Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Optimum temperature for floral terpene emissions tracks the mean temperature of the flowering season

Gerard Farré-Armengol A B E , Iolanda Filella A B , Joan Llusià A B , Ülo Niinemets C D and Josep Peñuelas A B
+ Author Affiliations
- Author Affiliations

A CSIC, Global Ecology Unit CREAF-CSIC-UAB, Cerdanyola del Vallès, 08193 Barcelona, Catalonia, Spain.

B CREAF, Cerdanyola del Vallès, 08193 Barcelona, Catalonia, Spain.

C Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, Tartu 51014, Estonia.

D Estonian Academy of Sciences, Kohtu 6, 10130 Tallinn, Estonia.

E Corresponding author. Email: g.farre@creaf.uab.es

Functional Plant Biology 42(9) 851-857 https://doi.org/10.1071/FP14279
Submitted: 4 October 2014  Accepted: 4 May 2015   Published: 22 June 2015

Abstract

Emissions of volatiles from leaves exhibit temperature dependence on maximums, but the optimum temperatures for the release of floral volatiles and the mechanism(s) of optimising these emissions have not been determined. We hypothesised that flowers have an optimum temperature for the emission of volatiles and, because the period of flowering varies highly among species, that this optimum is adapted to the temperatures prevailing during flowering. To test these hypotheses, we characterised the temperature responses of floral terpene emissions of diverse widespread Mediterranean plant species flowering in different seasons by using dynamic headspace sampling and analysis with GC-MS. The floral emissions of terpenes across species exhibited maximums at the temperatures corresponding to the season of flowering, with the lowest optimal temperatures observed in winter-flowering and the highest in summer-flowering species. These trends were valid for emissions of both total terpenes and the various terpene compounds. The results show that the optimum temperature of floral volatile emissions scales with temperature at flowering, and suggest that this scaling is the outcome of physiological adaptations of the biosynthetic or emission mechanisms of flowers.

Additional keywords: flower scent, interspecific variation, phenology, seasonal variability.


References

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends in Ecology & Evolution 22, 357–365.
Shifting plant phenology in response to global change.Crossref | GoogleScholarGoogle Scholar |

Cleveland WS, Grosse E, Shyu WM (1992) Local regression models. In ‘Statistical models in S’. (Eds JM Chambers, TJ Hastie) pp. 309–376. (Wadsworth: Pacific Grove, CA)

Colquhoun TA, Schwieterman ML, Gilbert JL, Jaworski EA, Langer KM, Jones CR, Rushing GV, Hunter TM, Olmstead J, Clark DG, Folta KM (2013) Light modulation of volatile organic compounds from petunia flowers and select fruits. Postharvest Biology and Technology 86, 37–44.
Light modulation of volatile organic compounds from petunia flowers and select fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFCqtr3K&md5=c105a9cf591572a072a60f46fba52e20CAS |

Copolovici LO, Niinemets U (2005) Temperature dependencies of Henry’s law constants and octanol/water partition coefficients for key plant volatile monoterpenoids. Chemosphere 61, 1390–1400.
Temperature dependencies of Henry’s law constants and octanol/water partition coefficients for key plant volatile monoterpenoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GgurvP&md5=4ef873be0b9246cc41f2d5a96b1ee8a0CAS | 15967478PubMed |

Dewick PM (2002) The biosynthesis of C5–C25 terpenoid compounds. Natural Product Reports 19, 181–222.
The biosynthesis of C5–C25 terpenoid compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFShsrc%3D&md5=1507c9e80c8261b24bc30eeb5598da14CAS | 12013278PubMed |

Dubey VS, Bhalla R, Luthra R (2003) An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants. Journal of Biosciences 28, 637–646.
An overview of the non-mevalonate pathway for terpenoid biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Ggt7g%3D&md5=5354a5406e09df43c3b7252e09d4c30eCAS | 14517367PubMed |

Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiology 122, 627–634.
Biochemical and molecular genetic aspects of floral scents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFSqsLg%3D&md5=ad09499e8e35f4271ad77dd8c9505f8eCAS | 10712525PubMed |

Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiology 135, 1893–1902.
Biochemistry of plant volatiles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1Ghu7w%3D&md5=ea75d8edc436e3c72addf2d0442872eeCAS | 15326281PubMed |

Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Science 25, 417–440.
Plant volatiles: recent advances and future perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Sqsb7O&md5=3ed5ba24b8d98bd31ec92e4e3107dd93CAS |

Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecological Monographs 73, 69–86.
Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods.Crossref | GoogleScholarGoogle Scholar |

Farré-Armengol G, Filella I, Llusia J, Peñuelas J (2013) Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspectives in Plant Ecology, Evolution and Systematics 15, 56–67.
Floral volatile organic compounds: between attraction and deterrence of visitors under global change.Crossref | GoogleScholarGoogle Scholar |

Farré-Armengol G, Filella I, Llusià J, Niinemets U, Peñuelas J (2014) Changes in floral bouquets from compound-specific responses to increasing temperatures. Global Change Biology 20, 3660–3669.
Changes in floral bouquets from compound-specific responses to increasing temperatures.Crossref | GoogleScholarGoogle Scholar | 24817412PubMed |

Fischbach RJ, Staudt M, Zimmer I, Rambal S, Schnitzler J-P (2002) Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex. Physiologia Plantarum 114, 354–360.
Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1altrg%3D&md5=1b4668655006c73e8fdaa1eda0c723e4CAS | 12060257PubMed |

