Plant isoprene emissions are known to contribute to abiotic stress tolerance, especially during episodes of high temperature and drought, and during cellular oxidative stress. Recent studies have ...shown that genetic transformations to add or remove isoprene emissions cause a cascade of cellular modifications that include known signaling pathways, and interact to remodel adaptive growth-defense tradeoffs. The most compelling evidence for isoprene signaling is found in the shikimate and phenylpropanoid pathways, which produce salicylic acid, alkaloids, tannins, anthocyanins, flavonols and other flavonoids; all of which have roles in stress tolerance and plant defense. Isoprene also influences key gene expression patterns in the terpenoid biosynthetic pathways, and the jasmonic acid, gibberellic acid and cytokinin signaling networks that have important roles in controlling inducible defense responses and influencing plant growth and development, particularly following defoliation. In this synthesis paper, using past studies of transgenic poplar, tobacco and
Arabidopsis
, we present the evidence for isoprene acting as a metabolite that coordinates aspects of cellular signaling, resulting in enhanced chemical defense during periods of climate stress, while minimizing costs to growth. This perspective represents a major shift in our thinking away from direct effects of isoprene, for example, by changing membrane properties or quenching ROS, to indirect effects, through changes in gene expression and protein abundances. Recognition of isoprene's role in the growth-defense tradeoff provides new perspectives on evolution of the trait, its contribution to plant adaptation and resilience, and the ecological niches in which it is most effective.
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 ¹³C-labeling technique, we analyzed the carbon fluxes through the pathway and into the major plastidic isoprenoid products in isoprene-emitting and transgenic isoprene-nonemitting (NE) gray poplar (Populus × canescens). We assessed the dependence on temperature, light intensity, and atmospheric CO₂. Isoprene biosynthesis was by far (99%) the main carbon sink of 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 approximately 0.5% of this saved carbon toward essential nonvolatile isoprenoids, i.e. β-carotene and lutein, most probably to compensate for the absence of isoprene and its antioxidant properties.
Fungi of the genus
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.
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
VOCs can inhibit growth of some plant pathogens, but their inhibition potentials during early interactions with mutualistic fungi remain unknown.
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
species,
, and
, as well as
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
species with
in different co-cultivation scenarios. The VOC profiles of the three
species were highly species-dependent.
was the strongest VOC emitter with the most diverse compound pattern, followed by
and
. Co-cultivation of
spp. and
altered the VOC emission patterns dramatically in some scenarios. The co-cultivations also revealed contact degree-dependent inhibition of one of the fungal partners.
growth was at least partially inhibited when sharing the same headspace with
. In direct contact between both mycelia, however,
growth was impaired, indicating that
and
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.
Plant–pathogen interactions have been widely studied, but mostly from the site of the plant secondary defense. Less is known about the effects of pathogen infection on plant primary metabolism. The ...possibility to transform a fluorescing protein into prokaryotes is a promising phenotyping tool to follow a bacterial infection in plants in a noninvasive manner. In the present study, virulent and avirulent
Pseudomonas syringae
strains were transformed with green fluorescent protein (GFP) to follow the spread of bacteria
in vivo
by imaging Pulse-Amplitude-Modulation (PAM) fluorescence and conventional binocular microscopy. The combination of various wavelengths and filters allowed simultaneous detection of GFP-transformed bacteria, PAM chlorophyll fluorescence, and phenolic fluorescence from pathogen-infected plant leaves. The results show that fluorescence imaging allows spatiotemporal monitoring of pathogen spread as well as phenolic and chlorophyll fluorescence
in situ
, thus providing a novel means to study complex plant–pathogen interactions and relate the responses of primary and secondary metabolism to pathogen spread and multiplication. The study establishes a deeper understanding of imaging data and their implementation into disease screening.
Abstract
Fungi produce a wide variety of volatile organic compounds (VOCs), which play central roles in the initiation and regulation of fungal interactions. Here we introduce a global overview of ...fungal VOC patterns and chemical diversity across phylogenetic clades and trophic modes. The analysis is based on measurements of comprehensive VOC profiles of forty-three fungal species. Our data show that the VOC patterns can describe the phyla and the trophic mode of fungi. We show different levels of phenotypic integration (PI) for different chemical classes of VOCs within distinct functional guilds. Further computational analyses reveal that distinct VOC patterns can predict trophic modes, (non)symbiotic lifestyle, substrate-use and host-type of fungi. Thus, depending on trophic mode, either individual VOCs or more complex VOC patterns (i.e., chemical communication displays) may be ecologically important. Present results stress the ecological importance of VOCs and serve as prerequisite for more comprehensive VOCs-involving ecological studies.
