Stress Volatile Emissions Research Articles

Limitations of Plant Stress Tolerance upon Heat and CO2 Exposure in Black Poplar: Assessment of Photosynthetic Traits and Stress Volatile Emissions.

Volatile organic compounds (VOCs) emitted by plants may help in understanding the status of a plant's physiology and its coping with mild to severe stress. Future climatic projections reveal that shifts in temperature and CO2 availability will occur, and plants may incur the uncoupling of carbon assimilation and synthesis of key molecules. This study explores the patterns of emissions of key VOCs (isoprene, methanol, acetaldehyde, and acetic acid) emitted by poplar leaves (more than 350) under a combined gradient of temperature (12-42 °C) and air CO2 concentration (400-1500 ppm), along with measurements of photosynthetic rates and stomatal conductance. Isoprene emission exhibited a rise with temperature and CO2 availability, peaking at 39 °C, the temperature at which methanol emission started to peak, illustrating the limit of stress tolerance to severe damage. Isoprene emission was uncoupled from the photosynthesis rate, indicating a shift from the carbon source for isoprene synthesis, while assimilation was decreased. Methanol and acetaldehyde emissions were correlated with stomatal conductance and peaked at 25 °C and 1200 ppm CO2. Acetic acid emissions lacked a clear correlation with stomatal conductance and the emission pattern of its precursor acetaldehyde. This study offers crucial insights into the limitations of photosynthetic carbon and stress tolerance.

The same boat, different storm: stress volatile emissions in response to biotrophic fungal infections in primary and alternate hosts

ABSTRACT Rust infection results in stress volatile emissions, but due to the complexity of host-pathogen interaction and variations in innate defense and capacity to induce defense, biochemical responses can vary among host species. Fungal-dependent modifications in volatile emissions have been well documented in numerous host species, but how emission responses vary among host species is poorly understood. Our recent experiments demonstrated that the obligate biotrophic crown rust fungus (P. coronata) differently activated primary and secondary metabolic pathways in its primary host Avena sativa and alternate host Rhamnus frangula. In A. sativa, emissions of methyl jasmonate, short-chained lipoxygenase products, long-chained saturated fatty acid derivatives, mono- and sesquiterpenes, carotenoid breakdown products, and benzenoids were initially elicited in an infection severity-dependent manner, but the emissions decreased under severe infection and photosynthesis was almost completely inhibited. In R. frangula, infection resulted in low-level induction of stress volatile emissions, but surprisingly, in enhanced constitutive isoprene emissions, and even severely-infected leaves maintained a certain photosynthesis rate. Thus, the same pathogen elicited a much stronger response in the primary than in the alternate host. We argue that future work should focus on resolving mechanisms of different fungal tolerance and resilience among primary and secondary hosts.

Differential impact of crown rust (Puccinia coronata) infection on photosynthesis and volatile emissions in the primary host Avena sativa and the alternate host Rhamnus frangula.

Rust infection results in decreases in photosynthesis and stress volatile emissions, but how these changes vary among host species has not been studied. We demonstrated that the impact of the obligate biotrophic fungus, Puccinia coronata f. sp. avenae, on foliage physiological processes is stronger in the primary host, Avena sativa (cultivated oat), than in the alternate host, Rhamnus frangula (alder buckthorn). Photosynthesis decreased with increasing percentage of damaged leaf area (DA) in both species, but reductions were greater in A. sativa. In A. sativa, photosynthetic reductions resulted from reductions in stomatal conductance and photosynthetic capacity; in R. frangula, reductions were due to reduced capacity. Infection reduced photosynthetic biomass and key nutrients in A. sativa, but not in R. frangula. In A. sativa, stress-elicited emissions (methyl jasmonate, green leaf volatiles, long-chain saturated aldehydes, mono- and sesquiterpenes, benzenoids, and carotenoid breakdown products) increased with increasing DA from 0% to 40%, but decreased with further increases in DA. In R. frangula, volatile emissions were slightly elicited but, surprisingly, constitutive isoprene emissions were enhanced. Different hosts had characteristic volatile fingerprints, indicating differential activation of biochemical pathways. Fungal-elicited reductions in photosynthesis scale uniformly with stress severity. In the sensitive host, biphasic scaling of volatiles indicates that heavy spread of chlorosis/necrosis leads to an overall cessation of physiological functioning.

