Skip to main content
SpringerLink
Log in

The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

In the genus Petunia, distinct pollination syndromes may have evolved in association with bee-visitation (P. integrifolia spp.) or hawk moth-visitation (P. axillaris spp). We investigated the extent of congruence between floral fragrance and olfactory perception of the hawk moth Manduca sexta. Hawk moth pollinated P. axillaris releases high levels of several compounds compared to the bee-pollinated P. integrifolia that releases benzaldehyde almost exclusively. The three dominating compounds in P. axillaris were benzaldehyde, benzyl alcohol and methyl benzoate. In P. axillaris, benzenoids showed a circadian rhythm with an emission peak at night, which was absent from P. integrifolia. These characters were highly conserved among different P. axillaris subspecies and P. axillaris accessions, with some differences in fragrance composition. Electroantennogram (EAG) recordings using flower-blends of different wild Petunia species on female M. sexta antennae showed that P. axillaris odours elicited stronger responses than P. integrifolia odours. EAG responses were highest to the three dominating compounds in the P. axillaris flower odours. Further, EAG responses to odour-samples collected from P. axillaris flowers confirmed that odours collected at night evoked stronger responses from M. sexta than odours collected during the day. These results show that timing of odour emissions by P. axillaris is in tune with nocturnal hawk moth activity and that flower-volatile composition is adapted to the antennal perception of these pollinators.

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

Abbreviations

EAG:

Electroantennogram

EAD:

Electroantennogram detection

QTL:

Quantitative trait loci

GC:

Gas chromatogram

MS:

Mass spectrometer

References

  • Altenburger R, Matile P (1988) Circadian rhythmicity of fragrance emission in flowers of Hoya carnosa R. Br Planta 174: 248–252

    CAS  Google Scholar 

  • Ando T, Iida S, Kokubun H, Ueda Y, Marchesi E (1995a) Distribution of Petunia axillaris sensu lato in Uruguay as revealed by discriminant analysis of the live plants. J Jpn Soc Hortic Sci 64:381–391

    Article  Google Scholar 

  • Ando T, Kurata S, Sasaki S, Ueda Y, Hashimoto G, Marchesi E (1995b) Comparative morphological studies on intraspecific taxa of Petunia integrifolia (Hook.) Schinz et Thell. (Solanaceae). Jpn Bot 70:205–217

    Google Scholar 

  • Ando T, Nomura M, Tsukahara J, Watanabe H, Kokubun H, Tsukamoto T, Hashimoto G, Marchesi E, Kitching IJ (2001) Reproductive isolation in a native population of Petunia sensu Jussieu (Solanaceae). Ann Bot 88:403–413

    Article  Google Scholar 

  • Arn H, Städler E, Rauscher S (1975) The electroantennographic detector-A selective and sensitive tool in gas chromatographic analysis of insect pheromones. Z Naturforsch 30:722–725

    Google Scholar 

  • Baldwin IT, Preston C, Euler M, Gorham D (1997) Patterns and consequences of benzyl acetone floral emissions from Nicotiana attenuata plants. J Chem Ecol 23:2327–2343

    Article  CAS  Google Scholar 

  • Boatright J, Negre F, Chen X, Kish CM, Wood B, Peel G, Orlova I, Gang D, Rhodes D, Dudareva N (2004) Understanding in vivo benzenoid metabolism in Petunia petal tissue. Plant Physiol 135:1993–2001

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw HD Jr, Otto KG, Frewen BE, McKay JK, Schemske DW (1998) Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149:367–382

    PubMed  CAS  Google Scholar 

  • Brantjes NBM (1978) Sensory responses to flowers in night-flying moths. In: Richards AJ (ed) The pollination of flowers by insects. Academic, London, pp 13–19

    Google Scholar 

  • Daly KC, Smith BH (2000) Associative olfactory learning in the moth Manduca sexta. J Exp Biol 203:2025–2038

    PubMed  CAS  Google Scholar 

  • Daly KC, Durtschi ML, Smith BH (2001) Olfactory-based discrimination learning in the moth, Manduca sexta. J Insect Physiol 47:375–384

