Drought priming reduces Calligonum mongolicum sensitivity to recurrent droughts via coordinated regulation of osmolytes, antioxidants, and hormones.

Pre-exposure of plants to abiotic stressors may induce stress memory and improve tolerance to subsequent stresses. Here, 3-month-old Calligonum mongolicum seedlings were exposed to drought (60 days) with (primed) or without (unprimed) early drought exposure of 50 days, to determine whether this enhances seedling resistance and investigate possible underlying mechanisms. Compared to unprimed, primed seedlings had higher biomass, shoot relative water content (15% and 22%), chlorophyll a, chlorophyll b, and carotenoids. They also had more superoxide anions (O2 -• ) and H2 O2 scavenging mechanisms through higher activity of SOD, CAT, APX, and dehydroascorbate reductase in assimilating shoots and roots, resulting in less ROS and oxidative stress damage. Plants also had higher ABA and JA but lower SA, likely reflecting an adaptive response to subsequent stress. Primed seedlings accumulated more IAA and brassinosteroids, which may account for their better growth. Accumulation of glycine betaine, pro, and total amino acids in assimilating shoots and roots of primed seedlings led to reduced osmotic stress. Drivers of responses of non-primed and primed seedlings to drought varied. Responses of primed seedlings were primarily characterized by more photosynthetic pigments, increased oxidative scavenging of O2 -• and H2 O2 , more phytohormones and osmolytes. Early drought priming of drought stress memory in C. mongolicum seedlings may provide a useful management approach to improve seedling establishment in vegetation restoration programs.

Metabolomics and transcriptomics to decipher molecular mechanisms underlying ectomycorrhizal root colonization of an oak tree.

Mycorrhizas are known to have a positive impact on plant growth and ability to resist major biotic and abiotic stresses. However, the metabolic alterations underlying mycorrhizal symbiosis are still understudied. By using metabolomics and transcriptomics approaches, cork oak roots colonized by the ectomycorrhizal fungus Pisolithus tinctorius were compared with non-colonized roots. Results show that compounds putatively corresponding to carbohydrates, organic acids, tannins, long-chain fatty acids and monoacylglycerols, were depleted in ectomycorrhizal cork oak colonized roots. Conversely, non-proteogenic amino acids, such as gamma-aminobutyric acid (GABA), and several putative defense-related compounds, including oxylipin-family compounds, terpenoids and B6 vitamers were induced in mycorrhizal roots. Transcriptomic analysis suggests the involvement of GABA in ectomycorrhizal symbiosis through increased synthesis and inhibition of degradation in mycorrhizal roots. Results from this global metabolomics analysis suggest decreases in root metabolites which are common components of exudates, and in compounds related to root external protective layers which could facilitate plant-fungal contact and enhance symbiosis. Root metabolic pathways involved in defense against stress were induced in ectomycorrhizal roots that could be involved in a plant mechanism to avoid uncontrolled growth of the fungal symbiont in the root apoplast. Several of the identified symbiosis-specific metabolites, such as GABA, may help to understand how ectomycorrhizal fungi such as P. tinctorius benefit their host plants.

Nutrient scarcity as a selective pressure for mast seeding.

Mast seeding is one of the most intriguing reproductive traits in nature. Despite its potential drawbacks in terms of fitness, the widespread existence of this phenomenon suggests that it should have evolutionary advantages under certain circumstances. Using a global dataset of seed production time series for 219 plant species from all of the continents, we tested whether masting behaviour appears predominantly in species with low foliar nitrogen and phosphorus concentrations when controlling for local climate and productivity. Here, we show that masting intensity is higher in species with low foliar N and P concentrations, and especially in those with imbalanced N/P ratios, and that the evolutionary history of masting behaviour has been linked to that of nutrient economy. Our results support the hypothesis that masting is stronger in species growing under limiting conditions and suggest that this reproductive behaviour might have evolved as an adaptation to nutrient limitations and imbalances.

Atmospheric deposition, CO2, and change in the land carbon sink.