Role of Stomatal Conductance in Modifying the Dose Response of Stress-Volatile Emissions in Methyl Jasmonate Treated Leaves of Cucumber (Cucumis sativa).

Treatment by volatile plant hormone methyl jasmonate (MeJA) leads to release of methanol and volatiles of lipoxygenase pathway (LOX volatiles) in a dose-dependent manner, but how the dose dependence is affected by stomatal openness is poorly known. We studied the rapid (0–60 min after treatment) response of stomatal conductance (Gs), net assimilation rate (A), and LOX and methanol emissions to varying MeJA concentrations (0.2–50 mM) in cucumber (Cucumis sativus) leaves with partly open stomata and in leaves with reduced Gs due to drought and darkness. Exposure to MeJA led to initial opening of stomata due to an osmotic shock, followed by MeJA concentration-dependent reduction in Gs, whereas A initially decreased, followed by recovery for lower MeJA concentrations and time-dependent decline for higher MeJA concentrations. Methanol and LOX emissions were elicited in a MeJA concentration-dependent manner, whereas the peak methanol emissions (15–20 min after MeJA application) preceded LOX emissions (20–60 min after application). Furthermore, peak methanol emissions occurred earlier in treatments with higher MeJA concentration, while the opposite was observed for LOX emissions. This difference reflected the circumstance where the rise of methanol release partly coincided with MeJA-dependent stomatal opening, while stronger stomatal closure at higher MeJA concentrations progressively delayed peak LOX emissions. We further observed that drought-dependent reduction in Gs ameliorated MeJA effects on foliage physiological characteristics, underscoring that MeJA primarily penetrates through the stomata. However, despite reduced Gs, dark pretreatment amplified stress-volatile release upon MeJA treatment, suggesting that increased leaf oxidative status due to sudden illumination can potentiate the MeJA response. Taken together, these results collectively demonstrate that the MeJA dose response of volatile emission is controlled by stomata that alter MeJA uptake and volatile release kinetics and by leaf oxidative status in a complex manner.

Impact of insect herbivory on plant stress volatile emissions from trees: A synthesis of quantitative measurements and recommendations for future research

Abstract Plants, and particularly trees, are the largest source of atmospheric volatile organic compounds globally. Insect herbivory alters plant volatile emission rates and the types of compounds that are emitted. These stress volatiles are a major contribution to total plant volatile emissions during active herbivore feeding, with important implications for atmospheric chemistry processes. However, emission models do not currently have a quantitative description of plant volatile emission rates during and after insect herbivore feeding. This review provides a brief background on plant volatile organic compounds, the urgency of including biotic stress emissions in models, and a summary of plant volatile emission models and steps they have taken to incorporate stress emissions into their framework. The review ends with a synthesis of volatile emissions from trees during insect herbivory. This synthesis highlights key gaps in studied systems and measurement approaches. We provide a summary of recommendations for future work to address these gaps, improve comparability between studies, and generate the data-sets we need to develop a descriptive model of these plant stress volatile emissions.

