Floral scent or flower scent is composed of all the volatile organic compounds (VOCs), or aroma compounds, emitted by floral tissue (e.g. flower petals). Floral scent is also referred to as aroma, fragrance, floral odour or perfume. Flower scent of most flowering plant species encompass a diversity of VOCs, sometimes up to several hundred different compounds. The primary functions of floral scent are to deter herbivorous and especially florivorous insects (see Plant defense against herbivory), and to attract pollinators. Floral scent is one of the most important communication channels mediating plant-pollinator interactions, along with visual cues (flower color, shape, etc.).
Perception by flower visitorsEdit
Flower visitors such as insects and bats detect floral scent thanks to chemoreceptors of variable specificity to a specific VOC. The fixation of a VOC on a chemoreceptor triggers the activation of an antennal glomerulus, further projecting on an olfactory receptor neuron and finally triggering a behavioral response after processing of the information (see also Olfaction, Insect olfaction). The simultaneous perception of various VOCs may cause the activation of several glomeruli, but the output signal may not be additive due to synergistic or antagonistic mechanisms linked with inter-neuronal activity. Therefore, the perception of a VOC within a floral blend may trigger a different behavioral response than when perceived isolated. Similarly, the output signal is not proportional to the amount of VOCs, with some VOCs in low amount in the floral blend having major effects on pollinator behavior. A good characterization of floral scent, both qualitative and quantitative, is necessary to understand and potentially predict flower visitors' behaviour.
Flower visitors use floral scent to detect, recognize and locate their host species, and even to discriminate among flowers of the same plant. This is made possible by the high specificity of floral scent, where both the diversity of VOCs and their relative amount may characterize the flowering species, an individual plant, a flower of the individual plant, and the distance of the plume from the source.
To make the best use of this specific information, flower visitors rely on long-term and short-term memory that allow them to efficiently choose their flower. They learn to associate the floral scent of a plant to a reward such as nectar and pollen, and have different behavioral responses to known scents versus unknown ones. They are also able to react similarly to slightly different odor blends.
Mediated biotic interactionsEdit
A major function of floral scent is to attract pollinators, and hence to ensure reproduction of animal-pollinated plants.
Some families of VOCs presented in floral scent have likely evolved as herbivore repellents. However, these plant defenses are also used by herbivores themselves to locate a plant resource, similarly to pollinators attracted by floral scent. Therefore, this phenotypic trait is subject to antagonistic selection pressures (positive selection by pollinators and negative selection by herbivores), leading to contrasting evolutionary patterns.
Floral scents are the only types of volatile cues that can be used to inform other plants about the mating environment. Plants that sense floral scents emitted by other plants can adapt their floral phenotypic traits that affect pollination and mating. For instance, in sexually deceptive orchids, floral scents emitted after pollination reduce attractiveness of the flower to pollinators, which acts as a signal to pollinators to visit unpollinated flowers within an inflorescence.
Synthesis of floral VOCsEdit
Most floral VOCs belong to three main chemical classes. VOCs in the same chemical class are synthesized from a shared precursor, but the biochemical pathway is specific for each VOC and often varies from a plant species to the other.
Terpenoids (or isoprenoids) are derived from isoprene and synthesized via the mevalonate pathway or the erythrol phosphate pathway. They represent the majority of floral VOCs, and are often the most abundant compounds in floral scent blends.
The second chemical class is composed of the fatty acid derivatives, synthesized from acetyl-CoA, of which most of them are also known as green leaf volatiles, because there are also emitted by vegetative parts (ie leaves and stems) of plants, and in sometimes higher abundance than from floral tissue.
Regulation of emissionsEdit
Floral scent emissions of most flowering plants vary predictably throughout the day, following a circadian rhythm. This variation is controlled by light intensity. Maximal emissions coincide with peaks of highest activity of visiting pollinators. For instance, snapdragon flowers, mostly pollinated by bees, have highest emissions at noon, whereas nocturnally-visited tobacco plants have highest emissions at night.
Floral scent emissions also vary along floral development, with highest emissions at anthesis, i.e. when the flower is fecund, and reduced emissions after pollination, probably due to mechanisms linked with fecundation. In tropical orchids, floral scent emission is terminated immediately following pollination, primarily to reduce expenditure of energy on fragrance production. In petunia flowers, ethylene is released to stop synthesis of benzenoid floral volatiles after successful pollination.
Abiotic factors, such as temperature, atmospheric CO2 concentration, hydric stress and soil nutrient status also impact the regulation of floral scent. For instance, increased temperatures in the environment can increase emission of VOCs in flowers, potentially altering communication between plants and pollinators.