    Article  PubMed  CAS  Google Scholar 

  • Dobson HEM (1994) Floral volatiles in insect biology. In: Bernays EA (ed) Insect plant interactions, vol 5. CRC Press, Boca Raton, pp 47–81

  • Euler M, Baldwin IT (1996) The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107:102–112

    Article  Google Scholar 

  • Fraser AM, Mechaber WL, Hildebrand JG (2003) Electroantennographic and behavioral responses of the sphynx moth Manduca sexta to host plant headspace volatiles. J Chem Ecol 29:1813–1833

    Article  PubMed  CAS  Google Scholar 

  • Guerenstein PG, Guerin PM (2001) Olfactory and behavioural responses of the blood-sucking bug Triatoma infestans to odours of vertebrate hosts. J Exp Biol 204:585–597

    PubMed  CAS  Google Scholar 

  • Helsper JPFG, Davies JA, Bouwmeester HJ, Krol AF, van Kampen MH (1998) Circadian rhythmicity in emission of volatile compounds by flowers of Rosa hybrida L. cv. Honesty. Planta 207:88–95

    Article  CAS  Google Scholar 

  • Hildebrand JG (1996) Olfactory control of behaviour in moths: central processing of odour information and the functional significance of olfactory glomeruli. J Comp Physiol A 178:5–19

    Article  PubMed  CAS  Google Scholar 

  • Itagaki H, Hildebrand JG (1990) Olfactory interneurons in the brain of the larval sphinx moth Manduca sexta. J Comp Physiol 167:309–320

    Article  CAS  Google Scholar 

  • Kalinová B, Hoskovec M, Liblikas I, Unelius CR, Hansson BS (2001) Detection of sex pheromone components in Manduca sexta (L.). Chem Senses 26:1175–1186

    Article  PubMed  Google Scholar 

  • Kelber A, Balkenius A, Warrant EJ (2002) Scotopic colour vision in nocturnal hawkmoths. Nature 419:922–925

    Article  PubMed  CAS  Google Scholar 

  • Knudsen JT, Tollsten L, Bergström GL (1993) Floral scents-a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280

    Article  CAS  Google Scholar 

  • Kolosova N, Gorenstein N, Kish CM, Dudareva N (2001) Regulation of cyrcadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:2333–2347

    Article  PubMed  CAS  Google Scholar 

  • Levin RA, Raguso RA, McDade LA (2001) Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58: 429–440

    Article  PubMed  CAS  Google Scholar 

  • Loughrin JH, Hamilton-Kemp TR, Andersen RA, Hildebrand DF (1991) Circadian-rhythm of volatile emission from flowers of Nicotiana sylvestris and N. suaveolens. Physiol Plantarum 83:492–496

    Article  CAS  Google Scholar 

  • Lu S, Xu R, Jia J-W, Pang J, Matsuda SPT, Chen X-Y (2002) Cloning and functional characterization of a β-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol 130:477–486

    Article  PubMed  CAS  Google Scholar 

  • Negre F, Kish CM, Boatright J, Underwood B, Shibuya K, Wagner C, Clark DG, Dudareva N (2003) Regulation of methylbenzoate emission after pollination in snapdragon and petunia flowers. Plant Cell 15:2992–3006

    Article  PubMed  CAS  Google Scholar 

  • Overland L (1960) Endogenous rhythm in opening and odor of flowers of Cestrum nocturnum. Am J Bot 47:378–382

    Article  Google Scholar 

  • Raguso RA, Light DM (1998) Electroantennogram responses of male Sphinx perelegans hawkmoths to floral and “green-leaf volatiles”. Entomol Exp Appl 86:287–293

    Article  CAS  Google Scholar 

  • Raguso RA, Pichersky E (1995) Floral volatiles from Clarkia breweri and C. concinna (Onagraceae): recent evolution of floral scent and moth pollination. Plant Syst Evol 194:55–67

    Article  CAS  Google Scholar 

  • Raguso RA, Willis MA (2002) Synergy between visual and olfactory cues in nectar feeding by naïve hawkmoths, Manduca sexta. Anim Behav 64:685–695

