-like gene FLESHY showed a strongly altered expression profile consistent with pit hardening and fruit ripening, generated at a post-transcriptional level. A double function for FLESHY in channelling the phenylpropanoid pathway to either lignin or flavour/aroma is suggested, along with its possible role in triggering auxin-ethylene cross talk at the start of ripening.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Bassi D, Monet R (2008) Botany and taxonomy. In: Layne DR, Bassi D (eds) The peach, botany, production and uses. CAB Intl, Wallingford, pp 1–36

    Chapter  Google Scholar 

  • Begheldo M, Ziliotto F, Rasori A, Bonghi C (2007) The use of μPEACH 1.0 to investigate the role of ethylene in the initiation of peach fruit ripening. In: Ramina A, Chang C, Giovannoni J, Klee H, Perata P, Woltering E (eds) Advances in plant ethylene research. Springer, Berlin, pp 265–267

    Chapter  Google Scholar 

  • Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, Rossetto Pde B, Angenent GC, de Maagd RA (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24:4437–4451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biais B, Allwood JW, Deborde C et al (2009) 1H NMR, GC–EI-TOFMS, and data set correlation for fruit metabolomics, Application to spatial metabolite analysis in melon. Anal Chem 81:2884–2894

    Article  CAS  PubMed  Google Scholar 

  • Bonghi C, Trainotti L, Botton A, Tadiello A, Rasori A, Ziliotto F, Zaffalon V, Casadoro G, Ramina A (2011) A microarray approach to identify genes involved in seed-pericarp cross-talk and development in peach. BMC Plant Biol 11:107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Botton A, Vegro M, De Franceschi F, Ramina A, Gemignani C, Marcer G, Pasini G, Tonutti P (2006) Different expression of Pp-LTP1 and accumulation of Pru p 3 in fruits of two Prunus persica L. Batsch genotypes. Plant Sci 171:106–113

    Article  CAS  Google Scholar 

  • Brecht KJ, Kader AA (1984) Ethylene production by fruit of some slow-ripening nectarine genotypes. J Am Soc Hortic Sci 109:763–767

    CAS  Google Scholar 

  • Brecht KJ, Kader AA, Ramming DW (1984) Description and postharvest physiology of some slow-ripening nectarine genotypes. J Am Soc Hortic Sci 109:509–600

    Google Scholar 

  • Callahan AM, Dardick C, Scorza R (2009) Characterization of ‘Stoneless’, A naturally occurring, partially stoneless plum cultivar. J Am Soc Hortic Sci 134:120–125

    Google Scholar 

  • Carceller M, Davey MR, Fowler MW, Street HE (1971) The influence of sucrose, 2,4-D and kinetin on the growth, fine structure and lignin content of cultured SYCAMORE cells. Protoplasma 73:367–385

    Article  CAS  PubMed  Google Scholar 

  • Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN, Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene group. BMC Genom 9:561

    Article  Google Scholar 

  • Cline MS, Smoot M, Cerami E et al (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2:2366–2382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dardick C, Callahan A (2014) Evolution of the fruit endocarp, molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Front Plant Sci 5:284

    Article  PubMed  PubMed Central  Google Scholar 

  • Dardick CD, Callahan AM, Chiozzotto R, Schaffer RJ, Piagnani MC, Scorza R (2010) Stone formation in peach fruit exhibits spatial coordination of the lignin and flavonoid pathways and similarity to Arabidopsis dehiscence. BMC Biol 8:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Eccher G, Botton A, Di Mauro M, Boschetti A, Ruperti B, Ramina A (2013) Early induction of apple fruitlet abscission is characterized by an increase of both isoprene emission and abscisic acid content. Plant Physiol 161:1952–1969

    Article  CAS  Google Scholar 

  • Eduardo I, Picañol R, Rojas E, Batlle I, Howad W, Aranzana MJ, Arùs P (2015) Mapping of a major gene for the slow ripening character in peach: co-location with the maturity date gene and development of a candidate gene-based diagnostic marker for its selection. Euphytica 205:627–636

    Article  CAS  Google Scholar 

  • El-Sharkawy I, Mila I, Bouzayen M, Jayasankar S (2010) Regulation of two germin-like protein genes during plum fruit development. J Exp Bot 61:1761–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fasoli M, Santo SD, Zenoni S, Tornielli GB et al (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24:3489–3505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrándiz C, Liljegren SJ, Yanofsky MF (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289:436–438

    Article  PubMed  Google Scholar 

  • Ferrándiz C, Fourquin C, Prunet N, Scutt CP, Sundberg E, Trehin C, Vialette-Guiraud ACM (2010) Carpel development. In: Kader JC, Delseny M (eds) Advances in botanical research. Academic Press, Burlington, pp 1–73

    Google Scholar 

  • Ferry-Dumazet H, Gil L, Deborde C, Moing A, Bernillon S, Rolin D, Nikolski M, de Daruvar A, Jacob D (2011) MeRy-B, a web knowledgebase for the storage, visualization, analysis and annotation of plant NMR metabolomic profiles. BMC Plant Biol 11:104

