Boreal forests emit a large amount of monoterpenes into the atmosphere. Traditionally these emissions are assumed to originate as evaporation from large storage pools. Thus, their diurnal cycle would depend mostly on temperature. However, there is indication that a significant part of the monoterpene emission would originate directly from de novo synthesis. By applying 13 CO2 fumigation and analyzing the isotope fractions with proton transfer reaction mass spectrometry (PTR-MS) and classical GC-MS, we determined the fractions of monoterpene emissions originating from de novo biosynthesis in Pinus sylvestris (58%), Picea abies (33.5%), Larix decidua (9.8%) and Betula pendula (100%). Application of the observed split between de novo and pool emissions from P. sylvestris in a hybrid emission algorithm resulted in a better description of ecosystem scale monoterpene emissions from a boreal Scots pine forest stand.
This study investigates the role of volatile organic compounds in systemic acquired resistance (SAR), a salicylic acid (SA)-associated, broad-spectrum immune response in systemic, healthy tissues of locally infected plants. Gas chromatography coupled to mass spectrometry analyses of SAR-related emissions of wild-type and non-SAR-signal-producing mutant plants associated SAR with monoterpene emissions. Headspace exposure of to a mixture of the bicyclic monoterpenes α-pinene and β-pinene induced defense, accumulation of reactive oxygen species, and expression of SA- and SAR-related genes, including the SAR regulatory () gene and three of its paralogs. Pinene-induced resistance was dependent on SA biosynthesis and signaling and on Arabidopsis mutants with reduced monoterpene biosynthesis were SAR-defective but mounted normal local resistance and methyl salicylate-induced defense responses, suggesting that monoterpenes act in parallel with SA The volatile emissions from SAR signal-emitting plants induced defense in neighboring plants, and this was associated with the presence of α-pinene, β-pinene, and camphene in the emissions of the "sender" plants. Our data suggest that monoterpenes, particularly pinenes, promote SAR, acting through ROS and , and likely function as infochemicals in plant-to-plant signaling, thus allowing defense signal propagation between neighboring plants.
The 2-C-methylerythritol 4-phosphate (MEP) pathway supplies precursors for plastidial isoprenoid biosynthesis including carotenoids, redox cofactor side chains, and biogenic volatile organic compounds. We examined the first enzyme of this pathway, 1-deoxyxylulose 5-phosphate synthase (DXS), using metabolic control analysis. Multiple Arabidopsis (Arabidopsis thaliana) lines presenting a range of DXS activities were dynamically labeled with 13 CO 2 in an illuminated, climate-controlled, gas exchange cuvette. Carbon was rapidly assimilated into MEP pathway intermediates, but not into the mevalonate pathway. A flux control coefficient of 0.82 was calculated for DXS by correlating absolute flux to enzyme activity under photosynthetic steady-state conditions, indicating that DXS is the major controlling enzyme of the MEP pathway. DXS manipulation also revealed a second pool of a downstream metabolite, 2-Cmethylerythritol-2,4-cyclodiphosphate (MEcDP), metabolically isolated from the MEP pathway. DXS overexpression led to a 3-to 4-fold increase in MEcDP pool size but to a 2-fold drop in maximal labeling. The existence of this pool was supported by residual MEcDP levels detected in dark-adapted transgenic plants. Both pools of MEcDP are closely modulated by DXS activity, as shown by the fact that the concentration control coefficient of DXS was twice as high for MEcDP (0.74) as for 1-deoxyxylulose 5-phosphate (0.35) or dimethylallyl diphosphate (0.34). Despite the high flux control coefficient for DXS, its overexpression led to only modest increases in isoprenoid end products and in the photosynthetic rate. Diversion of flux via MEcDP may partly explain these findings and suggests new opportunities to engineer the MEP pathway.
The plastidic 2-C-methyl-D-erythritol-4-phosphate (MEP) pathway is one of the most important pathways in plants and produces a large variety of essential isoprenoids. Its regulation, however, is still not well understood. Using the stable isotope 13 C-labeling technique, we analyzed the carbon fluxes through the MEP pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus 3 canescens). We assessed the dependence on temperature, light intensity, and atmospheric [CO 2 ]. Isoprene biosynthesis was by far (99%) the main carbon sink of MEP pathway intermediates in mature gray poplar leaves, and its production required severalfold higher carbon fluxes compared with NE leaves with almost zero isoprene emission. To compensate for the much lower demand for carbon, NE leaves drastically reduced the overall carbon flux within the MEP pathway. Feedback inhibition of 1-deoxy-Dxylulose-5-phosphate synthase activity by accumulated plastidic dimethylallyl diphosphate almost completely explained this reduction in carbon flux. Our data demonstrate that short-term biochemical feedback regulation of 1-deoxy-D-xylulose-5-phosphate synthase activity by plastidic dimethylallyl diphosphate is an important regulatory mechanism of the MEP pathway. Despite being relieved from the large carbon demand of isoprene biosynthesis, NE plants redirected only approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. b-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.