    Article  Google Scholar 

  • Raguso RA, Levin RA, Foose SE, Holmberg MW, McDade LA (2003) Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry 63:265–284

    Article  PubMed  CAS  Google Scholar 

  • Schiestl FP, Marion-Poll F (2002) Detection of physiologically active flower volatiles using gas chromatography coupled with electroantennography. In: Jackson JF, Linskens HF (eds) Analysis of taste and aroma, vol 21. Springer, Berlin Heidelberg New York, pp 173–198

  • Schneider D (1957) Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. Z Vergl Physiol 40:8–41

    Article  Google Scholar 

  • Shields VDC, Hildebrand JG (2001) Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J Comp Physiol A 186:1135–1151

    Article  CAS  Google Scholar 

  • Steullet D, Guerin PM (1994) Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae). I. Receptors within the Haller’s organe capsule. J Comp Physiol 174:27–38

    Article  CAS  Google Scholar 

  • Stuurman J, Hoballah ME, Broger L, Moore J, Basten C, Kuhlemeier C (2004) Genetic basis of floral pollination syndromes in Petunia integrifolia and Petunia axillaris. Genetics 168:1585–1599

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Ando T, Kurata M, Watanabe H, Kokubun H, Hashimoto G, Marchesi A (1998) Resurrection of Petunia occidentalis R. E. Fr. (Solanaceae) inferred from a cross compatibility study. J Jpn Bot 73:15–21

    Google Scholar 

  • Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152

    Article  CAS  Google Scholar 

  • Verdonk JC, Ric de Vos CH, Verhoeven HA, Haring MA, van Tunen AJ, Schuurink RC (2003) Regulation of floral scent production in Petunia revealed by targeted metabolomics. Phytochemistry 62:997–1008

    Article  PubMed  CAS  Google Scholar 

  • Watanabe H, Ando T, Iida S, Suzuki A, Buto K, Tsukamoto T, Hashimoto G, Marchesi E (1996) Cross compatibility of Petunia cultivars and P. axillaris with native taxa of Petunia in relation to their chromosome number. J Jpn Soc Hortic Sci 65:625–634

    Article  Google Scholar 

  • Wijsman HJW (1982) On the interrelationships of certain species of Petunia. I. Taxonomic notes on the parental species of Petunia hybrida. Acta Bot Neerl 31:477–490

    Google Scholar 

  • Wijsman HJW (1983) On the interrelationships of certain species of Petunia II. Experimental data: crosses between different taxa. Acta Bot Neerl 32:97–107

    Google Scholar 

  • Willis MA, Butler MA, Tolbert LP (1995) Normal glomerular organization of the antennal lobes is not necessary for odor-modulated flight in female moths. J Comp Physiol A 176:205–216

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Special thanks to C. Ball, R. Alder (University of Bern, Institute of Plant Sciences) and C. Faria (University of Neuchâtel, Institute of Zoology) for plant care, and to L. Broger, Dr. J. Moore, C. Galliot, R. Schreyer and A. Dell’Olivo (University of Bern, Institute of Plant Sciences) for insightful comments on an earlier version of the manuscript. This work was part of the National Centre for Competence in Research “Plant Survival” with financial support by the Swiss National Science Foundation and the Canton Bern.

Author information

Authors and Affiliations

  1. Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013, Bern, Switzerland

    Maria Elena Hoballah, Jeroen Stuurman & Cris Kuhlemeier

  2. Institute of Zoology, University of Neuchâtel, Case postale 2, 2007, Neuchâtel, Switzerland

    Ted C. J. Turlings, Patrick M. Guerin & Sophie Connétable

Authors
  1. Maria Elena Hoballah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeroen Stuurman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ted C. J. Turlings
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick M. Guerin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sophie Connétable
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cris Kuhlemeier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cris Kuhlemeier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoballah, M.E., Stuurman, J., Turlings, T.C.J. et al. The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta . Planta 222, 141–150 (2005). https://doi.org/10.1007/s00425-005-1506-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-1506-8

Keywords

Search

Navigation