    Article  PubMed  PubMed Central  Google Scholar 

  • Gabotti D, Negrini N, Morgutti S, Nocito FF, Cocucci M (2015) Cinnamyl alcohol dehydrogenases in the mesocarp of ripening fruit of Prunus persica genotypes with different flesh characteristics, changes in activity and protein and transcript levels. Physiol Plantarum 154:329–348

    Article  CAS  Google Scholar 

  • Ghiani A, Onelli E, Aina R, Cocucci M, Citterio S (2011) A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endopolygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. J Exp Bot 62:4043–4054

    Article  CAS  PubMed  Google Scholar 

  • Hagendoorn MJM, Traas TP, Boon JJ, van der Plas LHW (1990) Orthovanadate induced lignin production, in Batch and continuous cultures of Petunia hybrida. J Plant Physiol 137:72–80

    Article  CAS  Google Scholar 

  • Hayama H, Tatsuki M, Yoshioka H, Nakamura Y (2008) Regulation of stony hard peach softening with ACC treatment. Postharvest Biol Technol 50:231–232

    Article  CAS  Google Scholar 

  • Kay P, Groszmann M, Ross JJ, Parish RW, Swain SM (2012) Modifications of a conserved regulatory network involving INDEHISCENT controls multiple aspects of reproductive tissue development in Arabidopsis. New Phytol 197:73–87

    Article  PubMed  Google Scholar 

  • Klie S, Osorio S, Tohge T, Drincovich MF, Fait A, Giovannoni JJ, Fernie AR, Nikoloski Z (2013) Conserved changes in the dynamics of metabolic processes during fruit development and ripening across species. Plant Physiol 164:55–68

    Article  PubMed  PubMed Central  Google Scholar 

  • Knapp S (2002) Tobacco to tomatoes, a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022

    Article  CAS  PubMed  Google Scholar 

  • Kroon PA, Williamson G (1999) Hydroxycinnamates in plants and food, current and future perspectives. J Sci Food Agric 79:355–361

    Article  CAS  Google Scholar 

  • Kumar A, Ellis BE (2003) 4-Coumarate: CoA ligase gene family in Rubus idaeus, cDNA structures, evolution, and expression. Plant Mol Biol 31:327–340

    Article  Google Scholar 

  • Lester DR, Sherman WB, Atwell BJ (1996) Endopolygalacturonase and the melting flesh (M) locus in peach. J Am Soc Hortic Sci 121:231–235

    CAS  Google Scholar 

  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770

    Article  CAS  PubMed  Google Scholar 

  • Liljegren SJ, Roeder AH, Kempin SA, Gremski K, Ostergaard L, Guimil S, Reyes DK, Yanofsky MF (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116:843–853

    Article  CAS  PubMed  Google Scholar 

  • Mack AL (2000) Did fleshy fruit pulp evolve as a defence against seed loss rather as dispersal mechanism? J Biosci 25:93–97

    Article  CAS  PubMed  Google Scholar 

  • Masia A, Zanchin A, Rascio N, Ramina A (1992) Some biochemical and ultrastructural aspects of peach fruit development. J Am Soc Hortic Sci 117:808–815

    CAS  Google Scholar 

  • Moing A, Aharoni A, Biais B et al (2011) Extensive metabolic crosstalk in melon fruit revealed by spatial and developmental combinatorial metabolomics. New Phytol 190:683–696

    Article  CAS  PubMed  Google Scholar 

  • Mounet F, Lemaire-Chamley M, Maucourt M et al (2007) Quantitative metabolic profiles of tomato flesh and seeds during fruit development, complementary analysis with ANN and PCA. Metabolomics 3:273–288

    Article  CAS  Google Scholar 

  • Nuñez-LilloG Cifuentes-Esquivel A, Troggio M et al (2015) Identification of candidate genes associated with mealiness and maturity date in peach [Prunus persica (L.) Batsch] using QTL analysis and deep sequencing. Tree Genet Genomes 11:86

    Article  Google Scholar 

  • Pascual L, Xu J, Biais B et al (2013) Deciphering genetic diversity and inheritance of tomato fruit weight and composition through a systems biology approach. J Exp Bot 64:5737–5752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45–e50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity, BestKeeper–Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515

    Article  CAS  PubMed  Google Scholar 

  • Qiao H, Chang KN, Yazaki J, Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Gene Dev 23:512–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajani S, Sundaresan V (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11:1914–1922

    Article  CAS  PubMed  Google Scholar 

  • Ramming D (1991) Genetic-control of a slow-ripening fruit trait in nectarine. Can J Plant Sci 71:601–603

    Article  Google Scholar 

  • Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10:1507–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruperti B, Bonghi C, Rasori A, Ramina A, Tonutti P (2001) Characterization and expression of two members of the peach 1-aminocyclopropane-1-carboxylate oxidase gene family. Physiol Planturum 111:336–344

    Article  CAS  Google Scholar 

  • Salentijn EMJ, Aharoni A, Schaart JG, Boone MJ, Krens FA (2003) Differential gene expression analysis of strawberry cultivars that differ in fruit firmness. Physiol Plantarum 118:571–578

