Lucian Copolovici

Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models

Foliage photosynthetic and structural traits were studied in 15 species with a wide range of foliage anatomies to gain insight into the importance of key anatomical traits in the limitation of diffusion of CO2 from substomatal cavities to chloroplasts. The relative importance of different anatomical traits in constraining CO2 diffusion was evaluated using a quantitative model. Mesophyll conductance (g m) was most strongly correlated with chloroplast exposed surface to leaf area ratio (S c/S) and cell wall thickness (T cw), but, depending on foliage structure, the overall importance of g m in constraining photosynthesis and the importance of different anatomical traits in the restriction of CO2 diffusion varied. In species with mesophytic leaves, membrane permeabilities and cytosol and stromal conductance dominated the variation in g m. However, in species with sclerophytic leaves, g m was mostly limited by T cw. These results demonstrate the major role of anatomy in constraining mesophyll diffusion conductance and, consequently, in determining the variability in photosynthetic capacity among species.

The Capacity for Thermal Protection of Photosynthetic Electron Transport Varies for Different Monoterpenes in Quercus ilex

Heat stress resistance of foliar photosynthetic apparatus was investigated in the Mediterranean monoterpene-emitting evergreen sclerophyll species Quercus ilex. Leaf feeding with fosmidomycin, which is a specific inhibitor of the chloroplastic isoprenoid synthesis pathway, essentially stopped monoterpene emission and resulted in the decrease of the optimum temperature of photosynthetic electron transport from approximately 38°C to approximately 30°C. The heat stress resistance was partly restored by fumigation with 4 to 5 nmol mol−1 air concentrations of monoterpene α-pinene but not with fumigations with monoterpene alcohol α-terpineol. Analyses of monoterpene physicochemical characteristics demonstrated that α-pinene was primarily distributed to leaf gas and lipid phases, while α-terpineol was primarily distributed to leaf aqueous phase. Thus, for a common monoterpene uptake rate, α-terpineol is less efficient in stabilizing membrane liquid-crystalline structure and as an antioxidant in plant membranes. Furthermore, α-terpineol uptake rate (U) strongly decreased with increasing temperature, while the uptake rates of α-pinene increased with increasing temperature, providing a further explanation of the lower efficiency of thermal protection by α-terpineol. The temperature-dependent decrease of α-terpineol uptake was both due to decreases in stomatal conductance, gw, and increased volatility of α-terpineol at higher temperature that decreased the monoterpene diffusion gradient between the ambient air (FA) and leaf (FI; U = gw[FA − FI]). Model analyses suggested that α-pinene reacted within the leaf at higher temperatures, possibly within the lipid phase, thereby avoiding the decrease in diffusion gradient, FA − FI. Thus, these data contribute to the hypothesis of the antioxidative protection of leaf membranes during heat stress by monoterpenes. These data further suggest that fumigation with the relatively low atmospheric concentrations of monoterpenes that are occasionally observed during warm windless days in the Mediterranean canopies may significantly improve the heat tolerance of nonemitting vegetation that grows intermixed with emitting species.

Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage

Plants have to cope with a plethora of biotic stresses such as herbivory and pathogen attacks throughout their life cycle. The biotic stresses typically trigger rapid emissions of volatile products of lipoxygenase (LOX) pathway (LOX products: various C6 aldehydes, alcohols, and derivatives, also called green leaf volatiles) associated with oxidative burst. Further a variety of defense pathways is activated, leading to induction of synthesis and emission of a complex blend of volatiles, often including methyl salicylate, indole, mono-, homo-, and sesquiterpenes. The airborne volatiles are involved in systemic responses leading to elicitation of emissions from non-damaged plant parts. For several abiotic stresses, it has been demonstrated that volatile emissions are quantitatively related to the stress dose. The biotic impacts under natural conditions vary in severity from mild to severe, but it is unclear whether volatile emissions also scale with the severity of biotic stresses in a dose-dependent manner. Furthermore, biotic impacts are typically recurrent, but it is poorly understood how direct stress-triggered and systemic emission responses are silenced during periods intervening sequential stress events. Here we review the information on induced emissions elicited in response to biotic attacks, and argue that biotic stress severity vs. emission rate relationships should follow principally the same dose–response relationships as previously demonstrated for different abiotic stresses. Analysis of several case studies investigating the elicitation of emissions in response to chewing herbivores, aphids, rust fungi, powdery mildew, and Botrytis, suggests that induced emissions do respond to stress severity in dose-dependent manner. Bi-phasic emission kinetics of several induced volatiles have been demonstrated in these experiments, suggesting that next to immediate stress-triggered emissions, biotic stress elicited emissions typically have a secondary induction response, possibly reflecting a systemic response. The dose–response relationships can also vary in dependence on plant genotype, herbivore feeding behavior, and plant pre-stress physiological status. Overall, the evidence suggests that there are quantitative relationships between the biotic stress severity and induced volatile emissions. These relationships constitute an encouraging platform to develop quantitative plant stress response models.

