Fernández-Martínez M., Llusià J., Filella I., Niinemets Ü., Arneth A., Wright I.J., Loreto F., Peñuelas J. (2018) Nutrient-rich plants emit a less intense blend of volatile isoprenoids. New Phytologist. 220: 773-784.EnlaceDoi: 10.1111/nph.14889
The emission of isoprenoids (e.g. isoprene and monoterpenes) by plants plays an important defensive role against biotic and abiotic stresses. Little is known, however, about the functional traits linked to species-specific variability in the types and rates of isoprenoids emitted and about possible co-evolution of functional traits with isoprenoid emission type (isoprene emitter, monoterpene emitter or both). We combined data for isoprene and monoterpene emission rates per unit dry mass with key functional traits (foliar nitrogen (N) and phosphorus (P) concentrations, and leaf mass per area) and climate for 113 plant species, covering the boreal, wet temperate, Mediterranean and tropical biomes. Foliar N was positively correlated with isoprene emission, and foliar P was negatively correlated with both isoprene and monoterpene emission rate. Nonemitting plants generally had the highest nutrient concentrations, and those storing monoterpenes had the lowest concentrations. Our phylogenetic analyses found that the type of isoprenoid emission followed an adaptive, rather than a random model of evolution. Evolution of isoprenoids may be linked to nutrient availability. Foliar N and P are good predictors of the type of isoprenoid emission and the rate at which monoterpenes, and to a lesser extent isoprene, are emitted. © 2017 The Authors. New Phytologist © 2017 New Phytologist Trust
Farré-Armengol G., Filella I., Llusià J., Peñuelas J. (2017) β-Ocimene, a Key Floral and Foliar Volatile Involved in Multiple Interactions between Plants and Other Organisms. Molecules (Basel, Switzerland). 22: 0-0.EnlaceDoi: 10.3390/molecules22071148
β-Ocimene is a very common plant volatile released in important amounts from the leaves and flowers of many plant species. This acyclic monoterpene can play several biological functions in plants, by potentially affecting floral visitors and also by mediating defensive responses to herbivory. The ubiquity and high relative abundance of β-ocimene in the floral scents of species from most plant families and from different pollination syndromes (ranging from generalism to specialism) strongly suggest that this terpenoid may play an important role in the attraction of pollinators to flowers. We compiled abundant evidence from published studies that supports β-ocimene as a generalist attractant of a wide spectrum of pollinators. We found no studies testing behavioural responses of pollinators to β-ocimene, that could directly demonstrate or deny the function of β-ocimene in pollinator attraction; but several case studies support that the emissions of β-ocimene in flowers of different species follow marked temporal and spatial patterns of emission, which are typical from floral volatile organic compound (VOC) emissions that are involved in pollinator attraction. Furthermore, important β-ocimene emissions are induced from vegetative plant tissues after herbivory in many species, which have relevant functions in the establishment of tritrophic interactions. We thus conclude that β-ocimene is a key plant volatile with multiple relevant functions in plants, depending on the organ and the time of emission. Experimental behavioural studies on pure β-ocimene conducted with pollinating insects will be necessary to prove the assumptions made here.
Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino-Serrano, M., Vives-Ingla, M., Stocker, B.D., Balzarolo, M., Guerrieri, R., Peaucelle, M., Marañón-Jiménez, S., Bórnez-Mejías, K., Mu, Z., Descals, A., Castellanos, A., Terradas, J. (2017) Impacts of global change on Mediterranean forests and their services. Forests. 8: 0-0.EnlaceDoi: 10.3390/f8120463
Zhang, C., Filella, I., Liu, D., Ogaya, R., Llusià, J., Asensio, D., Peñuelas, J. (2017) Photochemical Reflectance Index (PRI) for detecting responses of diurnal and seasonal photosynthetic activity to experimental drought and warming in a Mediterranean shrubland. Remote Sensing. 9: 0-0.EnlaceDoi: 10.3390/rs9111189
Farré-Armengol, G., Filella, I., Llusia, J., Peñuelas, J. (2016) Bidirectional Interaction between Phyllospheric Microbiotas and Plant Volatile Emissions. Trends in Plant Science. 21: 854-860.EnlaceDoi: 10.1016/j.tplants.2016.06.005
Gargallo-Garriga A., Sardans J., Pérez-Trujillo M., Guenther A., Llusià J., Rico L., Terradas J., Farré-Armengol G., Filella I., Parella T., Peñuelas J. (2016) Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota. BMC Plant Biology. 16: 0-0.EnlaceDoi: 10.1186/s12870-016-0767-7
Background: The phyllospheric microbiota is assumed to play a key role in the metabolism of host plants. Its role in determining the epiphytic and internal plant metabolome, however, remains to be investigated. We analyzed the Liquid Chromatography-Mass Spectrometry (LC-MS) profiles of the epiphytic and internal metabolomes of the leaves and flowers of Sambucus nigra with and without external antibiotic treatment application. Results: The epiphytic metabolism showed a degree of complexity similar to that of the plant organs. The suppression of microbial communities by topical applications of antibiotics had a greater impact on the epiphytic metabolome than on the internal metabolomes of the plant organs, although even the latter changed significantly both in leaves and flowers. The application of antibiotics decreased the concentration of lactate in both epiphytic and organ metabolomes, and the concentrations of citraconic acid, acetyl-CoA, isoleucine, and several secondary compounds such as terpenes and phenols in the epiphytic extracts. The metabolite pyrogallol appeared in the floral epiphytic community only after the treatment. The concentrations of the amino acid precursors of the ketoglutarate-synthesis pathway tended to decrease in the leaves and to increase in the foliar epiphytic extracts. Conclusions: These results suggest that anaerobic and/or facultative anaerobic bacteria were present in high numbers in the phyllosphere and in the apoplasts of S. nigra. The results also show that microbial communities play a significant role in the metabolomes of plant organs and could have more complex and frequent mutualistic, saprophytic, and/or parasitic relationships with internal plant metabolism than currently assumed. © 2016 Gargallo-Garriga et al.
Peñuelas, J., Sardans, J., Filella, I., Estiarte, M., Llusià, J., Ogaya, R., Carnicer, J., Bartrons, M., Rivas-Ubach, A., Grau, O., Peguero, G., Margalef, O., Pla-Rabés, S., Stefanescu, C., Asensio, D., Preece, C., Liu, L., Verger, A., Rico, L., Barbeta, A., Achotegui-Castells, A., Gargallo-Garriga, A., Sperlich, D., Farré-Armengol, G., Fernández-Martínez, M., Liu, D., Zhang, C., Urbina, I., Camino, M., Vives, M., Nadal-Sala, D., Sabaté, S., Gracia, C., Terradas, J. (2016) Assessment of the impacts of climate change on Mediterranean terrestrial ecosystems based on data from field experiments and long-term monitored field gradients in Catalonia. Environmental and Experimental Botany. : 0-0.EnlaceDoi: 10.1016/j.envexpbot.2017.05.012
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.EnlaceDoi: 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.EnlaceDoi: 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.EnlaceDoi: 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.
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