Achotegui-Castells A., Danti R., Llusia J., Rocca G.D., Barberini S., Penuelas J. (2015) Strong Induction of Minor Terpenes in Italian Cypress, Cupressus sempervirens, in Response to Infection by the Fungus Seiridium cardinale. Journal of Chemical Ecology. : 0-0.LinkDoi: 10.1007/s10886-015-0554-1
Seiridium cardinale, the main fungal pathogen responsible for cypress bark canker, is the largest threat to cypresses worldwide. The terpene response of canker-resistant clones of Italian cypress, Cupressus sempervirens, to two differently aggressive isolates of S. cardinale was studied. Phloem terpene concentrations, foliar terpene concentrations, as well as foliar terpene emission rates were analyzed 1, 10, 30, and 90 days after artificial inoculation with fungal isolates. The phloem surrounding the inoculation point exhibited de novo production of four oxygenated monoterpenes and two unidentified terpenes. The concentrations of several constitutive mono- and diterpenes increased strongly (especially α-thujene, sabinene, terpinolene, terpinen-4-ol, oxygenated monoterpenes, manool, and two unidentified diterpenes) as the infection progressed. The proportion of minor terpenes in the infected cypresses increased markedly from the first day after inoculation (from 10 % in the control to 30–50 % in the infected treatments). Foliar concentrations showed no clear trend, but emission rates peaked at day 10 in infected trees, with higher δ-3-carene (15-fold) and total monoterpene (10-fold) emissions than the control. No substantial differences were found among cypresses infected by the two fungal isolates. These results suggest that cypresses activate several direct and indirect chemical defense mechanisms after infection by S. cardinale. © 2015 Springer Science+Business Media New York
Bernal M., Verdaguer D., Badosa J., Abadia A., Llusia J., Penuelas J., Nunez-Olivera E., Llorens L. (2015) Effects of enhanced UV radiation and water availability on performance, biomass production and photoprotective mechanisms of Laurus nobilis seedlings. Environmental and Experimental Botany. 109: 264-275.LinkDoi: 10.1016/j.envexpbot.2014.06.016
Climate models predict an increase in ultraviolet (UV) radiation and a reduction in precipitation in the Mediterranean region in the coming decades. High levels of UV radiation and water shortage can both cause photo-oxidative stress in plants. The aim of this study was to investigate the effects of enhanced UV radiation and its interaction with low water availability on seedling performance, biomass production, and photoprotective mechanisms of the sclerophyllous evergreen species Laurus nobilis L. (laurel). To achieve this goal, one-year-old seedlings of L. nobilis were grown outdoors under three UV conditions (ambient UV, enhanced UV-A, and enhanced UV-A. +. UV-B) and under two watering regimes (watered to field capacity and reduced water supply). The results show that plants produced more biomass when exposed to above ambient levels of UV-A or UV-A. +. UV-B radiation, especially under low water availability. This was probably related to a UV-induced increase in leaf relative water content and in leaf water use efficiency under water shortage. Even though our results suggest that UV-A supplementation may play an important role in the stimulation of biomass production, plants grown under enhanced UV-A plots showed higher levels of energy dissipation as heat (measured as NPQ) and a higher de-epoxidation state of the violaxanthin cycle. This suggests a greater excess of light energy under UV-A supplementation, in accordance with the observed reduction in the foliar content of light-absorbing pigments in these plants. Strikingly, the addition of UV-B radiation mitigated these effects. In conclusion, UV enhancement might benefit water status and growth of L. nobilis seedlings, especially under low water availability. The results also indicate the activation of different plant response mechanisms to UV-A and UV-B radiation, which would interact to produce the overall plant response. © 2014 Elsevier B.V.
Blanch J.S., Peñuelas J., Llusià J., Sardans J., Owen S.M. (2015) Differences in photosynthesis and terpene content in leaves and roots of wild-type and transgenic Arabidopsis thaliana plants. Russian Journal of Plant Physiology. 62: 823-829.LinkDoi: 10.1134/S1021443715060035
We investigated the hypotheses that two different varieties of Arabidopsis thaliana show differences in physiology and terpene production. The two varieties of A. thaliana used in this study were wild-type (WT) and transgenic line (CoxIV-FaNES I) genetically modified to emit nerolidol with linalool/nerolidol synthase (COX). Photosynthetic rate, electron transport rate, fluorescence, leaf volatile terpene contents and root volatile terpene contents were analyzed. For both types, we found co-eluting α-pinene+β-ocimene, limonene, and humulene in leaves; and in the roots we found co-eluting α-pinene+β-ocimene, sabinene+β-pinene, β-myrcene, limonene, and humulene. At the end of the growing cycle, COX plants tended to have lower pools of terpene compounds in their leaves, with 78.6% lower photosynthesis rates and 30.8% lower electron transport rates, compared with WT plants at that time. The maximal photochemical efficiency Fv/Fm was also significantly lower (25.5%) in COX plants, indicating that these varieties were more stressed than WT plants. However, COX plants had higher (239%) root terpene contents compared to WT plants. COX plants appear to favor root production of volatile terpenes rather than leaf production. Thus we conclude that there were significant differences between COX and WT plants in terms of terpenoid pools, stress status and physiology. © 2015, Pleiades Publishing, Ltd.
