Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota

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.
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Doi: 10.1186/s12870-016-0767-7

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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.

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Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions

Sardans J., Janssens I.A., Alonso R., Veresoglou S.D., Rillig M.C., Sanders T.G.M., Carnicer J., Filella I., Farre-Armengol G., Penuelas J. (2015) Foliar elemental composition of European forest tree species associated with evolutionary traits and present environmental and competitive conditions. Global Ecology and Biogeography. 24: 240-255.
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Doi: 10.1111/geb.12253

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Aim: Plant elemental composition and stoichiometry are crucial for plant structure and function. We studied to what extent elemental stoichiometry in plants might be strongly related to environmental drivers and competition from coexisting species. Location: Europe. Methods: We analysed foliar N, P, K, Ca and Mg concentrations and their ratios among 50 species of European forest trees sampled in 5284 plots across Europe and their relationships with phylogeny, forest type, current climate and N deposition. Results: Phylogeny is strongly related to overall foliar elemental composition in European tree species. Species identity explained 56.7% of the overall foliar elemental composition and stoichiometry. Forest type and current climatic conditions also partially explained the differences in foliar elemental composition among species. In the same genus co-occurring species had overall higher differences in foliar elemental composition and stoichiometry than the non-co-occurring species. Main conclusions: The different foliar elemental compositions among species are related to phylogenetic distances, but they are also related to current climatic conditions, forest types, drivers of global change such as atmospheric N deposition, and to differences among co-occurring species as a probable consequence of niche specialization to reduce direct competition for the same resources. Different species have their own 'fixed' foliar elemental compositions but retain some degree of plasticity to the current climatic and competitive conditions. A wider set of elements beyond N and P better represent the biogeochemical niche and are highly sensitive to plant function. Foliar elemental composition can thus be useful for representing important aspects of plant species niches. © 2014 John Wiley & Sons Ltd.

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A tethered-balloon PTRMS sampling approach for surveying of landscape-scale biogenic VOC fluxes

Greenberg J.P., Penuelas J., Guenther A., Seco R., Turnipseed A., Jiang X., Filella I., Estiarte M., Sardans J., Ogaya R., Llusia J., Rapparini F. (2014) A tethered-balloon PTRMS sampling approach for surveying of landscape-scale biogenic VOC fluxes. Atmospheric Measurement Techniques. 7: 2263-2271.
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Doi: 10.5194/amt-7-2263-2014

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Landscape-scale fluxes of biogenic gases were surveyed by deploying a 100 m Teflon tube attached to a tethered balloon as a sampling inlet for a fast-response proton-transfer-reaction mass spectrometer (PTRMS). Along with meteorological instruments deployed on the tethered balloon and a 3 m tripod and outputs from a regional weather model, these observations were used to estimate landscape-scale biogenic volatile organic compound fluxes with two micrometeorological techniques: mixed layer variance and surface layer gradients. This highly mobile sampling system was deployed at four field sites near Barcelona to estimate landscape-scale biogenic volatile organic compound (BVOC) emission factors in a relatively short period (3 weeks). The two micrometeorological techniques were compared with emissions predicted with a biogenic emission model using site-specific emission factors and land-cover characteristics for all four sites. The methods agreed within the uncertainty of the techniques in most cases, even though the locations had considerable heterogeneity in species distribution and complex terrain. Considering the wide range in reported BVOC emission factors for individual vegetation species (more than an order of magnitude), this temporally short and inexpensive flux estimation technique may be useful for constraining BVOC emission factors used as model inputs. © 2014 Author(s).

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Removal of floral microbiota reduces floral terpene emissions

Peñuelas J., Farré-Armengol G., Llusia J., Gargallo-Garriga A., Rico L., Sardans J., Terradas J., Filella I. (2014) Removal of floral microbiota reduces floral terpene emissions. Scientific Reports. 4: 0-0.
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Doi: 10.1038/srep06727

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The emission of floral terpenes plays a key role in pollination in many plant species. We hypothesized that the floral phyllospheric microbiota could significantly influence these floral terpene emissions because microorganisms also produce and emit terpenes. We tested this hypothesis by analyzing the effect of removing the microbiota from flowers. We fumigated Sambucus nigra L. plants, including their flowers, with a combination of three broad-spectrum antibiotics and measured the floral emissions and tissular concentrations in both antibiotic-fumigated and non-fumigated plants. Floral terpene emissions decreased by ca. two thirds after fumigation. The concentration of terpenes in floral tissues did not decrease, and floral respiration rates did not change, indicating an absence of damage to the floral tissues. The suppression of the phyllospheric microbial communities also changed the composition and proportion of terpenes in the volatile blend. One week after fumigation, the flowers were not emitting β-ocimene, linalool, epoxylinalool, and linalool oxide. These results show a key role of the floral phyllospheric microbiota in the quantity and quality of floral terpene emissions and therefore a possible key role in pollination.

