Skip to main content
SpringerLink
Log in

Involvement of Ethylene Biosynthesis and Signalling in the Transition from Male to Female Flowering in the Monoecious Cucurbita pepo

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

It is well established that ethylene is the main hormonal regulator of sexual expression in the Cucurbitaceae family, controlling not only the sexual fate of individual floral buds, but also the female flower transition, that is, the time at which the first female flower appears and therefore the number of female flowers per plant. Although sex determination of individual flower buds is known to be controlled by specific ethylene biosynthesis ACS genes in melon and cucumber, the role of ethylene genes in the control of the transition to female flowering is still unknown. We have identified two contrasting monoecious inbred lines of Cucurbita pepo, Bolognese (Bog) and Vegetable spaghetti (Veg), which differ in female flower transition but not in flower development. In Bog, which is very sensitive to ethylene, the transition to female flowering is very early, whereas in Veg, which is much less sensitive to ethylene, the transition occurs much later. In this article we compare the production of ethylene and the expression profiles of seven genes involved in the biosynthesis, perception, and signalling of ethylene in the two contrasting lines. Bog, with earlier female flower transition, showed higher ethylene production and CpACO1 expression in the apex at an earlier stage of plant development, when Bog is already producing female flowers, but Veg has not transitioned to female flowering yet. Moreover, the expression of the ethylene receptor and CTR-like genes in the apex of Veg and Bog plants indicates that these genes negatively regulate female flower transition during the earlier stages of plant development. The earlier transition to female flowering in Bog is not only associated with a higher production of ethylene in the apex but also with a premature decline of ethylene negative regulators (receptors and CTR-like) in the apex of the plant. These results provide the basis for a model that explains the regulation of female flowering transition in monoecious cucurbits.

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

Similar content being viewed by others

References

  • Bleecker AB (1999) Ethylene perception and signaling: an evolutionary perspective. Trends Plant Sci 4:269–274

    Article  PubMed  Google Scholar 

  • Boualem A, Fergany M, Fernandez R, Troadec C, Martin A, Morin H, Sari M, Collin F, Flowers JM, Pitrat M, Purugganan MD, Dogimont C, Bendahmane A (2008) A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321:836–838

    Article  CAS  PubMed  Google Scholar 

  • Boualem A, Troadec C, Kovalski I, Sari M, Perl-Treves R, Bendahmane A (2009) A conserved ethylene biosynthesis enzyme leads to andromonoecy in two Cucumis species. PLoS One 4:1–10

    Article  Google Scholar 

  • Byers RE, Baker LR, Sell HM, Herner RC, Dilley DR (1972) Ethylene: a natural regulator of sex expression in Cucumis melo L. Proc Natl Acad Sci USA 69:712–720

    Article  Google Scholar 

  • Clark KL, Larsen PB, Wang X, Chang C (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci USA 95:5401–5406

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duan Q, Wang D, Xu Z, Bai S (2008) Stamen development in Arabidopsis is arrested by organ-specific overexpression of a cucumber ethylene synthesis gene CsACO2. Planta 228:537–543

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94:261–271

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Chang C, Sun Q, Meyerowitz EM (1995) Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–1714

    Article  CAS  PubMed  Google Scholar 

  • Huang P, Parks JE, Rottmann WH, Theologis A (1991) Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. Proc Natl Acad Sci USA 88:7021–7025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamachi S, Sekimoto H, Kondo N, Sakai S (1997) Cloning of a cDNA for a 1-aminocyclopropane-1-carboxylate synthase that is expressed during development of female flowers at the apices of Cucumis sativus L. Plant Cell Physiol 38:1197–1206

    Article  CAS  PubMed  Google Scholar 

  • Kamachi S, Mizusawa H, Matsuura S, Sakai S (2000) Expression of two 1-aminocyclopropane-1- carboxylate synthase genes, CS-ACS1 and CS-ACS2, correlated with sex phenotypes in cucumber plants (Cucumis sativus L.). Plant Biotechnol 17:69–74

