Skip to main content
SpringerLink
Log in

Expression of auxin-binding protein1 during plum fruit ontogeny supports the potential role of auxin in initiating and enhancing climacteric ripening

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Auxin-binding protein1 (ABP1) is an active element involved in auxin signaling and plays critical roles in auxin-mediated plant development. Here, we report the isolation and characterization of a putative sequence from Prunus salicina L., designated PslABP1. The expected protein exhibits a similar molecular structure to that of well-characterized maize-ABP1; however, PslABP1 displays more sequence polarity in the active-binding site due to substitution of some crucial amino-acid residues predicted to be involved in auxin-binding. Further, PslABP1 expression was assessed throughout fruit ontogeny to determine its role in fruit development. Comparing the expression data with the physiological aspects that characterize fruit-development stages indicates that PslABP1 up-regulation is usually associated with the signature events that are triggered in an auxin-dependent manner such as floral induction, fruit initiation, embryogenesis, and cell division and elongation. However, the diversity in PslABP1 expression profile during the ripening process of early and late plum cultivars seems to be due to the variability of endogenous auxin levels among the two cultivars, which consequently can change the levels of autocatalytic ethylene available for the fruit to co-ordinate ripening. The effect of auxin on stimulating ethylene production and in regulating PslABP1 was investigated. Our data suggest that auxin is involved in the transition of the mature green fruit into the ripening phase and in enhancing the ripening process in both auxin- and ethylene-dependent manners thereafter.

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

Similar content being viewed by others

Abbreviations

ABP1:

Auxin-binding protein1

DAB:

Days after bloom

‘EG’:

‘Early Golden’

‘SH’:

‘Shiro’

S1–4:

Stage 1–4

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anai T, Miyata M, Kosemura S, Yamamura S, Tsuge T, Matsui M, Uchida H, Hasegawa K (1997) Comparison of abp1 primary sequences from monocotyledonous and dicotyledonous species. J Plant Physiol 151:446–449

    Article  CAS  Google Scholar 

  • Augustí M, Almela V, Andreu I, Juan M, Zacarias L (1999) Synthetic auxin 3,5,6-TPA promotes fruit development and climacteric in Prunus persica L. Batsch. J Hort Sci Biotech 74:556–560

    Google Scholar 

  • Bauly JM, Sealy IM, Macdonald H, Brearley J, Droge S, Hilmer S, Robinson DG, Venis MA, Blatt MR, Lazarus CM, Napier RM (2000) Overexpression of ABP1 heightens the sensitivity of guard cells to auxin. Plant Physiol 124:1229–1238

    Article  PubMed  CAS  Google Scholar 

  • Biale JB, Young RE (1981) Respiration and ripening in fruits-retrospect and prospect. In: Journal Friend, Rhodes MJC (eds) Recent advances in the biochemistry of fruits and vegetables. Academic Press, London, pp 1–39

    Google Scholar 

  • Bregoli AM, Fabbroni C, Costa F, Raimondi V, Costa G (2007) Auxin and ethylene interaction during fruit growth and ripening of Actinidia deliciosa. In: Ramina A, Chang C, Giovannoni J, Klee H, Perata P, Woltering E (eds) Advances in plant ethylene research: proceedings of the 7th international symposium on the plant hormone ethylene. Springer, Berlin, pp 105–107

    Google Scholar 

  • Chen JG, Shimomura S, Sitbon F, Sandberg G, Jones AM (2001) The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. Plant J 28:607–617

    Article  PubMed  CAS  Google Scholar 

  • Chen JG, Ullah H, Young JC, Sussman MR, Jones AM (2011) ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev 15:902–911

    Article  Google Scholar 

  • Christian M, Steffens B, Schenck D, Burmester S, Böttger M, Lüthen H (2006) How does auxin enhance cell elongation? Roles of auxin-binding proteins and potassium channels in growth control. Plant Biol 8:346–352

    Article  PubMed  CAS  Google Scholar 

  • David KM, Carnero-Diaz E, Leblanc N, Monestiez M, Grosclaude J, Perrot-Rechenmann C (2001) Conformational dynamics underlie the activity of the auxin-binding protein, Nt-abp1. J Biol Chem 276:34517–34523

    Article  PubMed  CAS  Google Scholar 

  • David KM, Couch D, Braun N, Brown S, Grosclaude J, Perrot-Rechenmann C (2007) The auxin-binding protein 1 is essential for the control of cell cycle. Plant J 50:197–206

    Article  PubMed  CAS  Google Scholar 

  • Davies PJ (2004) Plant hormones: biosynthesis, signal transduction, action. Kluwer, Dordrecht

    Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Dunwell JM, Khuri S, Gane PJ (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev 64:153–179

    Article  PubMed  CAS  Google Scholar 

  • El-Sharkawy I, Kim WS, El-Kereamy A, Jayasankar S, Svircev AM, Brown DCW (2007) Isolation and characterization of four ethylene signal transduction elements in plums (Prunus salicina L.). J Exp Bot 58:3631–3643