Farre-Armengol G., Filella I., Llusia J., Niinemets U., Penuelas J. (2015) Optimum temperature for floral terpene emissions tracks the mean temperature of the flowering season. Functional Plant Biology. 42: 851-857.LinkDoi: 10.1071/FP14279
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. © CSIRO 2015.
Farre-Armengol G., Filella I., Llusia J., Penuelas J. (2015) Relationships among floral VOC emissions, floral rewards and visits of pollinators in five plant species of a Mediterranean shrubland. Plant Ecology and Evolution. 148: 90-99.LinkDoi: 10.5091/plecevo.2015.963
Background and aims–In plant-pollinator communities seasonal changes in the abundance of pollinators lead to seasonal changes in competition among flowering plants for their services. Here we address the following question: Do flowers of a given species produce more olfactory signals (emissions of volatile compounds) and rewards (nectar and pollen) during the phase(s) of the flowering period within which they have to maximally compete with the signals and rewards of other co-flowering species in the community, compared to the amount of signals and rewards produced during the period(s) with less floral competition? Methods–We analysed the floral emission rates of biogenic volatile organic compounds by gas chromatography and proton transfer reaction mass spectrometry, the visitation rates of pollinators, and the availability of nectar and pollen during the flowering periods of five species to test whether floral rewards and signals would decrease with an increase in pollinator visitation rates during late spring and early summer, i.e. coinciding with decreasing competitive pressure for the services of pollinators. Key results–The results indicate that phenological patterns in the production of rewards are only present at the species level in those species with long flowering periods or with matching periods of changes in pollinator populations. The capacity of emitting isoprenoids and oxidised volatile organic compounds, however, did not present significant patterns during the flowering period in any of the five species studied. Conclusions–The results support the hypothesis of a decreasing competitive pressure for the attraction of pollinators that may drive a decrease in floral investment in rewards but not an accompanying decrease of the capacity of emitting volatile olfactory signals in a species with long flowering period. However, the negative correlation between nectar production and visitation rates may be reinforced by the opposite responses of these variables to climatic conditions. This fact makes difficult to discern possible evolutionary forces tending to decrease rewards from plastic responses to changing environmental conditions in that part of the flowering period in which pollinator visitation rates are higher. © 2015 Botanic Garden Meise and Royal Botanical Society of Belgium.
Farre-Armengol G., Filella I., Llusia J., Penuelas J. (2015) Pollination mode determines floral scent. Biochemical Systematics and Ecology. 61: 44-53.LinkDoi: 10.1016/j.bse.2015.05.007
The main objective of this study is to determine if the pollination vector influences the potential floral emissions of flowering plants. We hypothesized that flowers pollinated by insects would emit significantly higher amounts of volatile organic compounds (VOCs) and would present a higher diversity of these compounds than flowers pollinated by wind. The floral emissions of fifteen entomophilous species and eleven anemophilous species were captured by dynamic headspace sampling under field conditions and analyzed by gas chromatography-mass spectrometry. We searched for differences in the emission profiles between anemophilous and entomophilous flowers by considering the effects of phylogeny in our analysis. The floral emissions from the two groups were significantly different. Entomophilous species presented highly diverse emissions in both magnitude of emission rates and richness of compounds depending on the species, but overall, the flowers from entomophilous species had much higher VOC emission rates and VOC richness, both for terpenes and benzenoid compounds, than those from anemophilous species (two orders of magnitude higher emissions). The data thus confirm that the presence of intensely scented flowers with complex scents is strongly related to biotic pollination. © 2015 Elsevier Ltd.