Influence of Brevibacterium linens RS16 on foliage photosynthetic and volatile emission characteristics upon heat stress in Eucalyptus grandis

Heat stress induces secondary metabolic changes in plants, channeling photosynthetic carbon and energy, away from primary metabolic processes, including, growth. Use of ACC (1-aminocyclopropane-1-carboxylate) deaminase containing plant growth promoting bacteria (PGPB) in conferring heat resistance in plants and the role of PGPB, in altering net carbon assimilation, constitutive and stress volatile emissions has not been studied yet. We exposed leaves of Eucalyptus grandis inoculated and non-inoculated with PGPB Brevibacterium linens RS16 to two levels of heat stress (37 °C and 41 °C for 5 min) and quantified temporal changes in foliage photosynthetic characteristics and volatile emission rates at 0.5 h, day 1 and day 5 after the stress application. Heat stress resulted in immediate reductions in dark-adapted photosystem II (PSII) quantum yield (Fv/Fm), net assimilation rate (A), stomatal conductance to water vapor (gs), and enhancement of stress volatile emissions, including enhanced emissions of green leaf volatiles (GLV), mono- and sesquiterpenes, light weight oxygenated volatile organic compounds (LOC), geranyl-geranyl diphosphate pathway volatiles (GGDP), saturated aldehydes, and benzenoids, with partial recovery by day 5. Changes in stress-induced volatiles were always less in leaves inoculated with B. linens RS16. However, net assimilation rate was enhanced by bacterial inoculation only in the 37 °C treatment and overall reduction of isoprene emissions was observed in bacterially-treated leaves. Principal component analysis (PCA), correlation analysis and partial least squares discriminant analysis (PLS-DA) indicated that different stress applications influenced specific volatile organic compounds. In addition, changes in the expression analysis of heat shock protein 70 gene (DnaK) gene in B. linens RS16 upon exposure to higher temperatures further indicated that B. linens RS16 has developed its own heat resistance mechanism to survive under higher temperature regimes. Taken together, this study demonstrates that foliar application of ACC deaminase containing PGPB can ameliorate heat stress effects in realistic biological settings.

Foliage inoculation by Burkholderia vietnamiensis CBMB40 antagonizes methyl jasmonate-mediated stress in Eucalyptus grandis

Methyl jasmonate (MeJA) is widely used as a model chemical to study hypersensitive responses to biotic stress impacts in plants. Elevated levels of methyl jasmonate induce jasmonate-dependent defense responses, associated with a decline in primary metabolism and enhancement of secondary metabolism of plants. However, there is no information of how stress resistance of plants, and accordingly the sensitivity to exogenous MeJA can be decreased by endophytic plant growth promoting rhizobacteria (PGPR) harboring ACC (1-aminocyclopropane-1-carboxylate) deaminase. In this study, we estimated stress alleviating potential of endophytic PGPR against MeJA-induced plant perturbations through assessing photosynthetic traits and stress volatile emissions. We used mild (5 mM) to severe (20 mM) MeJA and endophytic plant growth promoting rhizobacteria Burkholderia vietnamiensis CBMB40 and studied how MeJA and B. vietnamiensis treatments influenced temporal changes in photosynthetic characteristics and stress volatile emissions. Separate application of MeJA markedly decreased photosynthetic characteristics and increased lipoxygenase pathway (LOX) volatiles, volatile isoprenoids, saturated aldehydes, lightweight oxygenated compounds (LOC), geranyl-geranyl diphosphate pathway (GGDP) volatiles, and benzenoids. However, MeJA-treated leaves inoculated by endophytic bacteria B. vietnamiensis had substantially increased photosynthetic characteristics and decreased emissions of LOX, volatile isoprenoids and other stress volatiles compared with non-inoculated MeJA treatments, especially at later stages of recovery. In addition, analysis of leaf terpenoid contents demonstrated that several mono- and sesquiterpenes were de novo synthesized upon MeJA and B. vietnamiensis applications. This study demonstrates that foliar application of endophytic bacteria B. vietnamiensis can potentially enhance resistance to biotic stresses and contribute to the maintenance of the integrity of plant metabolic activity.

Methylobacterium oryzae CBMB20 influences photosynthetic traits, volatile emission and ethylene metabolism in Oryza sativa genotypes grown in salt stress conditions.