Plant growth and development can be influenced by mutualistic and non-mutualistic microorganisms. We investigated the ability of the ericoid endomycorrhizal fungus Oidiodendron maius to influence ...growth and development of the non-host plant Arabidopsis thaliana. Different experimental setups (non-compartmented and compartmented co-culture plates) were used to investigate the influence of both soluble and volatile fungal molecules on the plant phenotype. O. maius promoted growth of A. thaliana in all experimental setups. In addition, a peculiar clumped root phenotype, characterized by shortening of the primary root and by an increase of lateral root length and number, was observed in A. thaliana only in the non-compartmented plates, suggesting that soluble diffusible molecules are responsible for this root morphology. Fungal auxin does not seem to be involved in plant growth promotion and in the clumped root phenotype because co-cultivation with O. maius did not change auxin accumulation in plant tissues, as assessed in plants carrying the DR5::GUS reporter construct. In addition, no correlation between the amount of fungal auxin produced and the plant root phenotype was observed in an O. maius mutant unable to induce the clumped root phenotype in A. thaliana. Addition of active charcoal, a VOC absorbant, in the compartmented plates did not modify plant growth promotion, suggesting that VOCs are not involved in this phenomenon. The low VOCs emission measured for O. maius further corroborated this hypothesis. By contrast, the addition of CO2 traps in the compartmented plates drastically reduced plant growth, suggesting involvement of fungal CO2 in plant growth promotion. Other mycorrhizal fungi, as well as a saprotrophic and a pathogenic fungus, were also tested with the same experimental setups. In the non-compartmented plates, most fungi promoted A. thaliana growth and some could induce the clumped root phenotype. In the compartmented plate experiments, a general induction of plant growth was observed for most other fungi, especially those producing higher biomass, further strengthening the role of a nonspecific mechanism, such as CO2 emission.
Pseudomonas
sp. SCA7, characterized in this study, was isolated from roots of the bread wheat
Triticum aestivum
. Sequencing and annotation of the complete SCA7 genome revealed that it represents a ...potential new
Pseudomonas
sp. with a remarkable repertoire of plant beneficial functions.
In vitro
and
in planta
experiments with the reference dicot plant
A. thaliana
and the original monocot host
T. aestivum
were conducted to identify the functional properties of SCA7. The isolate was able to colonize roots, modify root architecture, and promote growth in
A. thaliana
. Moreover, the isolate increased plant fresh weight in
T. aestivum
under unchallenged conditions. Gene expression analysis of SCA7-inoculated
A. thaliana
indicated a role of SCA7 in nutrient uptake and priming of plants. Moreover, confrontational assays of SCA7 with fungal and bacterial plant pathogens revealed growth restriction of the pathogens by SCA7 in direct as well as indirect contact. The latter indicated involvement of microbial volatile organic compounds (mVOCs) in this interaction. Gas chromatography-mass spectrometry (GC-MS) analyses revealed 1-undecene as the major mVOC, and octanal and 1,4-undecadiene as minor abundant compounds in the emission pattern of SCA7. Additionally, SCA7 enhanced resistance of
A. thaliana
against infection with the plant pathogen
Pseudomonas syringae pv. tomato
DC3000. In line with these results, SA- and JA/ET-related gene expression in
A. thaliana
during infection with
Pst
DC3000 was upregulated upon treatment with SCA7, indicating the ability of SCA7 to induce systemic resistance. The thorough characterization of the novel
Pseudomonas
sp. SCA7 showed a remarkable genomic and functional potential of plant beneficial traits, rendering it a promising candidate for application as a biocontrol or a biostimulation agent.
Plants are continuously interacting with other organisms to optimize their performance in a changing environment. Mycorrhization is known to affect the plant growth and nutrient status, but it also ...can lead to adjusted plant defense and alter interactions with other trophic levels. Here, we studied the effect of
-mycorrhization on the poplar (
x
) metabolome and volatilome on trees with and without a poplar leaf beetle (
) infestation. We analyzed the leaf and root metabolomes employing liquid chromatography-mass spectrometry, and the leaf volatilome employing headspace sorptive extraction combined with gas-chromatography-mass spectrometry. Mycorrhization caused distinct metabolic adjustments in roots, young/infested leaves and old/not directly infested leaves. Mycorrhization adjusted the lipid composition, the abundance of peptides and, especially upon herbivory, the level of various phenolic compounds. The greatest change in leaf volatile organic compound (VOC) emissions occurred four to eight days following the beetle infestation. Together, these results prove that mycorrhization affects the whole plant metabolome and may influence poplar aboveground interactions. The herbivores and the mycorrhizal fungi interact with each other indirectly through a common host plant, a result that emphasizes the importance of community approach in chemical ecology.
SUMMARY
Plants interact with other organisms employing volatile organic compounds (VOCs). The largest group of plant‐released VOCs are terpenes, comprised of isoprene, monoterpenes, and ...sesquiterpenes. Mono‐ and sesquiterpenes are well‐known communication compounds in plant–insect interactions, whereas the smallest, most commonly emitted terpene, isoprene, is rather assigned a function in combating abiotic stresses. Recently, it has become evident that different volatile terpenes also act as plant‐to‐plant signaling cues. Upon being perceived, specific volatile terpenes can sensitize distinct signaling pathways in receiver plant cells, which in turn trigger plant innate immune responses. This vastly extends the range of action of volatile terpenes, which not only protect plants from various biotic and abiotic stresses, but also convey information about environmental constraints within and between plants. As a result, plant–insect and plant–pathogen interactions, which are believed to influence each other through phytohormone crosstalk, are likely equally sensitive to reciprocal regulation via volatile terpene cues. Here, we review the current knowledge of terpenes as volatile semiochemicals and discuss why and how volatile terpenes make good signaling cues. We discuss how volatile terpenes may be perceived by plants, what are possible downstream signaling events in receiver plants, and how responses to different terpene cues might interact to orchestrate the net plant response to multiple stresses. Finally, we discuss how the signal can be further transmitted to the community level leading to a mutually beneficial community‐scale response or distinct signaling with near kin.
Significance Statement
Plants release a high diversity of various volatile terpene compounds that can function as intra‐ and interspecific chemical signals. In this review we discuss the current knowledge of different terpenes as plant‐to‐plant signaling cues, how the different cues may be perceived by plants, and how they may sensitize distinct signaling pathways in plant cells leading to improved immunity and fitness of plants and plant communities.
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