Finally, biotic interactions may affect floral scent. Plant leaves attacked by herbivores emit new VOCs in response to the attack, the so-called herbivore-induced plant volatiles (HIPVs). Similarly, damaged flowers have a modified floral scent compared to undamaged ones. Micro-organisms present in nectar may alter floral scent emissions as well.
Measuring floral scent both qualitatively (identification of VOCs) and quantitatively (absolute and/or relative emission of VOCs) requires the use of analytical chemistry techniques. It requires to collect floral VOCs, and then to analyze them.
It is also possible to extract chemicals stocked in petals by immersing them into a solvent, and then analyze the liquid residue. This is more adapted to the study of heavier organic compounds, and/or VOCs that are stored in floral tissue before being emitted in air.
- thermodesorption: the adsorbent material is flash-heated so that all adsorbed VOCs are carried away from the adsorbent and injected into the separation system. This is how work injectors in gas chromatography machines, which literally volatilize introduced samples. For VOCs adsorbed on bigger amount of adsorbent material such as cartridges, thermodesorption may require the use of a specific machine, a thermodesorber, connected to the separation system.
- desorption by solvent: VOCs adsorbed on the adsorbent material are carried away by a small quantity of solvent which is then volatilized in injected in the separation system. Most commonly used solvents are very volatile molecules, such as methanol, so as to avoid co-elution with slightly heavier VOCs
Gas chromatography (GC) is ideal to separate volatilized VOCs due to their low molecular weight. VOCs are carried by a gas vector (helium) through a chromatographic column (the solid phase) on which they have different affinities, which allows to separate them.
Liquid chromatography may be used for liquid extractions of floral tissue.
Detection and identificationEdit
Separation systems are coupled with a detector, that allows the detection and identification of VOCs based on their molecular weight and chemical properties. The most used system for the analysis of floral scent samples is GC-MS (gas chromatography coupled with mass spectrometry).
- internal calibration: a known quantity of a specific chemical standard is injected together with the VOCs, the measured area on the chromatogram is proportional to the injected quantity. Because the chemical properties of VOCs alter their affinity to the solid phase (the chromatographic column) and subsequently the peak area on the chromatogram, it is best to use several standards that best reflect the chemical diversity of the floral scent sample. This method allows a more robust comparison among samples.
- external calibration: calibration curves (quantity vs. peak area) are established independently by the injection of a range of quantities of chemical standard. This method is best when the relative and absolute amount of VOCs in floral scent samples varies from sample to sample and from VOC to VOC and when the chemical diversity of VOCs in the sample is high. However, it is more time consuming and may be source of errors (e.g. matrix effects due to solvent or very abundant VOCs compared to trace VOCs).
Specificity of floral scent analysisEdit
Floral scent is often composed of hundreds of VOCs, in very variable proportions. The method used is a tradeoff between accurately detecting quantifying minor compounds and avoiding detector saturation by major compounds. For most analysis methods routinely used, the detection threshold of many VOCs is still higher than the perception threshold of insects, which reduces our capacity to understand plant-insect interactions mediated by floral scent.
Further, the chemical diversity in floral scent samples is challenging. The time of analysis is proportional to the range in molecular weight of VOCs present in the sample, hence a high diversity will increase analysis time. Floral scent may also be composed of very similar molecules, such as isomers and especially enantiomers, which tend to co-elute and then to be very hardly separated. Unambiguously detecting and quantifying them is of importance though, as enantiomers may trigger very different responses in pollinators.
- Knudsen, Jette T.; Eriksson, Roger; Gershenzon, Jonathan; Ståhl, Bertil (March 2006). "Diversity and Distribution of Floral Scent". The Botanical Review. 72 (1): 1–120. doi:10.1663/0006-8101(2006)72[1:DADOFS]2.0.CO;2.
- Piechulla, B.; Effmert, U. (2010). "Biosynthesis and Regulation of Flower Scent". Plant Developmental Biology - Biotechnological Perspectives. Springer Berlin Heidelberg. pp. 189–205. doi:10.1007/978-3-642-04670-4_10. ISBN 9783642046698.
- Raguso, Robert A. (December 2008). "Wake Up and Smell the Roses: The Ecology and Evolution of Floral Scent". Annual Review of Ecology, Evolution, and Systematics. 39 (1): 549–569. doi:10.1146/annurev.ecolsys.38.091206.095601.