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. Harbor Laboratory, Cold Spring New York

    Google Scholar 

  • Scutt CP, Vinauger-Douard M, Fourquin C, Finet C, Dumas C (2006) An evolutionary perspective on the regulation of carpel development. J Exp Bot 57:2143–2152

    Article  CAS  PubMed  Google Scholar 

  • Simon P (2003) Q-Gene, processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tao S, Khanizadeh S, Zhang H, Zhang S (2009) Anatomy, ultrastructure and lignin distribution of stone cells in two Pyrus species. Plant Sci 176:413–419

    Article  CAS  Google Scholar 

  • Tataranni G, Spada A, Pozzi C, Bassi D (2010) AFLP-based bulk segregant analysis for tagging the slow-ripening trait in peach [Prunus persica (L.) Batsch]. J Hortic Sci Biotech 85:78–82

    Article  CAS  Google Scholar 

  • Tatsuki M, Haji T, Yamaguchi M (2006) The involvement of 1-aminocyclopropane-1-carboxylic acid synthase isogene, Pp-ACS1, in peach fruit softening. J Exp Bot 57:1281–1289

    Article  CAS  PubMed  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71

    Article  PubMed  PubMed Central  Google Scholar 

  • Tonutti P, Bonghi C, Ruperti B, Tornielli GB, Ramina A (1997) Ethylene evolution and 1-aminocyclopropane-1-carboxylate oxidase gene expression during early development and ripening of peach fruit. J Am Soc Hortic Sci 122:642–647

    CAS  Google Scholar 

  • Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age, the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308

    Article  CAS  PubMed  Google Scholar 

  • Van der Rest B, Danoun S, Boudet A-M, Rochange SF (2006) Down-regulation of cinnamoyl-CoA reductase in tomato (Solanum lycopersicum L.) induces dramatic changes in soluble phenolic pools. J Exp Bot 57:1399–1411

    Article  PubMed  Google Scholar 

  • Varotto S, Locatelli S, Canova S, Pipal A, Motto M, Rossi V (2003) Expression profile and cellular localization of maize rpd3-type histone deacetylases during plant development. Plant Physiol 133:606–617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vendramin E, Pea G, Dondini L et al (2014) A unique mutation in a MYB gene cosegregates with the nectarine phenotype in peach. PLoS One 9(10):e0090574

    Google Scholar 

  • Vrebalov J, Pan IL, Arroyo AJM et al (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21:3041–3062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziliotto F, Begheldo M, Rasori A, Bonghi C, Ramina A, Tonutti P (2005) Molecular and genetic aspects of ripening and qualitative traits in peach and nectarine fruits. Acta Hortic 682:237–246

    Article  CAS  Google Scholar 

  • Ziliotto F, Corso M, Rizzini FM, Rasori A, Botton A, Bonghi C (2012) Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin- and ethylene-related genes. BMC Plant Biol 12:185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This article is dedicated to the memory of our friend and colleague Angelo Ramina. We thank Daniel Jacob for developing and maintaining MeRy-B knowledge base and database. This research was financially supported by Project ex60 % (2013 and 2014) funded by the University of Padova.

Authors’ contributions

Claudio Bonghi conceived the study. Angela Rasori and Fiorenza Ziliotto made the molecular analyses, while Anna Petterle performed the histochemical assessments and microscopic analyses. Annick Moing, Stéphane Bernillon, Catherine Deborde and Mickaël Maucourt supervised and carried out the metabolomic analyses together with Angela Rasori and performed the related data mining. Alessandro Botton carried out the bioinformatic and statistical analyses and prepared the graphics. Serena Varotto gave useful advices and contributed to experiments. Claudio Bonghi and Alessandro Botton interpreted the results and wrote the paper.

Author information

Authors and Affiliations

  1. Department of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padova, viale dell’Università, 16, Agripolis, 35020, Legnaro, Italy

    Alessandro Botton, Angela Rasori, Fiorenza Ziliotto, Anna Petterle, Serena Varotto & Claudio Bonghi

  2. UMR1332 Biologie du Fruit et Pathologie, INRA, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Annick Moing, Stéphane Bernillon & Catherine Deborde

  3. Plateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, MetaboHUB, IBVM, Centre INRA Bordeaux, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Annick Moing, Mickaël Maucourt, Stéphane Bernillon & Catherine Deborde

  4. UMR1332 Biologie du Fruit et Pathologie, University of Bordeaux, 71 av Edouard Bourlaux, 33140, Villenave d’Ornon, France

    Mickaël Maucourt

Authors
  1. Alessandro Botton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Rasori
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fiorenza Ziliotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Annick Moing
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mickaël Maucourt
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stéphane Bernillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Catherine Deborde
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anna Petterle
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Serena Varotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Claudio Bonghi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudio Bonghi.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Botton, A., Rasori, A., Ziliotto, F. et al. The peach HECATE3-like gene FLESHY plays a double role during fruit development. Plant Mol Biol 91, 97–114 (2016). https://doi.org/10.1007/s11103-016-0445-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-016-0445-z

Keywords

Search

Navigation