The indirect defences of plants are comprised of herbivoreinduced plant volatiles (HIPVs) that among other things attract the natural enemies of insects. However, the actual extent of the benefits of HIPV emissions in complex co-evolved plant-herbivore systems is only poorly understood. The observation that a few Quercus robur L. trees constantly tolerated (T-oaks) infestation by a major pest of oaks (Tortrix viridana L.), compared with heavily defoliated trees (susceptible: S-oaks), lead us to a combined biochemical and behavioural study. We used these evidently different phenotypes to analyse whether the resistance of T-oaks to the herbivore was dependent on the amount and scent of HIPVs and/or differences in non-volatile polyphenolic leaf constituents (as quercetin-, kaempferol-and flavonol glycosides). In addition to non-volatile metabolic differences, typically defensive HIPV emissions differed between S-oaks and T-oaks. Female moths were attracted by the blend of HIPVs from S-oaks, showing significantly higher amounts of (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) and (E)-b-ocimene and avoid T-oaks with relative high fraction of the sesquiterpenes a-farnesene and germacrene D. Hence, the strategy of T-oaks exhibiting directly herbivore-repellent HIPV emissions instead of high emissions of predator-attracting HIPVs of the S-oaks appears to be the better mechanism for avoiding defoliation.
Salicylic acid (SA)-mediated innate immune responses are activated in plants perceiving volatile monoterpenes. Here, we show that monoterpene-associated responses are propagated in feed-forward loops involving the systemic acquired resistance (SAR) signaling components pipecolic acid, glycerol-3-phosphate, and LEGUME LECTIN-LIKE PROTEIN1 (LLP1). In this cascade, LLP1 forms a key regulatory unit in both within-plant and between-plant propagation of immunity. The data integrate molecular components of SAR into systemic signaling networks that are separate from conventional, SA-associated innate immune mechanisms. These networks are central to plant-to-plant propagation of immunity, potentially raising SAR to the population level. In this process, monoterpenes act as microbe-inducible plant volatiles, which as part of plant-derived volatile blends have the potential to promote the generation of a wave of innate immune signaling within canopies or plant stands. Hence, plant-to-plant propagation of SAR holds significant potential to fortify future durable crop protection strategies following a single volatile trigger.
BackgroundGlobally plants are the primary sink of atmospheric CO2, but are also the major contributor of a large spectrum of atmospheric reactive hydrocarbons such as terpenes (e.g. isoprene) and other biogenic volatile organic compounds (BVOC). The prediction of plant carbon (C) uptake and atmospheric oxidation capacity are crucial to define the trajectory and consequences of global environmental changes. To achieve this, the biosynthesis of BVOC and the dynamics of C allocation and translocation in both plants and ecosystems are important.MethodologyWe combined tunable diode laser absorption spectrometry (TDLAS) and proton transfer reaction mass spectrometry (PTR-MS) for studying isoprene biosynthesis and following C fluxes within grey poplar (Populus x canescens) saplings. This was achieved by feeding either 13CO2 to leaves or 13C-glucose to shoots via xylem uptake. The translocation of 13CO2 from the source to other plant parts could be traced by 13C-labeled isoprene and respiratory 13CO2 emission.Principal FindingIn intact plants, assimilated 13CO2 was rapidly translocated via the phloem to the roots within 1 hour, with an average phloem transport velocity of 20.3±2.5 cm h−1. 13C label was stored in the roots and partially reallocated to the plants' apical part one day after labeling, particularly in the absence of photosynthesis. The daily C loss as BVOC ranged between 1.6% in mature leaves and 7.0% in young leaves. Non-isoprene BVOC accounted under light conditions for half of the BVOC C loss in young leaves and one-third in mature leaves. The C loss as isoprene originated mainly (76–78%) from recently fixed CO2, to a minor extent from xylem-transported sugars (7–11%) and from photosynthetic intermediates with slower turnover rates (8–11%).ConclusionWe quantified the plants' C loss as respiratory CO2 and BVOC emissions, allowing in tandem with metabolic analysis to deepen our understanding of ecosystem C flux.
Fungi of the genus Trichoderma are economically important due to their plant growth- and performance-promoting effects, such as improved nutrient supply, mycoparasitism of plant-pathogens and priming of plant defense. Due to their mycotrophic lifestyle, however, they might also be antagonistic to other plant-beneficial fungi, such as mycorrhiza-forming species. Trichoderma spp. release a high diversity of volatile organic compounds (VOCs), which likely play a decisive role in the inter-species communication. It has been shown that Trichoderma VOCs can inhibit growth of some plant pathogens, but their inhibition potentials during early interactions with mutualistic fungi remain unknown. Laccaria bicolor is a common ectomycorrhizal fungus which in symbiotic relationship is well known to facilitate plant performance. Here, we investigated the VOC profiles of three strains of Trichoderma species, Trichoderma harzianum, Trichoderma Hamatum , and Trichoderma velutinum , as well as L. bicolor by stir bar sorptive extraction and gas chromatography – mass spectrometry (SBSE-GC-MS). We further examined the fungal performance and the VOC emission profiles during confrontation of the Trichoderma species with L. bicolor in different co-cultivation scenarios. The VOC profiles of the three Trichoderma species were highly species-dependent. T. harzianum was the strongest VOC emitter with the most diverse compound pattern, followed by T. hamatum and T. velutinum . Co-cultivation of Trichoderma spp. and L. bicolor altered the VOC emission patterns dramatically in some scenarios. The co-cultivations also revealed contact degree-dependent inhibition of one of the fungal partners. Trichoderma growth was at least partially inhibited when sharing the same headspace with L. bicolor . In direct contact between both mycelia, however, L. bicolor growth was impaired, indicating that Trichoderma and L. bicolor apply different effectors when defending their territory. Multivariate analysis demonstrated that all examined individual fungal species in axenic cultures, as well as their co-cultivations were characterized by a distinct VOC emission pattern. The results underline the importance of VOCs in fungal interactions and reveal unexpected adjustability of the VOC emissions according to the specific biotic environments.
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