Photosynthesis,stomatal conductance and terpene emission response to water availability in dry and mesic Mediterranean forests

Key message

Warmer summer conditions result in increased terpene emissions except under severe drought, in which case they strongly decrease.

Abstract

Water stress results in a reduction of the metabolism of plants and in a reorganization of their use of resources geared to survival. In the Mediterranean region, periods of drought accompanied by high temperatures and high irradiance occur in summer. Plants have developed various mechanisms to survive in these conditions by resisting, tolerating or preventing stress. We used three typical Mediterranean tree species in Israel, Pinus halepensis L., Quercus calliprinos and Quercus ithaburensis Webb, as models for studying some of these adaptive mechanisms. We measured their photosynthetic rates (A), stomatal conductance (g _s), and terpene emission rates during spring and summer in a geophysical gradient from extremely dry to mesic from Yatir (south, arid) to Birya (north, moist) with intermediate conditions in Solelim. A and g _s of P. halepensis were threefold higher in Birya than in Yatir where they remained very low both seasons. Quercus species presented 2–3-fold higher A and g _s but with much more variability between seasons, especially for Q. ithaburensis with A and g _s that decreased 10–30-fold from spring to summer. Terpene emission rates for pine were not different regionally in spring but they were 5–8-fold higher in Birya than in Yatir in summer (P < 0.05). Higher emissions were also observed in Solelim for the drought resistant Q. ithaburensis (P < 0.001) but not for Q. calliprinos. α-Pinene followed by limonene and 3-carene were the dominant terpenes. Warmer summer conditions result in increased Terpene emission rates except under severe drought, in which case they strongly decrease.

     

Plant coexistence alters terpene emission and content of Mediterranean species

There is evidence that secondary metabolism may modulate plant interactions and is modified by different biotic stress agents, such as herbivores or pathogens. However, it is poorly understood whether secondary metabolism is altered during competition among plants. The intraspecific and interspecific coexistence of some Mediterranean potted seedlings, namely Rosmarinus officinalis, Pinus halepensis, Cistus albidus and Quercus coccifera was investigated through their terpene accumulation within leaves (except for Q. coccifera, a non-storing species) and terpene emissions (for all species). Competition had both positive and negative effects for both terpene emissions and content, depending on the species a seedling coexisted with. For R. officinalis, terpene concentrations (1.8-cineole and camphor) and terpene emissions (camphene, camphor and overall monoterpenes) were lower when the neighbour species was P. halepensis. For C. albidus, no changes were observed in its content, while the overall sesquiterpene emissions (70% of total emissions) were reduced in all competition conditions, except in intraspecific competition. In the case of P. halepensis, the highest terpene content occurred when it grew with C. albidus, and in intraspecific competition, while its emissions were reduced under these conditions. Only emissions of Q. coccifera showed no significant changes in the different competition treatments.     

Effects of water and nitrogen interaction on net photosynthesis, stomatal conductance, and water-use efficiency in two hybrid poplar clones

We examined the interactions of water and nitrogen availability by subjecting two Populus clones. Tristis and Eugenei, to five soil moisture and three soil nitrogen levels. Nitrogen application significantly increased net photosynthesis and stomatal conductance of flooded Eugenei and Tristis. The onset of flooding caused partial stomatal closure. Net photosynthesis significantly declined after a longer flooding period. Emergence of adventitious roots on the submerged portions of stems in both clones seemingly helped net photosynthesis fully recover in Eugenei and partially recover in Tristis. Under the progressive drought conditions, stomatal conductance was more sensitive to drought than net photosynthesis in both clones. Addition of nitrogen to progressively drying soil induced more stomatal closure in both clones. The highest water-use efficiency was found on the high-N/severe drought zone for Eugenei, whereas it was found on the high-N/mild to moderate drought zone for Tristis.     

Decoupling between stomatal conductance and photosynthesis occurs under extreme heat in broadleaf tree species regardless of water access