Farre-Armengol G., Penuelas J., Li T., Yli-Pirila P., Filella I., Llusia J., Blande J.D. (2015) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytologist. : 0-0.LinkDoi: 10.1111/nph.13620
In this work we analyzed the degradation of floral scent volatiles from Brassica nigra by reaction with ozone along a distance gradient and the consequences for pollinator attraction. For this purpose we used a reaction system comprising three reaction tubes in which we conducted measurements of floral volatiles using a proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS) and GC-MS. We also tested the effects of floral scent degradation on the responses of the generalist pollinator Bombus terrestris. The chemical analyses revealed that supplementing air with ozone led to an increasing reduction in the concentrations of floral volatiles in air with distance from the volatile source. The results revealed different reactivities with ozone for different floral scent constituents, which emphasized that ozone exposure not only degrades floral scents, but also changes the ratios of compounds in a scent blend. Behavioural tests revealed that floral scent was reduced in its attractiveness to pollinators after it had been exposed to 120 ppb O3 over a 4.5 m distance. The combined results of chemical analyses and behavioural responses of pollinators strongly suggest that high ozone concentrations have significant negative impacts on pollination by reducing the distance over which floral olfactory signals can be detected by pollinators. © 2015 New Phytologist Trust.
Farré-Armengol G., Filella I., Llusia J., Primante C., Peñuelas J. (2015) Enhanced emissions of floral volatiles by Diplotaxis erucoides (L.) in response to folivory and florivory by Pieris brassicae (L.). Biochemical Systematics and Ecology. 63: 51-58.LinkDoi: 10.1016/j.bse.2015.09.022
The main function of floral emissions of volatile organic compounds (VOCs) in entomophilous plants is to attract pollinators. Floral blends, however, can also contain volatile compounds with defensive functions. These defensive volatiles are specifically emitted when plants are attacked by pathogens or herbivores. We characterized the changes in the floral emissions of Diplotaxis erucoides induced by folivory and florivory by Pieris brassicae. Plants were continually subjected to folivory, florivory and folivory + florivory treatments for two days. We measured floral emissions with proton transfer reaction/mass spectroscopy (PTR-MS) at different times during the application of the treatments. The emissions of methanol, ethyl acetate and another compound, likely 3-butenenitrile, increased significantly in response to florivory. Methanol and 3-butenenitrile increased 2.4- and 26-fold, respectively, in response to the florivory treatment. Methanol, 3-butenenitrile and ethyl acetate increased 3-, 100- and 9-fold, respectively, in response to the folivory + florivory treatment. Folivory alone had no detectable effect on floral emissions. All VOC emissions began immediately after attack, with no evidence of delayed induction in any of the treatments. Folivory and florivory had a synergistic effect when applied together, which strengthened the defensive response when the attack was extended to the entire plant. © 2015 Elsevier Ltd.
Llusia J., Roahtyn S., Yakir D., Rotenberg E., Seco R., Guenther A., Peñuelas J. (2015) Photosynthesis, stomatal conductance and terpene emission response to water availability in dry and mesic Mediterranean forests. Trees - Structure and Function. : 1-11.LinkDoi: 10.1007/s00468-015-1317-x
Key message: Warmer summer conditions result in increased terpene emissions except under severe drought, in which case they strongly decrease.Abstract: Water stress results in a reduction of the metabolism of plants and in a reorganization of their use of resources geared to survival. In the Mediterranean region, periods of drought accompanied by high temperatures and high irradiance occur in summer. Plants have developed various mechanisms to survive in these conditions by resisting, tolerating or preventing stress. We used three typical Mediterranean tree species in Israel, Pinus halepensis L., Quercus calliprinos and Quercus ithaburensis Webb, as models for studying some of these adaptive mechanisms. We measured their photosynthetic rates (A), stomatal conductance (gs), and terpene emission rates during spring and summer in a geophysical gradient from extremely dry to mesic from Yatir (south, arid) to Birya (north, moist) with intermediate conditions in Solelim. A and gs of P. halepensis were threefold higher in Birya than in Yatir where they remained very low both seasons. Quercus species presented 2–3-fold higher A and gs but with much more variability between seasons, especially for Q. ithaburensis with A and gs that decreased 10–30-fold from spring to summer. Terpene emission rates for pine were not different regionally in spring but they were 5–8-fold higher in Birya than in Yatir in summer (P < 0.05). Higher emissions were also observed in Solelim for the drought resistant Q. ithaburensis (P < 0.001) but not for Q. calliprinos. α-Pinene followed by limonene and 3-carene were the dominant terpenes. Warmer summer conditions result in increased Terpene emission rates except under severe drought, in which case they strongly decrease. © 2015 Springer-Verlag Berlin Heidelberg
Penuelas J., Bartrons M., Llusia J., Filella I. (2015) Sensing the energetic status of plants and ecosystems. Trends in Plant Science. 20: 528-530.LinkDoi: 10.1016/j.tplants.2015.07.002
The emerging consistency of the relationship between biochemical, optical, and odorous signals emitted by plants and ecosystems offers promising prospects for continuous local and global monitoring of the energetic status of plants and ecosystems, and therefore of their processing of energy and matter. © 2015 Elsevier Ltd.
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