Concentrations of atmospheric carbon dioxide (CO2) have continued to increase whereas atmospheric deposition of sulphur and nitrogen has declined in Europe and the USA during recent decades. Using time series of flux observations from 23 forests distributed throughout Europe and the USA, and generalised mixed models, we found that forest-level net ecosystem production and gross primary production have increased by 1% annually from 1995 to 2011. Statistical models indicated that increasing atmospheric CO2 was the most important factor driving the increasing strength of carbon sinks in these forests. We also found that the reduction of sulphur deposition in Europe and the USA lead to higher recovery in ecosystem respiration than in gross primary production, thus limiting the increase of carbon sequestration. By contrast, trends in climate and nitrogen deposition did not significantly contribute to changing carbon fluxes during the studied period. Our findings support the hypothesis of a general CO2-fertilization effect on vegetation growth and suggest that, so far unknown, sulphur deposition plays a significant role in the carbon balance of forests in industrialized regions. Our results show the need to include the effects of changing atmospheric composition, beyond CO2, to assess future dynamics of carbon-climate feedbacks not currently considered in earth system/climate modelling.

Global patterns of phosphatase activity in natural soils.

Soil phosphatase levels strongly control the biotic pathways of phosphorus (P), an essential element for life, which is often limiting in terrestrial ecosystems. We investigated the influence of climatic and soil traits on phosphatase activity in terrestrial systems using metadata analysis from published studies. This is the first analysis of global measurements of phosphatase in natural soils. Our results suggest that organic P (Porg), rather than available P, is the most important P fraction in predicting phosphatase activity. Structural equation modeling using soil total nitrogen (TN), mean annual precipitation, mean annual temperature, thermal amplitude and total soil carbon as most available predictor variables explained up to 50% of the spatial variance in phosphatase activity. In this analysis, Porg could not be tested and among the rest of available variables, TN was the most important factor explaining the observed spatial gradients in phosphatase activity. On the other hand, phosphatase activity was also found to be associated with climatic conditions and soil type across different biomes worldwide. The close association among different predictors like Porg, TN and precipitation suggest that P recycling is driven by a broad scale pattern of ecosystem productivity capacity.

Similar local, but different systemic, metabolomic responses of closely related pine subspecies to folivory by caterpillars of the processionary moth.

Plants respond locally and systemically to herbivore attack. Most of the research conducted on plant-herbivore relationships at element and molecular levels have focused on the elemental composition or/and certain molecular compounds or specific families of defence metabolites showing that herbivores tend to select plant individuals or species with higher nutrient concentrations and avoid those with higher levels of defence compounds. We performed stoichiometric and metabolomics, both local and systemic, analyses in two subspecies of Pinus sylvestris under attack from caterpillars of the pine processionary moth, an important pest in the Mediterranean Basin. Both pine subspecies responded locally to folivory mainly by increasing relative concentrations of terpenes and some phenolics. Systemic responses differed between pine subspecies, and most of the metabolites presented intermediate concentrations between those of the affected parts and unattacked trees. Our results support the hypothesis that foliar nutrient concentrations are not a key factor for plant selection by adult female processionary moths for oviposition, since folivory was not associated with any of the elements analysed. Phenolic compounds generally did not increase in the attacked trees, questioning the suggestion of induction of phenolics following folivory attack and the anti-feeding properties of phenolics. Herbivory attack produced a general systemic shift in pines, in both primary and secondary metabolism, which was less intense and chemically different from the local responses. Local pine responses were similar between pine subspecies, while systemic responses were more distant.

Trees increase their P:N ratio with size.

AIM: Phosphorus (P) tends to become limiting in aging terrestrial ecosystems, and its resorption efficiency is higher than for other elements such as nitrogen (N). We thus hypothesized that trees should store more P than those other elements such as N when tree size increases and that this process should be enhanced in slow-growing late successional trees. LOCATION: Catalan forests. METHODS: We have used data from the Catalan Forest Inventory that contains field data of the P and N contents of total aboveground, foliar and woody biomasses of the diverse Mediterranean, temperate and alpine forests of Catalonia (1018 sites). We used correlation and general lineal models (GLM) to analyze the allometric relationships between nutrient contents of different aboveground biomass fractions (foliar, branches and stems) and total aboveground biomass. RESULTS: Aboveground forest P content increases proportionally more than aboveground forest N content with increasing aboveground biomass. Two mechanisms underlie this. First, woody biomass increases proportionally more than foliar biomass having woody biomass higher P:N ratio than foliar biomass. Second, wood P:N ratio increases with tree size. These results are consistent with the generally higher foliar resorption of P than of N. Slow-growing species accumulate more P in total aboveground with size than fast-growing species mainly as a result of their large capacity to store P in wood. MAIN CONCLUSIONS: Trees may have thus developed long-term adaptive mechanisms to store P in biomass, mainly in wood, thereby slowing the loss of P from the ecosystems, reducing its availability for competitors, and implying an increase in the P:N ratio in forest biomass with aging. This trend to accumulate more P than N with size is more accentuated in slow-growing, large, long-living species of late successional stages. This way they partly counterbalance the gradual decrease of P in the soil.