- El-Sayed, A. M.; Mitchell, V. J.; McLaren, G. F.; Manning, L. M.; Bunn, B.; Suckling, D. M. (15 May 2009). "Attraction of New Zealand Flower Thrips, Thrips obscuratus, to cis-Jasmone, a Volatile Identified from Japanese Honeysuckle Flowers". Journal of Chemical Ecology. 35 (6): 656–663. doi:10.1007/s10886-009-9619-3. PMID 19444522.
- Cunningham, J. P. (2012-02-01). "Can mechanism help explain insect host choice?". Journal of Evolutionary Biology. 25 (2): 244–251. doi:10.1111/j.1420-9101.2011.02435.x. ISSN 1420-9101. PMID 22225990.
- Dudareva, Natalia; Negre, Florence; Nagegowda, Dinesh A.; Orlova, Irina (October 2006). "Plant Volatiles: Recent Advances and Future Perspectives". Critical Reviews in Plant Sciences. 25 (5): 417–440. doi:10.1080/07352680600899973.
- Chittka, Lars; Thomson, James D.; Waser, Nickolas M. (1999). "Flower Constancy, Insect Psychology, and Plant Evolution". Naturwissenschaften. 86 (8): 361–377. doi:10.1007/s001140050636. ISSN 0028-1042.
- Giurfa, Martin (2007-07-17). "Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well". Journal of Comparative Physiology A. 193 (8): 801–824. doi:10.1007/s00359-007-0235-9. ISSN 0340-7594. PMID 17639413.
- Junker, Robert R.; Höcherl, Nicole; Blüthgen, Nico (2010-07-01). "Responses to olfactory signals reflect network structure of flower-visitor interactions". Journal of Animal Ecology. 79 (4): 818–823. doi:10.1111/j.1365-2656.2010.01698.x. ISSN 1365-2656. PMID 20412348.
- Guerrieri, Fernando; Schubert, Marco; Sandoz, Jean-Christophe; Giurfa, Martin (2005-02-22). "Perceptual and Neural Olfactory Similarity in Honeybees". PLOS Biol. 3 (4): e60. doi:10.1371/journal.pbio.0030060. ISSN 1545-7885. PMC 1043859. PMID 15736975.
- Jaworski, Coline C.; Andalo, Christophe; Raynaud, Christine; Simon, Valérie; Thébaud, Christophe; Chave, Jérôme; Huang, Shuang-Quan (11 August 2015). "The Influence of Prior Learning Experience on Pollinator Choice: An Experiment Using Bumblebees on Two Wild Floral Types of Antirrhinum majus". PLOS ONE. 10 (8): e0130225. doi:10.1371/journal.pone.0130225. PMC 4532467. PMID 26263186.
- Schiestl, Florian P. (2010-05-01). "The evolution of floral scent and insect chemical communication". Ecology Letters. 13 (5): 643–656. doi:10.1111/j.1461-0248.2010.01451.x. ISSN 1461-0248. PMID 20337694.
- Theis, Nina; Adler, Lynn S. (2012-02-01). "Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction". Ecology. 93 (2): 430–435. doi:10.1890/11-0825.1. ISSN 1939-9170.
- Caruso, Christina M.; Parachnowitsch, Amy L. (2016). "Do Plants Eavesdrop on Floral Scent Signals?". Trends in Plant Science. 21 (1): 9–15. doi:10.1016/j.tplants.2015.09.001. PMID 26476624.
- Schiestl, Florian P.; Ayasse, Manfred (2001-02-01). "Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success?". Oecologia. 126 (4): 531–534. doi:10.1007/s004420000552. ISSN 0029-8549. PMID 28547238.
- Gershenzon, Jonathan; Dudareva, Natalia (18 June 2007). "The function of terpene natural products in the natural world". Nature Chemical Biology. 3 (7): 408–414. doi:10.1038/nchembio.2007.5. PMID 17576428.
- Harmer, Stacey L.; Hogenesch, John B.; Straume, Marty; Chang, Hur-Song; Han, Bin; Zhu, Tong; Wang, Xun; Kreps, Joel A.; Kay, Steve A. (2000-12-15). "Orchestrated Transcription of Key Pathways in Arabidopsis by the Circadian Clock". Science. 290 (5499): 2110–2113. doi:10.1126/science.290.5499.2110. ISSN 0036-8075. PMID 11118138.
- Kolosova, Natalia; Gorenstein, Nina; Kish, Christine M.; Dudareva, Natalia (2001-10-01). "Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants". The Plant Cell. 13 (10): 2333–2347. doi:10.1105/tpc.010162 (inactive 2019-02-22). ISSN 1532-298X. PMC 139162. PMID 11595805.
