Skip to main content
Log in

Hormonal regulation during plant fruit development

  • Biology of Plant Development
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The modern concept of the hormonal regulation of fruit set, growth, maturation, and ripening is considered. Pollination and fertilization induce ovule activation by surmounting the blocking action of ethylene and ABA to be manifested in auxin accumulation. Active fruit growth by pericarp cell division and elongation is due to the syntheses of auxin in the developing seed and of gibberellins in the pericarp. In climacteric fleshy fruits, the maturation is controlled by ethylene via so-called System 1 combining the possibilities of autoinhibition and autocatalysis by ethylene of its own biosynthesis. Transition of tomato fruits from maturation to ripening is characterized by highly active synthesis of ethylene and its receptors due to the functioning of regulatory System 2 resulting in the up-regulation of much greater number of ethylene-inducible genes. In peach fruits, the hormonal regulation of ripening includes also an active auxin involvement in the ethylene biosynthesis, which is combined with the ethylene-induced expression of genes encoding both auxin biosynthesis and the response to auxin. Ethylene induces the expression of genes responsible for the fruit softening, its taste, color, and flavor. Nonclimacteric fleshy fruits produce very small amounts of ethylene; its evolution increases only by the very end of ripening and can be described by a reduced System 1. The ripening of nonclimacteric fruits only weakly depends on ethylene but is stimulated by abscisic acid.

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.

Similar content being viewed by others

References

  • Alexander, L. and Grierson, D., Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening, J. Exp. Bot., 2002, vol. 53, pp. 2039–2055.

    Article  CAS  PubMed  Google Scholar 

  • Bonghi, C., Trainotti, L., Botton, A., et al., A microarray approach to identify genes involved in seed-pericarp cross-talk and development in peach, BMC Plant Biol., 2011, vol. 11, pp. 107–121.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chai, Y.M., Jia, H.F., Li, C.L., et al., FaPYR1 is involved in strawberry fruit ripening, J. Exp. Bot., 2011, vol. 62, pp. 5079–5089.

    Article  CAS  PubMed  Google Scholar 

  • Dorcey, E., Urbez, C., Blazquez, M.A., et al., Fertilizationdependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis, Plant J., 2009, vol. 58, pp. 318–332.

    Article  CAS  PubMed  Google Scholar 

  • Emery, R.J.N., Ma, Q., and Atkins, C.A., The forms and sources of cytokinins in developing white lupine seeds and fruits, Plant Physiol., 2000, vol. 123, pp. 1593–1604.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Epstein, E., Cohen, J.D., and Solvin, J.P., The biosynthetic pathway for indole-3-acetic acid changes during tomato fruit development, Plant Growth Regul., 2002, vol. 38, pp. 15–20.

    Article  CAS  Google Scholar 

  • Fernandez-Otero, C., Matilla, A.J., Rasori, A., et al., Regulation of ethylene biosynthesis in reproductive organs of damson plum (Prunus domestica L. subsp. syriaca), Plant Sci., 2006, vol. 171, pp. 74–83.

    Article  CAS  Google Scholar 

  • Fernandez-Otero, C.I., de la Torre, F., Iglesias, R., et al., Stage- and tissue-expression of genes involved in the biosynthesis and signaling of ethylene in reproductive organs of damson plum (Prunus domestica L. subsp. insititia), Plant Physiol. Biochem., 2007, vol. 45, pp. 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Martinez, J.L., Santos, C., Crocker, S.J., et al., Identification, quantitation and distribution of gibberellins in fruits of Pisum sativum L., cv. Alaska during pod development, Planta, 1991, vol. 184, pp. 53–60.

    Article  CAS  PubMed  Google Scholar 

  • Goetz, M., Hooper, L.C., Johnson, S.D., et al., Expression of aberrant forms of ARF8 stimulates parthenocarpy in Arabidopsis and tomato, Plant Physiol., 2007, vol. 145, pp. 351–366.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harpster, M.H., Brummel, D.A., and Dunsmuir, P., Expression analysis of a ripening-specific, auxinrepressed endo-1,4-beta-glucanase gene in strawberry, Plant Physiol., 1998, vol. 118, pp. 1307–1316.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hays, D.B., Yeung, E.C., and Pharis, R.P., The role of gibberellins in embryo axis development, J. Exp. Bot., 2002, vol. 53, no. 375, pp. 1747–1751.