Drought-Tolerance of Wheat Improved by Rhizosphere Bacteria from Harsh Environments: Enhanced Biomass Production and Reduced Emissions of Stress Volatiles

Water is the key resource limiting world agricultural production. Although an impressive number of research reports have been published on plant drought tolerance enhancement via genetic modifications during the last few years, progress has been slower than expected. We suggest a feasible alternative strategy by application of rhizospheric bacteria coevolved with plant roots in harsh environments over millions of years, and harboring adaptive traits improving plant fitness under biotic and abiotic stresses. We show the effect of bacterial priming on wheat drought stress tolerance enhancement, resulting in up to 78% greater plant biomass and five-fold higher survivorship under severe drought. We monitored emissions of seven stress-related volatiles from bacterially-primed drought-stressed wheat seedlings, and demonstrated that three of these volatiles are likely promising candidates for a rapid non-invasive technique to assess crop drought stress and its mitigation in early phases of stress development. We conclude that gauging stress by elicited volatiles provides an effectual platform for rapid screening of potent bacterial strains and that priming with isolates of rhizospheric bacteria from harsh environments is a promising, novel way to improve plant water use efficiency. These new advancements importantly contribute towards solving food security issues in changing climates.

Flooding induced emissions of volatile signalling compounds in three tree species with differing waterlogging tolerance

To gain insight into variations in waterlogging responsiveness, net assimilation rate, stomatal conductance, emissions of isoprene and marker compounds of anoxic metabolism ethanol and acetaldehyde, and stress marker compounds nitric oxide (NO), volatile products of lipoxygenase (LOX) pathway and methanol were studied in seedlings of temperate deciduous tree species Alnus glutinosa, Populus tremula and Quercus rubra (from highest to lowest waterlogging tolerance) throughout sustained root zone waterlogging of up to three weeks. In all species, waterlogging initially resulted in reductions in net assimilation and stomatal conductance and enhanced emissions of ethanol, acetaldehyde, NO, LOX products and methanol, followed by full or partial recovery depending on process and species. Strong negative correlations between g(s) and internal NO concentration and NO flux, valid within and across species, were observed throughout the experiment. Isoprene emission capacity was not related to waterlogging tolerance. Less waterlogging tolerant species had greater reduction and smaller acclimation capacity in foliage physiological potentials, and larger emission bursts of volatile stress marker compounds. These data collectively provide encouraging evidence that emissions of volatile organics and NO can be used as quantitative measures of stress tolerance and acclimation kinetics in temperate trees.

Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments.

Plant-generated volatiles constitute a sensitive signal of stress response, but quantitative relationships between the stress severity and volatile emissions have been demonstrated only for a few stresses. Among important stresses in the field, chilling and frost stress in spring and heat stress mid-season can significantly curb productivity. We studied the effects of cold and heat shock treatments on leaf photosynthesis and the emission of the volatile products of the lipoxygenase pathway (LOX, also called green leaf volatiles) and mono- and sesquiterpene emissions in tomato (Solanum lycopersicum cv. Mato) to gain quantitative insights into temperature stress-elicited volatile emissions. Both cold and heat stress treatments ranged from mild, which only weakly affected foliage photosynthesis, to severe, which almost completely inhibited photosynthesis. Under non-stressed conditions, LOX emissions were close to the detection limit, and terpene emissions were low. Both cold and heat stress led to enhancement of LOX emissions according to a switch-type response with essentially no emissions under mild stress and major emissions under severe stress. The emissions of mono- and sesquiterpenes increased gradually with the severity of stress, but cold stress resulted in higher sesquiterpene emissions at any given monoterpene emission level. We suggest that the quantitative relationships between the stress strength and emissions observed in this study provide an important means to characterize the severity of cold and heat stresses.