High air temperatures increase atmospheric vapor pressure deficit (VPD) and the severity of drought, threatening forests worldwide. Plants regulate stomata to maximize carbon gain and minimize water loss, resulting in a close coupling between net photosynthesis (A_net) and stomatal conductance (g_s). However, evidence for decoupling of g_s from A_net under extreme heat has been found. Such a response both enhances survival of leaves during heat events but also quickly depletes available water. To understand the prevalence and significance of this decoupling, we measured leaf gas exchange in 26 tree and shrub species growing in the glasshouse or at an urban site in Sydney, Australia on hot days (maximum T_air > 40°C). We hypothesized that on hot days plants with ample water access would exhibit reduced A_net and use transpirational cooling leading to stomatal decoupling, whereas plants with limited water access would rely on other mechanisms to avoid lethal temperatures. Instead, evidence for stomatal decoupling was found regardless of plant water access. Transpiration of well-watered plants was 23% higher than model predictions during heatwaves, which effectively cooled leaves below air temperature. For hotter, droughted plants, the increase in transpiration during heatwaves was even more pronounced—g_s was 77% higher than model predictions. Stomatal decoupling was found for most broadleaf evergreen and broadleaf deciduous species at the urban site, including some wilted trees with limited water access. Decoupling may simply be a passive consequence of the physical effects of high temperature on plant leaves through increased cuticular conductance of water vapor, or stomatal decoupling may be an adaptive response that is actively regulated by stomatal opening under high temperatures. This temperature response is not yet included in any land surface model, suggesting that model predictions of evapotranspiration may be underpredicted at high temperature and high VPD.     

A coupled model of stomatal conductance, photosynthesis and transpiration

A model that couples stomatal conductance, photosynthesis, leaf energy balance and transport of water through the soil–plant–atmosphere continuum is presented. Stomatal conductance in the model depends on light, temperature and intercellular CO₂ concentration via photosynthesis and on leaf water potential, which in turn is a function of soil water potential, the rate of water flow through the soil and plant, and on xylem hydraulic resistance. Water transport from soil to roots is simulated through solution of Richards’ equation. The model captures the observed hysteresis in diurnal variations in stomatal conductance, assimilation rate and transpiration for plant canopies. Hysteresis arises because atmospheric demand for water from the leaves typically peaks in mid‐afternoon and because of uneven distribution of soil matric potentials with distance from the roots. Potentials at the root surfaces are lower than in the bulk soil, and once soil water supply starts to limit transpiration, root potentials are substantially less negative in the morning than in the afternoon. This leads to higher stomatal conductances, CO₂ assimilation and transpiration in the morning compared to later in the day. Stomatal conductance is sensitive to soil and plant hydraulic properties and to root length density only after approximately 10 d of soil drying, when supply of water by the soil to the roots becomes limiting. High atmospheric demand causes transpiration rates, LE, to decline at a slightly higher soil water content, θ_s, than at low atmospheric demand, but all curves of LE versus θ_s fall on the same line when soil water supply limits transpiration. Stomatal conductance cannot be modelled in isolation, but must be fully coupled with models of photosynthesis/respiration and the transport of water from soil, through roots, stems and leaves to the atmosphere.     

Effects of water vapour pressure deficit and stomatal conductance on photosynthesis,internal pressurization and convective flow in three emergent wetland plants

Internal pressurization and convective gas flow in emergent wetland plants is a function of the water vapour pressure deficit (WPD) and stomatal conductance (G _s) separating the external atmosphere from the internal aerenchyma. We have compared the effects of WPD and G _s under a range of light intensities on static pressures and convective flows in Phragmites australis, Typha orientalis and Baumea articulata. The capacity of the three species to generate flows per unit leaf area differed, being greatest in P. australisand lowest in B. articulata. In all three species, decreasing light intensity from full sunlight (2200 mol m^–2 s^–1 photosynthetically active photon flux density (PPFD)) to < 200 and < 10 mol m^–2 s^–1PPFD caused immediate decreases in photosynthetic assimilation, followed by more gradual decreases in transpiration and G _s. However, internal pressures and flows in the two low light intensities remained similar to values recorded in full sunlight. WPD was more significantly related to pressures and flows in P. australis and T. orientalis than G _s. In B. articulata, pressures increased at low G _s values but flow rates were unaffected, as predicted by earlier models describing pore size effects on pressures and flows. The data suggest that emergent macrophytes can maintain significant internal convection even at low light intensities, and this may be beneficial for nocturnal aeration, particularly in arid climates where the atmospheric humidity at night is low.     

Effects of temperature and UV radiation increases on the photosynthetic efficiency in four scleractinian coral species

Experiments were performed on coral species containing clade A (Stylophora pistillata, Montipora aequituberculata) or clade C (Acropora sp., Pavona cactus) zooxanthellae. The photosynthetic efficiency (F(v)/F(m)) of the corals was first assessed during a short-term increase in temperature (from 27 degrees C to 29 degrees C, 32 degrees C, and 34 degrees C) and acute exposure to UV radiation (20.5 W m(-2) UVA and 1.2 W m(-2) UVB) alone or in combination. Increasing temperature to 34 degrees C significantly decreased the F(v)/F(m) in S. pistillata and M. aequituberculata. Increased UV radiation alone significantly decreased the F(v)/F(m) of all coral species, even at 27 degrees C. There was a combined effect of temperature and UV radiation, which reduced F(v)/F(m) in all corals by 25% to 40%. During a long-term exposure to UV radiation (17 days) the F(v)/F(m) was significantly reduced after 3 days' exposure in all species, which did not recover their initial values, even after 17 days. By this time, all corals had synthesized mycosporine-like amino acids (MAAs). The concentration and diversity of MAAs differed among species, being higher for corals containing clade A zooxanthellae. Prolonged exposure to UV radiation at the nonstressful temperature of 27 degrees C conferred protection against independent, thermally induced photoinhibition in all four species.     