    Article  CAS  PubMed  Google Scholar 

  • Janetta, P.P.M., Laarhoven, L.-J., Medina-Escobar, N., et al., Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit, Physiol. Plant., 2006, vol. 127, pp. 247–259.

    Article  Google Scholar 

  • Jia, H.-F., Chai, Y.-M., Li, C.-L., et al., Abscisic acid plays an important role in the regulation of strawberry fruit ripening, Plant Physiol., 2011, vol. 157, pp. 188–199.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang, Y. and Fu, J., Ethylene regulation of fruit ripening: molecular aspects, Plant Growth Regul., 2000, vol. 30, pp. 193–200.

    Article  CAS  Google Scholar 

  • Johnstone, M.M.G., Reinecke, D.M., and Ozga, J.A., The auxins, IAA and 4-Cl-IAA differentially modify gibberellin action via ethylene response in developing pea fruits, J. Plant Growth Regul., 2005, vol. 24, pp. 214–225.

    Article  CAS  Google Scholar 

  • de Jong, M., Mariani, C., and Vriezen, H., The role of auxin and gibberellin in tomato fruit set, J. Exp. Bot., 2009, vol. 60, pp. 1523–1532.

    Article  PubMed  Google Scholar 

  • Klee, H.J. and Clark, D.G., Ethylene signal transduction in fruit and flowers, in Plant Hormones: Biosynthesis, Signal Transduction, Action, Davies, P.J., Ed., Dordrecht: Kluwer Acad. Publ., 2004, pp. 369–390.

    Google Scholar 

  • Klee, H.J. and Giovannoni, J.J., Genetics and control of tomato fruit ripening and quality attributes, Annu. Rev. Genet., 2011, vol. 45, pp. 41–59.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, R., Tyagi, A.K., and Sharma, A.K., Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development, Mol. Genet. Genomics, 2011, vol. 285, pp. 245–260.

    Article  CAS  PubMed  Google Scholar 

  • Lemaire-Chamley, M., Petit, G., Garcia, V., et al., Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato, Plant Physiol., 2005, vol. 139, pp. 750–769.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu, D.-J., Chen, J.-Y., and Lu, W.-J., Expression and regulation of the early auxin-responsive Aux/IAA genes during strawberry fruit development, Mol. Biol. Rep., 2011, vol. 38, pp. 1187–1192.

    Article  CAS  PubMed  Google Scholar 

  • Manning, K., Tor, M., Poole, M., et al., A naturally occurring epigenetic mutation in a gene encoding an SBPbox transcription factor inhibits tomato fruit ripening, Nat. Genet., 2006, vol. 38, pp. 948–952.

    Article  CAS  PubMed  Google Scholar 

  • Mapelli, S.C., Frova, C., Torti, G., et al., Relationship between set, development and activities of growth regulators in tomato fruits, Plant Cell Physiol., 1978, vol. 19, pp. 1281–1288.

    CAS  Google Scholar 

  • Marti, E., Orzaez, D., Ellul, P., et al., Silencing of DELLA induces facultative parthenocarpy in tomato fruits, Plant J., 2007, vol. 52, pp. 865–876.

    Article  CAS  PubMed  Google Scholar 

  • Marty, I., Bureau, S., Sarkissian, S., et al., Ethylene regulation of carotenoid accumulation and carotenogenic gene expression in color-contrasted apricot varieties (Prunus armeniaca), J. Exp. Bot., 2005, vol. 56, pp. 1877–1886.

    Article  CAS  PubMed  Google Scholar 

  • Moussa, H.R. and Salem, A.A.K., Parthenocarpy of watermelon cultivars induced by γ-irradiation, Russ. J. Plant Physiol., 2010, vol. 57, no. 4, pp. 574–581.