Grote R, Monson RK, Niinemets Ü (2013) Leaf-level models of constitutive and stress-driven volatile organic compound emissions. In ‘Biology, controls and models of tree volatile organic compound emissions’ (Eds Ü Niinemets, RK Monson) pp. 315–355. (Springer: Berlin)

Harley PC (2013) The roles of stomatal conductance and compound volatility in controlling the emission of volatile organic compounds from leaves. In ‘Biology, controls and models of tree volatile organic compound emissions’. (Eds Ü Niinemets, RK Monson RK) pp. 181–208. (Springer: Berlin)

Helmig D, Daly RW, Milford J, Guenther A (2013) Seasonal trends of biogenic terpene emissions. Chemosphere 93, 35–46.
Seasonal trends of biogenic terpene emissions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVCgt7bI&md5=96a09dc4200e56ca400bfcf389a01fe8CAS | 23827483PubMed |

Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant, Cell & Environment 30, 1176–1190.
Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrE&md5=4798d570c27221880fa7c135219e65b9CAS |

Kuzuyama T, Seto H (2003) Diversity of the biosynthesis of the isoprene units. Natural Product Reports 20, 171–183.
Diversity of the biosynthesis of the isoprene units.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslCqsbs%3D&md5=01bbb710f2a7979a1def643f0c713b20CAS | 12735695PubMed |

Li Z, Sharkey TD (2013) Molecular and pathway controls on biogenic volatile organic compound emissions. In ‘Biology, controls and models of tree volatile organic compound emissions’. (Eds Ü Niinemets, RK Monson) pp. 119–151. (Springer: Berlin)

Llusia J, Peñuelas J, Alessio GA, Estiarte M (2006) Seasonal contrasting changes of foliar concentrations of terpenes and other volatile organic compound in four dominant species of a Mediterranean shrubland submitted to a field experimental drought and warming. Physiologia Plantarum 127, 632–649.
Seasonal contrasting changes of foliar concentrations of terpenes and other volatile organic compound in four dominant species of a Mediterranean shrubland submitted to a field experimental drought and warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovFGhu78%3D&md5=8017701011126c4f9539e67385097d28CAS |

Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A, Wang K, Loustau D (2002) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25, 1167–1179.
Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWitL0%3D&md5=7ceaf02ceff7664ed7b835b39f8e82e6CAS |

Monson RK (2013) Metabolic and gene expression controls on the production of biogenic volatile organic compounds. In ‘Biology, control and models of tree volatile organic compound emissions’. (Eds Ü Niinemets, RK Monson) pp. 153–179. (Springer: Berlin)

Niinemets Ü (2004) Costs of production and physiology of emission of volatile leaf isoprenoids. In ‘Advances in plant physiology: an international treaties series’. (Ed A Hemantaranjan) pp. 233–268. (Scientific Publishers: Jodhpur)

Niinemets Ü, Oja V, Kull O (1999) Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees. Plant, Cell & Environment 22, 1497–1513.
Shape of leaf photosynthetic electron transport versus temperature response curve is not constant along canopy light gradients in temperate deciduous trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVKmsw%3D%3D&md5=34b9e04aefa0212b70387b9e617dd763CAS |

Niinemets Ü, Reichstein M, Staudt M, Seufert G, Tenhunen JD (2002) Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea. Plant Physiology 130, 1371–1385.
Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOmsL4%3D&md5=4911d03373c090b183b8fc1fbb6cba7dCAS | 12428002PubMed |

Niinemets U, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends in Plant Science 9, 180–186.
Physiological and physicochemical controls on foliar volatile organic compound emissions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVGjsb8%3D&md5=07b570d991e4fd1e793fdcf4bbb80427CAS | 15063868PubMed |

Niinemets Ü, Monson RK, Arneth A, Ciccioli P, Kesselmeier J, Kuhn U, Noe SM, Peñuelas J, Staudt M (2010) The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling. Biogeosciences 7, 1809–1832.
The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2ksrrF&md5=a8d1a47489985156244123f8b0ab6715CAS |

Peñuelas J, Llusià J (2001) The complexity of factors driving volatile organic compound emissions by plants. Biologia Plantarum 44, 481–487.
The complexity of factors driving volatile organic compound emissions by plants.Crossref | GoogleScholarGoogle Scholar |

R Development Core Team (2011) ‘R : a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna)

Servei Meteorològic de Catalunya (2010) Meteocat home page. (Servei Meteorològic de Catalunya: Barcelona). Available at: http://www.meteo.cat/ [Verified 15 May 2015].

Staudt M, Joffre R, Rambal S (2003) How growth conditions affect the capacity of Quercus ilex leaves to emit monoterpenes. New Phytologist 158, 61–73.
How growth conditions affect the capacity of Quercus ilex leaves to emit monoterpenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1Wlsbk%3D&md5=be431895c4637c997d33e14a674e0defCAS |

van Schie CCN, Haring MA, Schuurink RC (2006) Regulation of terpenoid and benzenoid production in flowers. Current Opinion in Plant Biology 9, 203–208.
Regulation of terpenoid and benzenoid production in flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhvVWrur0%3D&md5=e574706b8be6102f39ae8bf60ffe29d2CAS |