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

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 (1)H NMR-based metabolomic profiling studies to detect global metabolome shifts after wounding stress in tree leaves, and therefore its suitability in ecometabolomic studies.

Climate and taxonomy underlie different elemental concentrations and stoichiometries of forest species: the optimum "biogeochemical niche".

We previously hypothesised the existence of a "biogeochemical niche" occupied by each plant species. Different species should have a specific elemental composition, stoichiometry and allocation as a consequence of their particular metabolism, physiology and structure (morphology) linked to their optimal functioning under the environmental (abiotic and biotic) conditions where they have evolved. We tested this hypothesis using data from the Catalan Forestry Inventory that covers different forest groups growing under a large climatic gradient. Mediterranean species that occupy hotter-drier environments have lower leaf N, P and K concentrations than non-Mediterranean forest species. Within a determined climatic biome, different species competing in the same space have different elemental compositions and allocations linked to their taxonomical differences and their phenotypic plasticity. Gymnosperms have a proportionally higher elemental allocation to leaves than to wood, higher C concentrations, and lower N, P and K concentrations mainly in the stem and branches than angiosperms. The differences among species are linked to asymmetrical use of different elements, suggesting that the biogeochemical niche is a final expression and consequence of long-term species adaptation to particular abiotic factors, ecological role (stress tolerant, ruderal, competitor), different soil occupation and use of resources to avoid interspecific competition, and finally of a certain degree of flexibility to adapt to current environmental shifts.

Responses of soil nutrient concentrations and stoichiometry to different human land uses in a subtropical tidal wetland.

We studied the impacts of anthropogenic changes in land use on the stoichiometric imbalance of soil carbon (C), nitrogen (N), phosphorus (P) and potassium (K) in Phragmites australis wetlands in the Minjiang River estuary. We compared five areas with different land uses: P. australis wetland (control), grassland, a mudskipper breeding flat, pond aquaculture and rice cropland. Human activity has affected the elemental and stoichiometric compositions of soils through changes in land use. In general, soil C and N concentrations were lower and total soil K concentrations were higher at the sites under human land uses relative to the control site, and total soil P concentrations were generally not significantly different. The close relationship between total soil C and N concentrations in all cases, including fertilization with N, suggested that N was the most limiting nutrient in these wetlands. Lower soil N concentrations and similar soil P concentrations and higher soil K concentrations under human land-use activities suggest that human activity has increased the role of N limitation in these wetlands. Only grassland use increases soil N contents (only in the 0-10 cm of soil). Despite N fertilization, lower soil N concentrations were also observed in the rice cropland, indicating the difficulty of avoiding N limitation in these wetlands. The observed lower soil N:P ratio, together with higher soil P and K availabilities in rice croplands, is consistent with the tendency of human activity to change the competitive relationships of plants, in this case favoring species adapted to high rates of growth (low N:P ratio) and/or favoring plants with high demands for P and K. Both, soil C storage and respiration were higher in grasslands, likely due to the introduction of grasses, which led to a high density of plants, increased grazing activity and soil compaction. Soil C storage and respiration were lower under human land uses, except in the rice cropland, with respect to natural wetland. Using overall data, soil C storage and respiration were correlated, indicating that soil respiration was correlated with plant productivity. In this wetland area the impacts of different human land-uses on soil stoichiometry and C-cycle can be very different depending on the activity. Further regeneration of natural communities can be determined by the previous type of land-use.

Plant-soil interactions in Mediterranean forest and shrublands: impacts of climatic change.