    Article  CAS  Google Scholar 

  • Nakatsuka, A., Murachi, S., Okunishi, H., et al., Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening, Plant Physiol., 1998, vol. 118, pp. 1295–1305.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ozga, J.A., Reinecke, D.M., Ayele, B.T., et al., Developmental and hormonal regulation of gibberellin biosynthesis and catabolism in pea fruit, Plant Physiol., 2009, vol. 150, pp. 448–462.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pech, J.-C., Purgatto, E., Bouzayen, M., et al., Ethylene and fruit ripening, Ann. Plant Rev., 2012, vol. 44, pp. 275–304.

    Article  CAS  Google Scholar 

  • Rieu, I., Ericksson, S., and Powers, S.J., et al., Genetic analysis reveals that C19 GA2-oxidation is a major gibberellin inactivation pathway in Arabidopsis, Plant Cell, 2008, vol. 20, pp. 2420–2436.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schaffer, R.J., Ireland, H.S., Ross, J.J., et al., Sepallata1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes, AoB PLANTS, 2012, vol. 5, p. pls047. doi: 10.1093/aobpla/pls047

    Google Scholar 

  • Schakeel, S.N., Wang, X., Binder, B.M., et al., Mechanisms of signal transduction by ethylene: overlapping and non-overlapping signaling roles in a receptor family, AoB PLANTS, 2012, vol. 5, p. plt010. doi: 10.1093/aobpla/plt010

    Google Scholar 

  • Serrani, J.C., Ruiz-Rivero, O., Fos, M., et al., Auxininduced fruit-set in tomato is mediated in part by gibberellins, Plant J., 2008, vol. 56, pp. 922–934.

    Article  CAS  PubMed  Google Scholar 

  • Serrani, J.C., Carrera, E., Ruiz-Rivero, O., et al., Inhibition of auxin transport from ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins, Plant Physiol., 2010, vol. 153, pp. 851–862.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seymour, G.B., Ostergaard, L., Chapman, N.H., et al., Fruit development and ripening, Annu. Rev. Plant Biol., 2013, vol. 64, pp. 219–241.

    Article  CAS  PubMed  Google Scholar 

  • Sharova, E.I., Kletochnaya stenka rastenii (Plant Cell Wall), St. Petersburg: S.-Peterb. Gos. Univ., 2004.

    Google Scholar 

  • Sjut, V. and Bangerth, F., Effect of pollination or treatment with growth regulators on levels of extractable hormones in tomato ovaries and young fruits, Physiol. Plant., 1981, vol. 53, pp. 76–78.

    Article  CAS  Google Scholar 

  • Tang, X. and Woodson, W.R., Temporal and spatial expression of 1-aminocyclopropane-1-carboxylate oxidase mRNA following pollination of immature and mature petunia flowers, Plant Physiol., 1996, vol. 112, pp. 503–511.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Trainotti, L., Pavanello, A., and Casadoro, G., Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits?, J. Exp. Bot., 2005, vol. 56, pp. 2037–2046.

    Article  CAS  PubMed  Google Scholar 

  • Trainotti, L., Tadlello, A., and Casadoro, G., 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., 2007, vol. 58, pp. 3299–3308.

    Article  CAS  PubMed  Google Scholar 

  • Vriezen, W.H., Feron, R., Maretto, F., et al., Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set, New Phytol., 2008, vol. 177, pp. 60–76.

    CAS  PubMed  Google Scholar 

  • Wang, H., Jones, B., Li, Z., et al., The tomato Aux/IAA transcription factor is involved in fruit development and leaf morphogenesis, Plant Cell, 2005, vol. 17, pp. 2676–2692.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu, Kh.L., Zhu, B.Ts., Fu, D.Ts., et al., Role of ethylene in the biosynthetic pathways of aroma volatiles in ripening fruit, Russ. J. Plant Physiol., 2005, vol. 52, pp. 691–695.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. V. Obroucheva.

Additional information

Original Russian Text © N.V. Obroucheva, 2014, published in Ontogenez, 2014, Vol. 45, No. 1, pp. 14–27.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Obroucheva, N.V. Hormonal regulation during plant fruit development. Russ J Dev Biol 45, 11–21 (2014). https://doi.org/10.1134/S1062360414010068

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360414010068

Keywords

Navigation