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Metabolic responses of Quercus ilex seedlings to wounding analysed with nuclear magnetic resonance profiling

Sardans J., Gargallo-Garriga A., Perez-Trujillo M., Parella T.J., Seco R., Filella I., Penuelas J. (2014) Metabolic responses of Quercus ilex seedlings to wounding analysed with nuclear magnetic resonance profiling. Plant Biology. 16: 395-403.
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Doi: 10.1111/plb.12032

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Plants defend themselves against herbivory at several levels. One of these is the synthesis of inducible chemical defences. Using NMR metabolomic techniques, we studied the metabolic changes of plant leaves after a wounding treatment simulating herbivore attack in the Mediterranean sclerophyllous tree Quercus ilex. First, an increase in glucose content was observed in wounded plants. There was also an increase in the content of C-rich secondary metabolites such as quinic acid and quercitol, both related to the shikimic acid pathway and linked to defence against biotic stress. There was also a shift in N-storing amino acids, from leucine and isoleucine to asparagine and choline. The observed higher content of asparagine is related to the higher content of choline through serine that was proved to be the precursor of choline. Choline is a general anti-herbivore and pathogen deterrent. The study shows the rapid metabolic response of Q. ilex in defending its leaves, based on a rapid increase in the production of quinic acid, quercitol and choline. The results also confirm the suitability of 1H NMR-based metabolomic profiling studies to detect global metabolome shifts after wounding stress in tree leaves, and therefore its suitability in ecometabolomic studies. © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Intensive measurements of gas, water, and energy exchange between vegetation and troposphere during the MONTES campaign in a vegetation gradient from short semi-desertic shrublands to tall wet temperate forests in the NW Mediterranean Basin

Penuelas J., Guenther A., Rapparini F., Llusia J., Filella I., Seco R., Estiarte M., Mejia-Chang M., Ogaya R., Ibanez J., Sardans J., Castano L.M., Turnipseed A., Duhl T., Harley P., Vila J., Estavillo J.M., Menendez S., Facini O., Baraldi R., Geron C., Mak J., Patton E.G., Jiang X., Greenberg J. (2013) Intensive measurements of gas, water, and energy exchange between vegetation and troposphere during the MONTES campaign in a vegetation gradient from short semi-desertic shrublands to tall wet temperate forests in the NW Mediterranean Basin. Atmospheric Environment. 75: 348-364.
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Doi: 10.1016/j.atmosenv.2013.04.032

