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

Resum:

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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The foliar microbiome

Penuelas J., Terradas J. (2014) The foliar microbiome. Trends in Plant Science. 19: 278-280.
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Doi: 10.1016/j.tplants.2013.12.007

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Proficient performance in plants is strongly associated with distinct microbial communities that live in and on their organs. We comment here on the current knowledge of the composition of the foliar microbiome, highlight its importance for plants, ecosystemic functioning, and crop yields, and propose tools and experiments to overcome the current knowledge gap© 2013 Elsevier Ltd.

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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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Community structures of N2-fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought

Rico L., Ogaya R., Terradas J., Penuelas J. (2014) Community structures of N2-fixing bacteria associated with the phyllosphere of a Holm oak forest and their response to drought. Plant Biology. 16: 586-593.
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Doi: 10.1111/plb.12082

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Biological nitrogen (N) fixation is a key pathway in terrestrial ecosystems and is therefore critical for understanding the responses of ecosystems to global environmental changes. The free-living diazotrophic community is distributed along the canopy-to-soil profile, but the ecological significance of epiphyllic N2 fixers, despite their functional relevance, on plant foliar surfaces remains very poorly understood compared with the N2-fixing community in forest litter and soils. We assessed the community structure of N2 fixers and overall bacteria by genetic fingerprinting (t-RFLP) to explore the seasonal successional patterns of the microbial community in the natural phyllosphere of a Holm oak (Quercus ilex) forest submitted to 12-year field experiment of rain exclusion mimicking the conditions of drought projected for the coming decades. Leaves of Holm oak were analysed in different seasons over a period of 1.5 years. The bacterial community of the phyllosphere did not correspond to the surrounding soil biome in the same area. These analyses provided field evidence for the presence of free-living diazotrophs associated with the tissues of leaves of Holm oak, the dominant tree species of many Mediterranean forests. The results also revealed that the community composition is affected seasonally and inter-annually by the environment, and that the composition shifts in response to climate change. Drought treatment increased the richness of the epiphyllic microbial community, especially during the summer. These changes were associated with higher C:N ratios of leaves observed in response to drought in semiarid areas. This epiphyllic microbiota that can potentially fix N2 extends the capacity of plants to adapt to the environment. © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Physical ecology: The search for life law

Penuelas J., Terradas J. (2013) Physical ecology: The search for life law. Open Ecology Journal. 6: 7-9.
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Doi: 10.2174/1874213020130516001

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Life on Earth is the result of a continuous accumulation of information by combination and innovation riding on endo and exosomatic energy gradients and discontinuous destructions. © Penuelas and Terradas; Licensee Bentham Open.

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Ecosystemic and biospheric interactions with carbon cycle

Peñuelas J, Filella I, Estiarte M, Ogaya R, Llusià J, Sardans J, Jump A, Carnicer J, Rico L, Garbulsky M, Coll M, Díaz de Quijano M, Seco R, Rivas-Ubach A, Kefauver S, Barbeta A, Achoategui A, Mejía-Chang M, Gallardo A, Farre G, Fernández M, Terradas J (2012) Ecosystemic and biospheric interactions with carbon cycle. In Carbon dioxide budget: processes and tendencies symposium. Universitat Politècnica de Catalunya, May 23-25.

Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest

Peñuelas J., Rico L., Ogaya R., Jump A.S., Terradas J. (2012) Summer season and long-term drought increase the richness of bacteria and fungi in the foliar phyllosphere of Quercus ilex in a mixed Mediterranean forest. Plant Biology. 14: 565-575.
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Doi: 10.1111/j.1438-8677.2011.00532.x

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We explored the changes in richness, diversity and evenness of epiphytic (on the leaf surface) and endophytic (within leaf tissues) bacteria and fungi in the foliar phyllosphere of Quercus ilex, the dominant tree species of Mediterranean forests. Bacteria and fungi were assessed during ontogenic development of the leaves, from the wet spring to the dry summer season in control plots and in plots subjected to drought conditions mimicking those projected for future decades. Our aim was to monitor succession in microbiota during the colonisation of plant leaves and its response to climate change. Ontogeny and seasonality exerted a strong influence on richness and diversity of the microbial phyllosphere community, which decreased in summer in the whole leaf and increased in summer in the epiphytic phyllosphere. Drought precluded the decrease in whole leaf phyllosphere diversity and increased the rise in the epiphytic phyllosphere. Both whole leaf bacterial and fungal richness decreased with the decrease in physiological activity and productivity of the summer season in control trees. As expected, the richness of epiphytic bacteria and fungi increased in summer after increasing time of colonisation. Under summer dry conditions, there was a positive relationship between TRF (terminal restriction fragments) richness and drought, both for whole leaf and epiphytic phyllosphere, and especially for fungal communities. These results demonstrate that changes in climate are likely to significantly alter microbial abundance and composition of the phyllosphere. Given the diverse functions and large number of phyllospheric microbes, the potential functional implications of such community shifts warrant exploration. © 2012 German Botanical Society and The Royal Botanical Society of the Netherlands.

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Llebot E. (ed). Impactes, vulnerabilitat i retroalimentacions climàtiques als ecosistemes terrestres catalans. Segon informe sobre el canvi climàtic a Catalunya.

Peñuelas J, Filella I, Estiarte M, Ogaya R, Llusià J, Sardans J, Jump A, Curiel J, Carnicer J, Rutishauser T, Rico L, Keenan T, Garbulsky M, Coll M, Diaz de Quijano M, Seco R, Rivas-Ubach A, Silva J, Boada M, Stefanescu C, Lloret F, Terradas J (2011) Llebot E. (ed). Impactes, vulnerabilitat i retroalimentacions climàtiques als ecosistemes terrestres catalans. Segon informe sobre el canvi climàtic a Catalunya. Institut d'Estudis Catalans i Generalitat de Catalunya. Barcelona, pp. 373-407.

Misleading ideas about top-down and bottom-up control in communities and the role of omnivores.

Terradas J, Peñuelas J (2011) Misleading ideas about top-down and bottom-up control in communities and the role of omnivores. Polish Journal of Ecology 59: 381-389

Solving the conundrum of plant species coexistence: Water in space and time matters most

Peñuelas J., Terradas J., Lloret F. (2011) Solving the conundrum of plant species coexistence: Water in space and time matters most. New Phytologist. 189: 5-8.
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Doi: 10.1111/j.1469-8137.2010.03570.x

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[No abstract available]

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