BACKGROUND: In the Mediterranean climate, plants have evolved under conditions of low soil-water and nutrient availabilities and have acquired a series of adaptive traits that, in turn exert strong feedback on soil fertility, structure, and protection. As a result, plant-soil systems constitute complex interactive webs where these adaptive traits allow plants to maximize the use of scarce resources. SCOPE: It is necessary to review the current bibliography to highlight the most know characteristic mechanisms underlying Mediterranean plant-soil feed-backs and identify the processes that merit further research in order to reach an understanding of the plant-soil feed-backs and its capacity to cope with future global change scenarios. In this review, we characterize the functional and structural plant-soil relationships and feedbacks in Mediterranean regions. We thereafter discuss the effects of global change drivers on these complex interactions between plants and soil. CONCLUSIONS: The large plant diversity that characterizes Mediterranean ecosystems is associated to the success of coexisting species in avoiding competition for soil resources by differential exploitation in space (soil layers) and time (year and daily). Among plant and soil traits, high foliar nutrient re-translocation and large contents of recalcitrant compounds reduce nutrient cycling. Meanwhile increased allocation of resources to roots and soil enzymes help to protect against soil erosion and to improve soil fertility and capacity to retain water. The long-term evolutionary adaptation to drought of Mediterranean plants allows them to cope with moderate increases of drought without significant losses of production and survival in some species. However, other species have proved to be more sensitive decreasing their growth and increasing their mortality under moderate rising of drought. All these increases contribute to species composition shifts. Moreover, in more xeric sites, the desertification resulting from synergic interactions among some related process such as drought increases, torrential rainfall increases and human driven disturbances is an increasing concern. A research priority now is to discern the effects of long-term increases in atmospheric CO2 concentrations, warming, and drought on soil fertility and water availability and on the structure of soil communities (e.g. shifts from bacteria to fungi) and on patching vegetation and root-water uplift (from soil to plant and from soil deep layers to soil superficial layers) roles in desertification.

Higher allocation to low cost chemical defenses in invasive species of Hawaii.

The capacity to produce carbon-based secondary compounds (CBSC), such as phenolics (including tannins) and terpenes as defensive compounds against herbivores or against neighboring competing plants can be involved in the competition between alien and native plant species. Since the Hawaiian Islands are especially vulnerable to invasions by alien species, we compared total phenolic (TP), total tannin (Tta), and total terpene (TT) leaf contents of alien and native plants on Oahu Island (Hawaii). We analyzed 35 native and 38 alien woody plant species randomly chosen among representative current Hawaiian flora. None of these CBSC exhibited phylogenetic fingerprinting. Alien species had similar leaf TP and leaf Tta contents, and 135% higher leaf TT contents compared with native species. Alien plants had 80% higher leaf TT:N leaf content ratio than native plants. The results suggest that apart from greater growth rate and greater nutrient use, alien success in Oahu also may be linked to greater contents of low cost chemical defenses, such as terpenes, as expected in faster-growing species in resource rich regions. The higher TT contents in aliens may counterbalance their lower investment in leaf structural defenses and their higher leaf nutritional quality. The higher TT provides higher effectiveness in deterring the generalist herbivores of the introduced range, where specialist herbivores are absent. In addition, higher TT contents may favor aliens conferring higher protection against abiotic and biotic stressors. The higher terpene accumulation was independent of the alien species origin, which indicates that being alien either selects for higher terpene contents post-invasion, or that species with high terpene contents are pre-adapted to invasiveness. Although less likely, an originally lower terpene accumulation in Hawaiian than in continental plants that avoids the increased attraction of specialist enemies associated to terpenes may not be discarded.

Increased eutrophication and nutrient imbalances in the agricultural soil of NE Catalonia, Spain.

The soil C, N, P and K content of agricultural soil were measured over the last 4 decades in NE Catalonia (NE Spain). Plant-available P and K increased by ca 109 and 105% respectively and total N decreased by 30%. The increases in plant-available P content are in accordance with the increasingly used pig slurry being very rich in P, and with P tendency to be retained in soils, since it is less mobile than N. The total soil N (N(tot)) decrease occurred in the first decade (by 41%). The uptake and withdrawal of mineral N by crops and the leaching of mineral N into groundwater and rivers after torrential rainfalls were the two likely major pathways of N-loss from the soil. After the first decade, there has been no further decrease of N(tot) as a result of the increasing fertilization of these fields, including the increasing applications of pig slurry. These results show an increasing P eutrophication in Mediterranean agricultural soils and will have several consequences for the next decades with (i) an increasing unbalance between N and P (and K) in soils that might affect crop productivity (ii) an increasing leaching of N as nitrate to continental waters, both ground and surface waters, and (iii) a consequent need for the establishment of another fertilization strategy based on lowering the use of pig slurry and on increasing the use of fertilizers of slow mineralization that increase soil organic matter, and stabilise the soil N and P contents.