    Article  PubMed  CAS  Google Scholar 

  • El-Sharkawy I, Kim WS, Jayasankar S, Svircev AM, Brown DCW (2008) Differential regulation of four members of ACC synthase gene family in plum. J Exp Bot 59:2009–2027

    Article  PubMed  CAS  Google Scholar 

  • El-Sharkawy I, Sherif S, Mila I, Bouzayen M, Jayasankar S (2009) Molecular characterization of seven genes encoding ethylene-responsive transcriptional factors during plum fruit development and ripening. J Exp Bot 60:907–922

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • El-Sharkawy I, El Kayal W, Prasath D, Fernández H, Bouzayen M, Svircev AM, Jayasankar S (2012) Identification and genetic characterization of a gibberellin 2-oxidase gene that controls the tree stature and reproductive growth in plum. J Exp Bot 63:1225–1239

    Article  PubMed  CAS  Google Scholar 

  • Feckler C, Muster G, Feser W, Römer A, Palme K (2001) Mass spectrometric analysis reveals a cysteine bridge between residues 2 and 61 of the auxin-binding protein 1 from Zea mays L. FEBS Lett 509:446–450

    Article  PubMed  CAS  Google Scholar 

  • Friml J (2003) Auxin transport-shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180

    Article  PubMed  CAS  Google Scholar 

  • Hertel R, Thomson K, Russo VEA (1972) In vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta 107:325–340

    Article  CAS  Google Scholar 

  • Hou ZX, Huang WD (2005) Immunohistochemical localization of IAA and ABP1 in strawberry shoot apexes during floral induction. Planta 222:678–687

    Article  PubMed  CAS  Google Scholar 

  • Jones AM (1994) Auxin-binding proteins. Annu Rev Plant Physiol Plant Mol Biol 45:393–420

    Article  CAS  Google Scholar 

  • Jones AM, Herman EM (1993) KDEL-containing auxin-binding protein is secreted to the plasma membrane and cell wall. Plant Physiol 101:595–606

    PubMed  CAS  Google Scholar 

  • Jones AM, Im KH, Savka MA, Wu MJ, DeWitt NG, Shillito R, Binns AN (1998) Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282:1114–1117

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Kim YS, Kim D, Jung J (2000) Two isoforms of soluble auxin receptor in rice (Oryza sativa L.) plants: binding property for auxin and interaction with plasma membrane H+ -TPase. Plant Growth Regul 32:143–150

    Article  CAS  Google Scholar 

  • Kukuruzinska MA, Lennon K (1998) Protein N-glycosylation: molecular genetics and functional significance. Crit Rev Oral Biol Med 9:415–448

    Article  PubMed  CAS  Google Scholar 

  • Lang A (1961) Auxins in flowering. Encycl Plant Physiol 14:909–950

    Google Scholar 

  • Lazarus CM, MacDonald H (1996) Characterization of a strawberry gene for auxin-binding protein, and its expression in insect cells. Plant Mol Biol 31:267–277

    Article  PubMed  CAS  Google Scholar 

  • Leblanc N, Roux C, Pradier JM, Perrot-Rechenmann C (1997) Characterization of two cDNAs encoding auxin-binding proteins in Nicotiana tabacum. Plant Mol Biol 33:679–689

    Article  PubMed  CAS  Google Scholar 

  • Leblanc N, David K, Grosclaude J, Pradier JM, Barbier-Brygoo H, Labiau S, Perrot-Rechenmann C (1999) A novel immunological approach establishes that the auxin-binding protein, Nt-abp1, is an element involved in auxin signaling at the plasma membrane. J Biol Chem 274:28314–28320

    Article  PubMed  CAS  Google Scholar 

  • Lelièvre JM, Latché A, Jones B, Bouzayen M, Pech JC (1997) Ethylene and fruit ripening. Physiol Plant 101:727–739

    Article  Google Scholar 

  • Litz RE, Gray DJ (1992) Organogenesis and somatic embryogenesis. In: Hammerschlag FA, Litz RE (eds) Biotechnology of perennial fruit crops. Academic Press, London, pp 3–34

    Google Scholar 

  • Löbler M, Klämbt D (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.): purification by immunological methods and characterization. J Biol Chem 260:9848–9853

    PubMed  Google Scholar 

  • Lüthen H, Claussen M, Böttger M (1999) Growth: progress in auxin research. Prog Bot 60:315–340

    Article  Google Scholar 

  • Meisel L, Fonseca B, González S, Baezayates R, Cambiazo V, Campos R, Gonzalez M, Orellana A, Retamales J, Silva H (2005) A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 38:83–88

    Article  PubMed  CAS  Google Scholar 

  • Miller AN, Walsh CS, Cohen JD (1987) Measurement of Indole-3-Acetic Acid in peach fruits (Prunus persica L. Batsch cv Redhaven) during development. Plant Physiol 84:491–494