Seasonal patterns of terpene content and emission from seven Mediterranean woody species in field conditions

The seasonal pattern of terpene content and emission by seven Mediterranean woody species was studied under field conditions. Emission rates were normalized at 30°C and 1000 μmol·m·s PFD (photosynthetic photon flux density). Bupleurum fruticosum, Pinus halepensis, and Cistus albidus stored large amounts of terpenes (0.01-1.77% [dry matter]) with maximum values in autumn and minimum values in spring. They emitted large amounts of terpenes (2-40 μg·g DM·h), but with no clear seasonal trend except for Cistus albidus, which had maximum values in spring and minimum values in autumn. The nonstoring species Arbutus unedo, Erica arborea, Quercus coccifera and Quercus ilex also emitted large amounts of terpenes (0-40 μg·g DM·h) and also tended to present maximum emission rates in spring, although this trend was significant only for A. unedo. At the seasonal scale, emission rates did not follow changes in photosynthetic rates; instead, they mostly followed changes in temperature. From autumn to spring, the least volatile monoterpenes such as limonene were emitted at highest rates, whereas the most volatile monoterpenes such as α-pinene and β-pinene were the most emitted in summer. The monoterpene emission rates represented a greater percentage of the photosynthetic carbon fixation in summer (from 0.51% in Arbutus unedo to 5.64% in Quercus coccifera) than in the rest of the seasons. All these seasonality trends must be considered when inventorying and modeling annual emission rates in Mediterranean ecosystems.     

Interactive effects of UV radiation and water availability on seedlings of six woody Mediterranean species

To assess the effects of UV radiation and its interaction with water availability on Mediterranean plants, we performed an experiment with seedlings of six Mediterranean species (three mesophytes vs three xerophytes) grown in a glasshouse from May to October under three UV conditions (without UV, with UVA and with UVA+UVB) and two irrigation levels (watered to saturation and low watered). Morphological, physiological and biochemical measures were taken. Exposure to UVA+UVB increased the overall leaf mass per area (LMA) and the leaf carotenoids/chlorophyll a + b ratio of plants in relation to plants grown without UV or with UVA, respectively. In contrast, we did not find a general effect of UV on the leaf content of phenols or UVB‐absorbing compounds of the studied species. Regarding plant growth, UV inhibited the above‐ground biomass production of well‐watered plants of Pistacia lentiscus. Conversely, under low irrigation, UVA tended to abolish the reduction in growth experienced by P. lentiscus plants growing in a UV‐free environment, in accordance with UVA‐enhanced apparent electron transport rate (ETR) values under drought in this species. UVA also induced an overall increase in root biomass when plants of the studied species were grown under a low water supply. In conclusion, while plant exposition to UVA favored root growth under water shortage, UVB addition only gave rise to photoprotective responses, such as the increase in LMA or in the leaf carotenoids/chlorophyll a + b ratio of plants. Species‐specific responses to UV were not related with the xerophytic or mesophytic character of the studied species.     

Leaf photosynthesis and conductance of selected triticum species at different water potentials

Leaf gas exchange characteristics of a desert annual (Triticum kotschyi [Boiss.] Bowden) and the wheat cultivar TAM W-101 (Triticum aestivum L. em Thell) were compared over a range of leaf water potentials from −0.50 to −2.9 megapascals. At an ambient [CO₂] of 330 microliters per liter, T. kotschyi had higher conductance and CO₂ assimilation (A) at a given water potential than T. aestivum. Under well watered conditions, A versus internal CO₂ concentration (C_i) response curves for both species were similar in shape and magnitude, and the higher A of T. kotschyi at an ambient [CO₂] of 330 microliters per liter was mostly related to the higher stomatal conductance of T. kotschyi. The higher conductance of T. kotschyi than T. aestivum under well watered conditions was associated with higher C_i and lower water use efficiency. Under water deficits, however, C_i at 330 microliters per liter ambient [CO₂] did not differ significantly between species. T. kotschyi had higher A under water deficits than T. aestivum primarily because its A versus C_i response curves had higher A at C_i values above about 150 microliters per liter. The results show that conductance played an important role in the high A of T. kotschyi under well watered conditions, but under water deficits the high A of T. kotschyi was related more to the maintenance of a higher capacity for mesophyll photosynthesis.     