    Article  CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kieber JJ, Ecker JR (1993) Ethylene gas: it’s not just for ripening any more! Trends Genet 9:356–362

    Article  CAS  PubMed  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441

    Article  CAS  PubMed  Google Scholar 

  • Knopf RR, Trebitsh T (2006) The female-specific Cs-ACS1G gene of cucumber. A case of gene duplication and recombination between the non-sex-specific 1-aminocyclopropane-1-carboxylate synthase gene and a branched-chain amino acid transaminase gene. Plant Cell Physiol 47:1217–1228

    Article  CAS  PubMed  Google Scholar 

  • Krupnick GA, Brown KM, Stephenson AG (1999) The influence of fruit on the regulation of internal ethylene concentrations and sex expression in Cucurbita texana. Int J Plant Sci 160:321–330

    Article  CAS  Google Scholar 

  • Li Z, Huang S, Liu S, Pan J, Zhang Z, Tao Q, Shi Q, Jia Z, Zhang W, Chen H, Si L, Zhu L, Cai R (2009) Molecular isolation of the M gene suggests that a conserved-residue conversion induces the formation of bisexual flowers in cucumber plants. Genetics 784:1381–1385

    Article  Google Scholar 

  • Little HA, Papadopoulou E, Hammar SA, Grumet R (2007) The influence of ethylene perception on sex expression in melon (Cucumis melo L.) as assessed by expression of the mutant ethylene receptor, At-etr1-1, under the control of constitutive and floral targeted promoters. Sex Plant Reprod 20:123–136

    Article  CAS  Google Scholar 

  • Liu Q, Wen C (2012) Arabidopsis ETR1 and ERS1 differentially repress the ethylene response in combination with other ethylene receptor genes. Plant Physiol 158:1193–1207

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manzano S, Martínez C, Kraakman P, Jamilena M (2008) Use of ethylene production as a marker for the selection of gynoecy in melon (Cucumis melo). In: Pitrat M (ed) IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae. INRA, Avignon, pp 557–561

    Google Scholar 

  • Manzano S, Martínez C, Domínguez V, Avalos E, Garrido D, Gómez P, Jamilena M (2010a) A major gene conferring reduced ethylene sensitivity and maleness in Cucurbita pepo. J Plant Growth Regul 29:73–80

    Article  CAS  Google Scholar 

  • Manzano S, Martínez C, Gómez P, Garrido D, Jamilena M (2010b) Cloning and characterization of two CTR1-like genes in Cucurbita pepo: regulation of their expression during male and female flower development. Sex Plant Reprod 23:301–313

    Article  CAS  PubMed  Google Scholar 

  • Manzano S, Martínez C, Megías Z, Gómez P, Garrido D, Jamilena M (2011) The role of ethylene and brassinosteroids in the control of sex expression and flower development in Cucurbita pepo. Plant Growth Regul 65:213–221

    Article  CAS  Google Scholar 

  • Mibus H, Tatlioglu T (2004) Molecular characterization and isolation of the F/f gene for femaleness in cucumber (Cucumis sativus L.). Theor Appl Genet 109:1669–1676

    Article  CAS  PubMed  Google Scholar 

  • Owens KW, Peterson CE, Tolla GE (1980) Production of hermaphrodite flowers on gynoecious muskmelon by silver nitrate and aminoethyoxyvinylglycine. HortScience 15:654–655

    CAS  Google Scholar 

  • Papadopoulou E, Little HA, Hammar SA, Grumet R (2005) Effect of modified endogenous ethylene production on sex expression, bisexual flower development and fruit production in melon (Cucumis melo L.). Sex Plant Reprod 18:131–142

    Article  CAS  Google Scholar 

  • Payán MC, Peñaranda A, Rosales R, Garrido D, Gomez P, Jamilena M (2006) Ethylene mediates the induction of fruits with attached flower in zucchini squash. In: Holmes GJ (ed) Proceedings cucurbitaceae 2006. Universal Press, Raleigh, pp 171–179