    Article  PubMed  CAS  Google Scholar 

  • Napier RM (1997) Trafficking of the auxin-binding protein. Trends Plant Sci 2:251–255

    Article  Google Scholar 

  • Napier RM (2001) Models of auxin binding. J Plant Growth Regul 20:244–254

    Article  CAS  Google Scholar 

  • Napier RM, Venis MA (1995) Tansley review No 79: auxin action and auxin-binding proteins. New Phytol 129:167–201

    Article  CAS  Google Scholar 

  • Napier RM, David KM, Perrot-Rechenmann C (2002) A short history of auxin-binding proteins. Plant Mol Biol 49:339–348

    Article  PubMed  CAS  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, Heijne GV (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  CAS  Google Scholar 

  • Ohmiya A (2000) Effects of auxin on growth and ripening of mesocarp discs of peach fruit. Sci Hort 84:309–319

    Article  CAS  Google Scholar 

  • Ohmiya A, Motoyuki K, Sakai S, Hayashi T (1993) Purification and properties of an auxin-binding protein from the shoot apex of peach tree. Plant Cell Physiol 34:177–183

    CAS  Google Scholar 

  • Quint M, Gray WM (2006) Auxin signaling. Curr Opin Plant Biol 9:448–453

    Article  PubMed  CAS  Google Scholar 

  • Scherer FEG (2011) AUXIN-BINDING-PROTEIN1, the second auxin receptor: what is the significance of a two-receptor concept in plant signal transduction? J Exp Bot 62:3339–3357

    Article  PubMed  CAS  Google Scholar 

  • Shimomura S, Watanabe S, Ichikawa H (1999) Characterization of auxin-binding protein 1 from tobacco: content, localization and auxin-binding activity. Planta 209:118–125

    Article  PubMed  CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  PubMed  CAS  Google Scholar 

  • Thomas C, Meyer D, Wolff M, Himber C, Alioua M, Steinmetz A (2003) Molecular characterization and spatial expression of the sunflower ABP1 gene. Plant Mol Biol 52:1025–1036

    Article  PubMed  CAS  Google Scholar 

  • Thornton JM (1981) Disulphide bridges in globular proteins. J Mol Biol 151:261–287

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Tromas A, Braun N, Muller P, Khodus T, Paponov IA, Palme K, Ljung K, Lee JY, Benfey P, Murray JAH, Scheres B, Perrot-Rechenmann C (2009) The auxin binding protein 1 is required for differential auxin responses mediating root growth. PLoS One 4:e6648. doi:10.1371/journal.pone.0006648

    Article  PubMed  Google Scholar 

  • Varki A (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiol 3:97–130

    Article  CAS  Google Scholar 

  • Woo EJ, Marshall J, Bauly J, Chen JG, Venis M, Napier RM, Pickersgill RW (2002) Crystal structure of auxin-binding protein 1 in complex with auxin. EMBO J 21:2877–2885

    Article  PubMed  CAS  Google Scholar 

  • Yin K, Han X, Xu Z, Xue H (2009) Arabidopsis GLP4 is localized to the Golgi and binds auxin in vitro. Acta Biochim Biophys Sin (Shanghai) 6:478–487

    Article  Google Scholar 

  • Ziliotto F, Begheldo M, Rasori A, Bonghi C, Tonutti B (2008) Transcriptome profiling of ripening nectarine (Prunus persica L. Batsch) fruit treated with 1-MCP. J Exp Bot 59:2781–2791

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Agriculture, University of Guelph, 4890 Victoria Av. N, P.O. Box 7000, Vineland Station, ON, L0R 2E0, Canada

    I. El-Sharkawy, S. Sherif, K. Abubaker & S. Jayasankar

  2. Faculty of Agriculture, Damanhour University, Damanhour, Egypt

    I. El-Sharkawy & S. Sherif

  3. Department of Biological Sciences, Brock University, 500 Glenridge Av., St Catharines, ON, L2S 3A1, Canada

    A. Mahboob

  4. UMR 990 INRA/INPT-ENSAT “Génomique et Biotechnologie des Fruits”, Av. de l’Agrobiopole, BP 32607, 31326, Castanet-Tolosan Cedex, France

    M. Bouzayen

Authors
  1. I. El-Sharkawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Sherif
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Mahboob
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Abubaker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Bouzayen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. Jayasankar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Jayasankar.

Additional information

Communicated by P. Kumar.

Rights and permissions

Reprints and permissions

About this article

Cite this article

El-Sharkawy, I., Sherif, S., Mahboob, A. et al. Expression of auxin-binding protein1 during plum fruit ontogeny supports the potential role of auxin in initiating and enhancing climacteric ripening. Plant Cell Rep 31, 1911–1921 (2012). https://doi.org/10.1007/s00299-012-1304-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-012-1304-2

Keywords

Search

Navigation