Postillumination Isoprene Emission: In Vivo Measurements of Dimethylallyldiphosphate Pool Size and Isoprene Synthase Kinetics in Aspen Leaves

The control of foliar isoprene emission is shared between the activity of isoprene synthase, the terminal enzyme catalyzing isoprene formation from dimethylallyldiphosphate (DMADP), and the pool size of DMADP. Due to limited in vivo information of isoprene synthase kinetic characteristics and DMADP pool sizes, the relative importance of these controls is under debate. In this study, the phenomenon of postillumination isoprene release was employed to develop an in vivo method for estimation of the DMADP pool size and to determine isoprene synthase kinetic characteristics in hybrid aspen (Populus tremula × Populus tremuloides) leaves. The method is based on observations that after switching off the light, isoprene emission continues for 250 to 300 s and that the integral of the postillumination isoprene emission is strongly correlated with the isoprene emission rate before leaf darkening, thus quantitatively estimating the DMADP pool size associated with leaf isoprene emission. In vitro estimates demonstrated that overall leaf DMADP pool was very large, almost an order of magnitude larger than the in vivo pool. Yet, the difference between total DMADP pools in light and in darkness (light-dependent DMADP pool) was tightly correlated with the in vivo estimates of the DMADP pool size that is responsible for isoprene emission. Variation in in vivo DMADP pool size was obtained by varying light intensity and atmospheric CO2 and O2 concentrations. From these experiments, the in vivo kinetic constants of isoprene synthase were determined. In vivo isoprene synthase kinetic characteristics suggested that isoprene synthase mainly operates under substrate limitation and that short-term light, CO2, and O2 dependencies of isoprene emission result from variation in DMADP pool size rather than from modifications in isoprene synthase activity.

Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage

Plant volatile organic compounds (VOCs) elicited in response to herbivory serve as cues for parasitic and predatory insects. Knowledge about quantitative relationships between the extent of herbivore-induced damage and the quantities of VOCs released is scarce. We studied the kinetics of VOC-emissions from foliage of the deciduous tree Alnus glutinosa induced by feeding activity of larvae of the geometrid moth Cabera pusaria. Quantitative relationships between the intensity of stress and strength of plant response were determined. Intensity of biotic stress was characterized by herbivore numbers (0–8 larvae) and by the amount of leaf area eaten. The strength of plant response was characterized by monitoring (i) changes in photosynthesis, (ii) leaf ultrastructure, and (iii) plant volatiles. Net assimilation rate displayed compensatory responses in herbivore-damaged leaves compared with control leaves. This compensatory response was associated with an overall increase in chloroplast size. Feeding-induced emissions of products of the lipoxygenase pathway (LOX products; (E)-2-hexenal, (Z)-3-hexenol, 1-hexanol, and (Z)-3-hexenyl acetate) peaked at day 1 after larval feeding started, followed by an increase of emissions of ubiquitous monoterpenes peaking on days 2 and 3. The emission of the monoterpene (E)-β-ocimene and of the nerolidol-derived homoterpene 4,8-dimethyl-nona-1,3,7-triene (DMNT) peaked on day 3. Furthermore, the emission kinetics of the sesquiterpene (E,E)-α-farnesene tended to be biphasic with peaks on days 2 and 4 after start of larval feeding. Emission rates of the induced LOX products, of (E)-β-ocimene and (E,E)-α-farnesene were positively correlated with the number of larvae feeding. In contrast, the emission of DMNT was independent of the number of feeders. These data show quantitative relationships between the strength of herbivory and the emissions of LOX products and most of the terpenoids elicited in response to feeding. Thus, herbivory-elicited LOX products and terpenoid emissions may convey both quantitative and qualitative signals to antagonists of the herbivores. In contrast, our data suggest that the feeding-induced homoterpene DMNT conveys the information “presence of herbivores” rather than information about the quantities of herbivores to predators and parasitoids.

Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses

Plant volatile organic compounds (VOCs) elicited in response to herbivory can serve as cues for parasitic and predatory insects, but the modification of VOC elicitation responses under interacting abiotic stresses is poorly known. We studied foliage VOC emissions in the deciduous tree Alnus glutinosa induced by feeding by the larvae of green alder sawfly (Monsoma pulveratum) under well-watered and drought-stressed conditions. Drought strongly curbed photosynthesis rate and stomatal conductance, but there were no effects of insect feeding on photosynthetic characteristics. Feeding induced emissions of volatile products of lipoxygenase pathway and monoterpenes, and emissions of stress marker compounds (E)-β-ocimene and homoterpene DMNT. The emissions were more strongly elicited and reached a maximum value earlier in drought-stressed plants. In addition, methyl salicylate emissions were elicited in herbivory-fed drought-stressed plants. Herbivores were more strongly attracted to well-watered plants and consumed more than a four-fold greater fraction of leaf area than they consumed from drought-treated plants. Overall, this study demonstrates an important priming effect of drought, suggesting that plants under combined drought/herbivory stress are more resistant to herbivores.

Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain

Abstract Temperature response of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) catalytic properties directly determines the CO2 assimilation capacity of photosynthetic organisms as well as their survival in environments with different thermal conditions. Despite unquestionable importance of Rubisco, the comprehensive analysis summarizing temperature responses of Rubisco traits across lineages of carbon-fixing organisms is lacking. Here, we present a review of the temperature responses of Rubisco carboxylase specific activity (