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MONTES ("Woodlands") was a multidisciplinary international field campaign aimed at measuring energy, water and especially gas exchange between vegetation and atmosphere in a gradient from short semi-desertic shrublands to tall wet temperate forests in NE Spain in the North Western Mediterranean Basin (WMB). The measurements were performed at a semidesertic area (Monegros), at a coastal Mediterranean shrubland area (Garraf), at a typical Mediterranean holm oak forest area (Prades) and at a wet temperate beech forest (Montseny) during spring (April 2010) under optimal plant physiological conditions in driest-warmest sites and during summer (July 2010) with drought and heat stresses in the driest-warmest sites and optimal conditions in the wettest-coolest site. The objective of this campaign was to study the differences in gas, water and energy exchange occurring at different vegetation coverages and biomasses. Particular attention was devoted to quantitatively understand the exchange of biogenic volatile organic compounds (BVOCs) because of their biological and environmental effects in the WMB. A wide range of instruments (GC-MS, PTR-MS, meteorological sensors, O3 monitors,. .) and vertical platforms such as masts, tethered balloons and aircraft were used to characterize the gas, water and energy exchange at increasing footprint areas by measuring vertical profiles. In this paper we provide an overview of the MONTES campaign: the objectives, the characterization of the biomass and gas, water and energy exchange in the 4 sites-areas using satellite data, the estimation of isoprene and monoterpene emissions using MEGAN model, the measurements performed and the first results. The isoprene and monoterpene emission rates estimated with MEGAN and emission factors measured at the foliar level for the dominant species ranged from about 0 to 0.2mgm-2h-1 in April. The warmer temperature in July resulted in higher model estimates from about 0 to ca. 1.6mgm-2h-1 for isoprene and ca. 4.5mgm-2h-1 for monoterpenes, depending on the site vegetation and footprint area considered. There were clear daily and seasonal patterns with higher emission rates and mixing ratios at midday and summer relative to early morning and early spring. There was a significant trend in CO2 fixation (from 1 to 10mgCm-2d-1), transpiration (from1-5kgCm-2d-1), and sensible and latent heat from the warmest-driest to the coolest-wettest site. The results showed the strong land-cover-specific influence on emissions of BVOCs, gas, energy and water exchange, and therefore demonstrate the potential for feed-back to atmospheric chemistry and climate. •We present a multidisciplinary biosphere-atmosphere field campaign.•We measured a gradient from semi-desertic shrublands to wet temperate forests.•A wide range of instruments and vertical platforms were used.•Land cover strongly influenced emissions of BVOCs and gas, energy and water exchange.•Vegetation has strong potential for feed-back to atmospheric chemistry and climate. © 2013 Elsevier Ltd.

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Evidence of current impact of climate change on life: A walk from genes to the biosphere

Penuelas J., Sardans J., Estiarte M., Ogaya R., Carnicer J., Coll M., Barbeta A., Rivas-Ubach A., Llusia J., Garbulsky M., Filella I., Jump A.S. (2013) Evidence of current impact of climate change on life: A walk from genes to the biosphere. Global Change Biology. 19: 2303-2338.
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Doi: 10.1111/gcb.12143

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We review the evidence of how organisms and populations are currently responding to climate change through phenotypic plasticity, genotypic evolution, changes in distribution and, in some cases, local extinction. Organisms alter their gene expression and metabolism to increase the concentrations of several antistress compounds and to change their physiology, phenology, growth and reproduction in response to climate change. Rapid adaptation and microevolution occur at the population level. Together with these phenotypic and genotypic adaptations, the movement of organisms and the turnover of populations can lead to migration toward habitats with better conditions unless hindered by barriers. Both migration and local extinction of populations have occurred. However, many unknowns for all these processes remain. The roles of phenotypic plasticity and genotypic evolution and their possible trade-offs and links with population structure warrant further research. The application of omic techniques to ecological studies will greatly favor this research. It remains poorly understood how climate change will result in asymmetrical responses of species and how it will interact with other increasing global impacts, such as N eutrophication, changes in environmental N : P ratios and species invasion, among many others. The biogeochemical and biophysical feedbacks on climate of all these changes in vegetation are also poorly understood. We here review the evidence of responses to climate change and discuss the perspectives for increasing our knowledge of the interactions between climate change and life. © 2013 John Wiley & Sons Ltd.

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Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves

Peñuelas J., Sardans J., Stefanescu C., Parella T., Filella I. (2006) Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves. Journal of Chemical Ecology. 32: 1925-1933.
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Doi: 10.1007/s10886-006-9118-8

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We tested in the field the hypothesis that the specialist butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae, Melitaeinae) lays eggs on leaves of Lonicera implexa (Caprifoliaceae) plants with greater iridoid concentrations. We conducted our investigations in a Mediterranean site by analyzing leaves with and without naturally laid egg clusters. There were no significant differences in iridoid glycoside concentrations between leaves from plants that did not receive eggs and the unused leaves from plants receiving eggs, a fact that would seem to indicate that E. aurinia butterflies do not choose plants for oviposition by their iridoid content. However, the leaves of L. implexa that bore egg clusters had dramatically greater (over 15-fold) concentrations of iridoid glycosides than the directly opposite leaves on the same plant. These huge foliar concentrations of iridoids (15% leaf dry weight) may provide specialist herbivores with compounds that they either sequester for their own defense or use as a means of avoiding competition for food from generalist herbivores. Nevertheless, it may still be possible that these high concentrations are detrimental to the herbivore, even if the herbivore is a specialist feeder on the plant. © Springer Science + Business Media, Inc. 2006.

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