Inoculation of endophytic Methylobacterium oryzae CBMB20 in salt-stressed rice plants improves photosynthesis and reduces stress volatile emissions due to mellowing of ethylene-dependent responses and activating vacuolar H+-ATPase. The objective of this study was to analyze the impact of ACC (1-aminocyclopropane-1-carboxylate) deaminase-producing Methylobacterium oryzae CBMB20 in acclimation of plant to salt stress by controlling photosynthetic characteristics and volatile emission in salt-sensitive (IR29) and moderately salt-resistant (FL478) rice (Oryza sativa L.) cultivars. Saline levels of 50mM and 100mM NaCl with and without bacteria inoculation were applied, and the temporal changes in stress response and salinity resistance were assessed by monitoring photosynthetic characteristics, ACC accumulation, ACC oxidase activity (ACO), vacuolar H+ ATPase activity, and volatile organic compound (VOC) emissions. Salt stress considerably reduced photosynthetic rate, stomatal conductance, PSII efficiency and vacuolar H+ ATPase activity, but it increased ACC accumulation, ACO activity, green leaf volatiles, mono- and sesquiterpenes, and other stress volatiles. These responses were enhanced with increasing salt stress and time. However, rice cultivars treated with CBMB20 showed improved plant vacuolar H+ ATPase activity, photosynthetic characteristics and decreased ACC accumulation, ACO activity and VOC emission. The bacteria-dependent changes were greater in the IR29 cultivar. These results indicate that decreasing photosynthesis and vacuolar H+ ATPase activity rates and increasing VOC emission rates in response to high-salinity stress were effectively mitigated by M. oryzae CBMB20 inoculation.

Petiole gall aphid (Pemphigus spyrothecae) infestation of Populus × petrovskiana leaves alters foliage photosynthetic characteristics and leads to enhanced emissions of both constitutive and stress-induced volatiles.

Poplar spiral gall aphid (Pemphigus spyrothecae) forms galls on the petiole in poplars (Populus) and mass infestations are frequent in poplar stands, but how these parasite gall infestations can affect the leaf lamina structure, photosynthetic rate and constitutive and stress volatile emissions is unknown. We investigated how the infestation by the petiole gall aphids affects lamina photosynthetic characteristics (net assimilation rate, stomatal conductance), C and N contents, and constitutive isoprene and induced volatile emissions in Populus × petrovskiana. The dry gall mass per leaf dry mass (M g/M l) was used as a quantitative measure of the severity of gall infestation. Very high fraction of leaf biomass was invested in gall formation with M g/M l varying between 0.5-2. Over the whole range of the infestation severities, net assimilation rate per area, leaf dry mass per unit area and N content decreased with increasing the severity of infestation. In contrast, stomatal conductance, leaf dry mass per fresh mass, constitutive isoprene emissions, and induced green leaf volatile (GLV), monoterpene, sesquiterpene and benzenoid emissions increased with increasing the severity of gall infestation. The rates of induced emissions were low and these emissions were associated with methyl jasmonate release from leaf laminas. The data demonstrate that petiole gall infestations lead to major changes in leaf lamina sink-source relationships and leaf water relations, thereby significantly altering lamina photosynthesis. Modifications in stress-induced emissions likely indicated systemic signaling triggered by jasmonate transported from the petiole galls to the lamina where jasmonate elicited a cascade of volatile emission responses. Enhance isoprene emissions and induced volatile emissions can play a major role in indirect defense against other herbivores, securing the food source for the gall aphids. In conclusion, a massive infestation by petiole gall aphids can profoundly modify the foliage photosynthetic performance and volatile emission profiles in poplars.