- Dudareva, Natalia; Murfitt, Lisa M.; Mann, Craig J.; Gorenstein, Nina; Kolosova, Natalia; Kish, Christine M.; Bonham, Connie; Wood, Karl (2000-06-01). "Developmental Regulation of Methyl Benzoate Biosynthesis and Emission in Snapdragon Flowers". The Plant Cell. 12 (6): 949–961. doi:10.1105/tpc.12.6.949. ISSN 1532-298X. PMC 149095. PMID 10852939.
- Negre, Florence; Kish, Christine M.; Boatright, Jennifer; Underwood, Beverly; Shibuya, Kenichi; Wagner, Conrad; Clark, David G.; Dudareva, Natalia (2003-12-01). "Regulation of Methylbenzoate Emission after Pollination in Snapdragon and Petunia Flowers". The Plant Cell. 15 (12): 2992–3006. doi:10.1105/tpc.016766. ISSN 1532-298X. PMC 282847. PMID 14630969.
- Arditti, Joseph (1980). "Aspects of the Physiology of Orchids". Advances in Botanical Research Volume 7. Advances in Botanical Research. 7. pp. 421–655. doi:10.1016/s0065-2296(08)60091-9. ISBN 9780120059072.
- Schuurink, Robert C.; Haring, Michel A.; Clark, David G. (2006). "Regulation of volatile benzenoid biosynthesis in petunia flowers". Trends in Plant Science. 11 (1): 20–25. doi:10.1016/j.tplants.2005.09.009. PMID 16226052.
- Piechulla, B.; Effmert, U. (2010-01-01). Pua, Eng Chong; Davey, Michael R. (eds.). Plant Developmental Biology - Biotechnological Perspectives. Springer Berlin Heidelberg. pp. 189–205. doi:10.1007/978-3-642-04670-4_10. ISBN 9783642046698.
- Farré-Armengol, Gerard; Filella, Iolanda; Llusià, Joan; Niinemets, Ülo; Peñuelas, Josep (2014). "Changes in floral bouquets from compound-specific responses to increasing temperatures". Global Change Biology. 20 (12): 3660–3669. doi:10.1111/gcb.12628. PMC 5788256. PMID 24817412.
- Arimura, Gen-ichiro; Matsui, Kenji; Takabayashi, Junji (2009-05-01). "Chemical and Molecular Ecology of Herbivore-Induced Plant Volatiles: Proximate Factors and Their Ultimate Functions". Plant and Cell Physiology. 50 (5): 911–923. doi:10.1093/pcp/pcp030. ISSN 0032-0781. PMID 19246460.
- Peñuelas, Josep; Farré-Armengol, Gerard; Llusia, Joan; Gargallo-Garriga, Albert; Rico, Laura; Sardans, Jordi; Terradas, Jaume; Filella, Iolanda (2014-10-22). "Removal of floral microbiota reduces floral terpene emissions". Scientific Reports. 4: 6727. doi:10.1038/srep06727. ISSN 2045-2322. PMC 4205883. PMID 25335793.
- Tholl, Dorothea; Boland, Wilhelm; Hansel, Armin; Loreto, Francesco; Röse, Ursula S.R.; Schnitzler, Jörg-Peter (2006-02-01). "Practical approaches to plant volatile analysis". The Plant Journal. 45 (4): 540–560. doi:10.1111/j.1365-313X.2005.02612.x. ISSN 1365-313X. PMID 16441348.
- Kim, Ki-Hyun; Kim, Yong-Hyun; Brown, Richard J. C. (2013-08-02). "Conditions for the optimal analysis of volatile organic compounds in air with sorbent tube sampling and liquid standard calibration: demonstration of solvent effect". Analytical and Bioanalytical Chemistry. 405 (26): 8397–8408. doi:10.1007/s00216-013-7263-9. ISSN 1618-2642. PMID 23907690.
- Macel, Mirka; Van DAM, Nicole M.; Keurentjes, Joost J. B. (2010-07-01). "Metabolomics: the chemistry between ecology and genetics". Molecular Ecology Resources. 10 (4): 583–593. doi:10.1111/j.1755-0998.2010.02854.x. ISSN 1755-0998. PMID 21565063.
- Parachnowitsch, Amy; Burdon, Rosalie C. F.; Raguso, Robert A.; Kessler, André (2013-01-01). "Natural selection on floral volatile production in Penstemon digitalis: Highlighting the role of linalool". Plant Signaling & Behavior. 8 (1): e22704. doi:10.4161/psb.22704. PMC 3745574. PMID 23221753.