    Google Scholar 

  • Payán C, Peñaranda A, Mariotti B, Garrido D, Jamilena M, Gómez P (2008) Isolation of Cucurbita pepo ethylene receptors Cup-ETR1 and Cup-ERS1 and functional analysis during fruit formation. In: Pitrat M (ed) IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae. INRA, Avignon, pp 569–573

    Google Scholar 

  • Peñaranda A, Payán MC, Garrido D, Gómez P, Jamilena M (2007) Production of fruits with attached flowers in zucchini squash is correlated with the arrest of maturation of female flowers. J Hortic Sci Biotechnol 82:579–584

    Google Scholar 

  • Perl-Treves R (1999) Male to female conversion along the cucumber shoot: approaches to studying sex genes and floral development in Cucumis sativus. In: Ainsworth CC (ed) Sex determination in plants. BIOS Scientific, Oxford, pp 189–215

    Google Scholar 

  • Saito S, Fujii N, Miyazawa Y, Yamasaki S, Matsuura S, Mizusawa H, Fujita Y, Takahashi H (2007) Correlation between development of female flower buds and expression of the CS-ACS2 gene in cucumber plants. J Exp Bot 58:2897–2907

    Article  CAS  PubMed  Google Scholar 

  • Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM (1998) ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci USA 95:5812–5817

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trebitsh T, Staub JE, O’Neill SD (1997) Identification of a 1-aminocyclopropane-1-carboxylic acid synthase gene linked to the female (F) locus that enhances female sex expression in cucumber. Plant Physiol 113:987–995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:131–151

    Google Scholar 

  • Wang W, Hall AE, O’Malley R, Bleecker AB (2003) Canonical histidine kinase activity of the transmitter domain of the ETR1 ethylene receptor from Arabidopsis is not required for signal transmission. Proc Natl Acad Sci USA 100:352–357

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang D, Li F, Duan Q, Han T, Xu Z, Bai S (2010) Ethylene perception is involved in female cucumber flower development. Plant J 61:862–872

    Article  CAS  PubMed  Google Scholar 

  • 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 41:608–616

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki S, Fujii N, Matsuura S, Mizusawa H, Takahashi H (2001) The M locus and ethylene-controlled sex determination in andromonoecious cucumber plants. Plant Cell Physiol 42:608–619

    Article  CAS  PubMed  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants AGL2008-05619-C02-02/ALI and AGL2011-30568-C02-02/ALI, which are partly funded by ERDF (European Regional Development Fund) and by the Spanish Ministry of Science and Innovation, and by Grant CVI-02617, which is funded by ERDF and by the Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía, Spain. CM and ZM acknowledge FPU program scholarships from MEC, Spain. SM is funded by grant PTA2011-479-I from the Spanish Ministry of Science and Innovation.

Author information

Authors and Affiliations

  1. Departamento de Biología y Geología, Agrifood Campus of International Excellence (ceiA3), Escuela Politécnica Superior y Facultad de Ciencias Experimentales, Universidad de Almería, 04120, Almería, Spain

    Susana Manzano, Cecilia Martínez, Zoraida Megías & Manuel Jamilena

  2. Departamento de Fisiología Vegetal, Facultad de Ciencias, Universidad de Granada, 18071, Granada, Spain

    Dolores Garrido

Authors
  1. Susana Manzano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cecilia Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zoraida Megías
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dolores Garrido
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel Jamilena
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Jamilena.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 179 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Manzano, S., Martínez, C., Megías, Z. et al. Involvement of Ethylene Biosynthesis and Signalling in the Transition from Male to Female Flowering in the Monoecious Cucurbita pepo . J Plant Growth Regul 32, 789–798 (2013). https://doi.org/10.1007/s00344-013-9344-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-013-9344-6

Keywords

Search

Navigation