Inoculation of Brevibacterium linens RS16 in Oryza sativa genotypes enhanced salinity resistance: Impacts on photosynthetic traits and foliar volatile emissions

The emission of volatiles in response to salt stress in rice cultivars has not been studied much to date. Studies addressing the regulation of stress induced volatile emission by halotolerant plant growth promoting bacteria containing ACC (1-aminocyclopropane-1-carboxylate) deaminase are also limited. The objective of the present study was to investigate the salt alleviation potential of bacteria by regulating photosynthetic characteristics and volatile emissions in rice cultivars, and to compare the effects of the bacteria inoculation and salt responses between two rice genotypes. The interactive effects of soil salinity (0, 50, and 100 mM NaCl) and inoculation with Brevibacterium linens RS16 on ACC accumulation, ACC oxidase activity, carbon assimilation and stress volatile emissions after stress application were studied in the moderately salt resistant (FL478) and the salt-sensitive (IR29) rice (Oryza sativa L.) cultivars. It was observed that salt stress reduced foliage photosynthetic rate, but induced foliage ACC accumulation, foliage ACC oxidase activity, and the emissions of all the major classes of volatile organic compounds (VOCs) including the lipoxygenase pathway volatiles, light-weight oxygenated volatiles, long-chained saturated aldehydes, benzenoids, geranylgeranyl diphosphate pathway products, and mono- and sesquiterpenes. All these characteristics scaled up quantitatively with increasing salt stress. The effects of salt stress were more pronounced in the salt-sensitive genotype IR29 compared to the moderately salt resistant FL478 genotype. However, the bacterial inoculation significantly enhanced photosynthesis, and decreased ACC accumulation and the ACC oxidase activity, and VOC emissions both in control and salt-treated plants. Taken together, these results suggested that the ACC deaminase-containing Brevibacterium linens RS16 reduces the temporal regulation of VOC emissions and increases the plant physiological activity by reducing the availability of ethylene precursor ACC and the ACC oxidase activity under salt stress.

Changes in photosynthetic rate and stress volatile emissions through desiccation-rehydration cycles in desiccation-tolerant epiphytic filmy ferns (Hymenophyllaceae).

Exposure to recurrent desiccation cycles carries a risk of accumulation of reactive oxygen species that can impair leaf physiological activity upon rehydration, but changes in filmy fern stress status through desiccation and rewatering cycles have been poorly studied. We studied foliage photosynthetic rate and volatile marker compounds characterizing cell wall modifications (methanol) and stress development (lipoxygenase [LOX] pathway volatiles and methanol) through desiccation-rewatering cycles in lower-canopy species Hymenoglossum cruentum and Hymenophyllum caudiculatum, lower- to upper-canopy species Hymenophyllumplicatum and upper-canopy species Hymenophyllum dentatum sampled from a common environment and hypothesized that lower canopy species respond more strongly to desiccation and rewatering. In all species, rates of photosynthesis and LOX volatile emission decreased with progression of desiccation, but LOX emission decreased with a slower rate than photosynthesis. Rewatering first led to an emission burst of LOX volatiles followed by methanol, indicating that the oxidative burst was elicited in the symplast and further propagated to cell walls. Changes in LOX emissions were more pronounced in the upper-canopy species that had a greater photosynthetic activity and likely a greater rate of production of photooxidants. We conclude that rewatering induces the most severe stress in filmy ferns, especially in the upper canopy species.

Ozone-triggered surface uptake and stress volatile emissions in Nicotiana tabacum 'Wisconsin'.

Ozone is a strong oxidant and a key stress elicitor. The immediate and longer term impacts of ozone are poorly understood in species with emission of both de novo synthesized and stored volatiles, such a tobacco (Nicotiana tabacum), which has terpene-containing glandular trichomes on the leaf surface. In this study, we exposed N. tabacum 'Wisconsin' leaves to acute ozone doses of 0 (control), 400, 600, 800, and 1000 ppb for 30 min and studied the effects of ozone exposure on ozone uptake, gas-exchange characteristics, and emissions of lipoxygenase pathway volatiles, monoterpenes, and sesquiterpenes. Foliage emissions of lipoxygenase pathway volatiles were quantitatively related to the severity of ozone exposure, but the stress dose vs. emission relationship was weaker for terpenoids. Analysis of leaf terpene content and composition indicated that several monoterpenes and sesquiterpenes were not stored in leaves and were synthesized de novo upon ozone exposure. The highest degree of elicitation for each compound was observed immediately after ozone treatment and it declined considerably during recovery. Leaf ozone uptake was dominated by non-stomatal deposition, and the emissions of total lipoxygenase pathway volatiles and mono- and sesquiterpenes were positively correlated with non-stomatal ozone deposition. Overall, this study demonstrates remarkably high ozone resistance of the studied tobacco cultivar and indicates that ozone's effects on volatile emissions primarily reflect modifications in the release of stored volatiles and reaction of ozone with the leaf surface structure.