Root-surface phosphatase activity in shrublands across a European gradient: effects of warming.

Root-surface phosphatase activities were measured in natural and semi-natural shrublands across an European climatic gradient of temperature and rainfall including Wales (WL), Denmark (DK), Netherlands (NL), Hungary (HU), Italy (IT) and Spain (SP). In each site a warming experiment was conducted since 1999 or 2001 by means of passive night-time warming using reflective curtains that covered the vegetation at night. The treatments increased yearly average soil temperatures around 0. 8 degrees C in most of sites. Root-surface phosphatase activity values ranged between 56 mg PNP g(-1) h(-1) in IT and 3.5 mg PNP g(-1) h(-1) in HU. Warming had no effect on root-surface phosphatase activity across the sites and only in Hungary a slight increase was detected. Plants at Mediterranean sites (IT, SP) showed a higher root-surface phosphatase activity than plants at temperate sites (WL, NL, DK). We suggest it might be an adaptation of plant species evolved under Mediterranean climate that allows them a) to compensate in wet period for the decrease in phosphatase activity, and thus P uptake, during drought periods, and/or b) to benefit from soluble organic P flushes following the frequent drying-rewetting episodes experienced by soils in Mediterranean ecosystems.

Warming and drought change trace element bioaccumulation patterns in a Mediterranean shrubland.

A field experiment consisting of drought and warming manipulation was conducted in a Mediterranean shrubland dominated by the shrubs Erica multiflora and Globularia alypum. The aim was to investigate the effects of the climatic changes predicted by IPCC models for the coming decades on trace element concentration and accumulation in aboveground biomass, plant litter, and soil. Warming increased concentrations and aboveground accumulation of some trace elements related to plant root uptake, such as Al, As, Cr, Cu, and partially Pb. This effect was more general in E. multiflora than in G. alypum. The stronger effects were increases in Al leaf concentrations (42%) and aboveground accumulation (500gha(-1)) in E. multiflora, in As stem biomass accumulation (0.2gha(-1)) in E. multiflora, and in Cr leaf concentrations (51%) in G. alypum and stem aboveground accumulation in E. multiflora (1.1gha(-1)). These species-specific increases were related to greater retranslocation, photosynthetic capacity and growth in E. multiflora than in G. alypum. Warming decreased the concentrations of some trace elements in leaf litter, implying the existence of an increased leaf retranslocation. Drought increased As (40%) and Cd (55%) in E. multiflora stems, whereas it decreased Cu (50%) in leaves, Ni (28%) in stems and Pb (32%) in leaf litter of G. alypum. The increasing concentrations of some trace elements in E. multiflora and not in G. alypum were related to a greater growth reduction in E. multiflora than in G. alypum. Warming increased As soil solubility (67%) and decreased total soil As (21%). Those changes were related to a greater Fe mobilization in warming plot and to a greater plant capture. Drought increased Hg (350%) concentrations in soils but had no significant effects on trace element accumulation in aboveground biomass. The different response to warming and drought in the two dominant species implies uneven changes in the quality of the plant tissues that may have implications for herbivores. This may be specially important for the performance of the studied Mediterranean ecosystems under the warmer and drier conditions predicted by the next decades by the GCM and ecophysiological models.

Drought changes the dynamics of trace element accumulation in a Mediterranean Quercus ilex forest.

We conducted a field drought manipulation experiment in an evergreen oak Mediterranean forest from 1999 to 2005 to investigate the effects of the increased drought predicted for the next decades on the accumulation of trace elements that can be toxic for animals, in stand biomass, litter and soil. Drought increased concentrations of As, Cd, Ni, Pb and Cr in roots of the dominant tree species, Quercus ilex, and leaf Cd concentrations in Arbutus unedo and of Phillyrea latifolia codominant shrubs. The increased concentration of As and Cd can aggravate the toxic capacity of those two elements, which are already next or within the levels that have been shown to be toxic for herbivores. The study also showed a great reduction in Pb biomass content (100-135 gha(-1)) during the studied period (1999-2005) showing the effectiveness of the law that prohibited leaded fuel after 2001. The results also indicate that drought increases the exportation of some trace elements to continental waters.