Differential regulation of volatile emission from Eucalyptus globulus leaves upon single and combined ozone and wounding treatments through recovery and relationships with ozone uptake

Both ozone and wounding constitute two key abiotic stress factors, but their interactive effects on plant constitutive and stress-elicited volatile (VOC) emissions are poorly understood. Furthermore, the information on time-dependent modifications in VOC release during recovery from a combined stress is very limited. We studied the modifications in photosynthetic characteristics and constitutive and stress-induced volatile emissions in response to single and combined applications of acute ozone (4, 5, and 6ppm) and wounding treatments through recovery (0.5–75h) in a constitutive isoprene and mono- and sesquiterpene emitter Eucalyptus globulus. Overall, the photosynthetic characteristics were surprisingly resistant to all ozone and wounding treatments. Constitutive isoprene emissions were strongly upregulated by ozone and combined ozone and wounding treatments and remained high through recovery phase, but wounding applied alone reduced isoprene emission. All stress treatments enhanced emissions of lipoxygenase pathway volatiles (LOX), mono- and sesquiterpenes, saturated aldehydes (C7-C10), benzenoids, and geranylgeranyl diphosphate (GGDP) pathway volatiles. Once elicited, GGDP volatile, saturated aldehyde and benzenoid emissions remained high through the recovery period. In contrast, LOX emissions, and total mono- and sesquiterpene emissions decreased through recovery period. However, secondary rises in total sesquiterpene emissions at 75h and in total monoterpenes at 25–50h were observed. Overall, acute ozone and wounding treatments synergistically altered gas exchange characteristics and stress volatile emissions. Through the treatments and recovery period, stomatal ozone uptake rate and volatile emission rates were poorly correlated, reflecting possible ozone-scavenging effect of volatiles and thus, reduction of effective ozone dose and elicitation of induced defense by the acute ozone concentrations applied. These results underscore the important role of interactive stresses on both constitutive and induced volatile emission responses.

Oak powdery mildew (Erysiphe alphitoides)-induced volatile emissions scale with the degree of infection in Quercus robur.

Oak powdery mildew (Erysiphe alphitoides) is a major foliar pathogen of Quercus robur often infecting entire tree stands. In this study, foliage photosynthetic characteristics and constitutive and induced volatile emissions were studied in Q. robur leaves, in order to determine whether the changes in foliage physiological traits are quantitatively associated with the degree of leaf infection, and whether infection changes the light responses of physiological traits. Infection by E. alphitoides reduced net assimilation rate by 3.5-fold and isoprene emission rate by 2.4-fold, and increased stomatal conductance by 1.6-fold in leaves with the largest degree of infection of ∼60%. These alterations in physiological activity were quantitatively associated with the fraction of leaf area infected. In addition, light saturation of net assimilation and isoprene emission was reached at lower light intensity in infected leaves, and infection also reduced the initial quantum yield of isoprene emission. Infection-induced emissions of lipoxygenase pathway volatiles and monoterpenes were light-dependent and scaled positively with the degree of infection. Overall, this study indicates that the reduction of foliage photosynthetic activity and constitutive emissions and the onset of stress volatile emissions scale with the degree of infection, but also that the infection modifies the light responses of foliage physiological activities.