Recovery responses of photosynthesis,transpiration, and stomatal conductance in kidney bean following drought stress

Photosynthesis, transpiration, stomatal conductance and chlorophyll fluorescence characteristics were examined in kidney bean plants, with developing gradually water stress for several days after watering and then permitted to recover by re-watering. The photosynthetic rate, transpiration rate, and stomatal conductance decreased rapidly by withholding water for 2 days. The F_v/F_m of chlorophyll fluorescence characteristics slightly decreased when the water was withheld for 7 days. After re-watering the rate of recovery of photosynthesis, transpiration, and stomatal conductance decreased gradually as the days without watering became longer. The differences existed in rates of recovery of photosynthesis, transpiration, and stomatal conductance following drought stress. Among the fractional recoveries the highest was photosynthesis, and the lowest was stomatal conductance. Photosynthesis rate following drought stress was rapidly recovered until 2 days after re-watering, then recovered slowly. The critical time for the recovery of photosynthesis was recognized. The results show clearly a close correlation between the leaf water potential and the recovery level and speed of photosynthesis, transpiration, and stomatal conductance.     

Effect of jasmonic acid on the stomatal and nonstomatal limitation of leaf photosynthesis in barley leaves

The effect of long-term (7 days) and shortterm (up to 2 h) treatment of barley plants with jasmonic acid (JA) on the components contributing to stomatal and nonstomatal limitation of photosynthesis was studied. Net CO₂ assimilation rate (A) responses to intercellular CO₂ concentration (C _i ), i.e., A/C _i curves, were used to assess the photosynthetic ability. Long-term treatment of barley plants with JA led to a noticeable decrease in both the initial slope of the A/C _i curves and the maximum A at saturating C _i . The proportion of stomatal and nonstomatal factors in limitation of photosynthesis depended on the applied JA concentration. Short-term treatment with JA affected neither the stomatal conductivity for CO₂ nor the rate of photosynthetic CO₂ assimilation. We suggest that JA may affect photosynthesis indirectly, either as a stress-modulating substance, or through the alterations in gene expression.     

Effects of flooding and salinity on photosynthesis and water relations of four Southeastern Coastal Plain forest species

The influence of flooding and salinity on photosynthesis and water relations was examined for four common coastal tree species [green ash (Fraxinus pennsylvanica Marshall), water tupelo (Nyssa aquatica L.). Chinese tallow (Sapium sebiferum (L.) Roxb.), and baldcypress (Taxodium distichum (L.) Richard)]. Both chronic (as might be associated with sea level rise) and acute (similar to hurricane storm surges) exposures to these stresses were examined. Chronic freshwater flooding of green ash, water tupelo, and Chinese tallow seedlings reduced photosynthesis (A) relative to that of watered seedlings, while baldcypress was unaffected. Chinese tallow A declined with increasing length of flooding. A salinity increase of the floodwater to 2 ppt decreased A of baldcypress and water tupelo, but not A of green ash and Chinese tallow, which was already severely reduced by freshwater flooding. All seedlings of the four species died within 2 to 6 weeks when flooded with 10 ppt saltwater. Photosynthesis of all four species did not differ between 0 and 2 ppt watering. Watering with 10 ppt salinity initially reduced A of all four species, but the seedlings recovered over time. Photosynthesis was severely decreased for all species when flooded with 21 ppt salinity for 48 hours. Reduced A continued following the treatment. Photosynthesis of only green ash and water tupelo was reduced by watering with 21 ppt salinity for 48 hours. Flooding of low-lying areas with increased salinity would lead to shifts in species composition of coastal forests due to these differential tolerances.     

Differential coordination of stomatal conductance,mesophyll conductance,and leaf hydraulic conductance in response to changing light across species

Stomatal conductance (g_s) and mesophyll conductance (g_m) represent major constraints to photosynthetic rate (A), and these traits are expected to coordinate with leaf hydraulic conductance (K_leaf) across species, under both steady‐state and dynamic conditions. However, empirical information about their coordination is scarce. In this study, K_leaf, gas exchange, stomatal kinetics, and leaf anatomy in 10 species including ferns, gymnosperms, and angiosperms were investigated to elucidate the correlation of H₂O and CO₂ diffusion inside leaves under varying light conditions. Gas exchange, K_leaf, and anatomical traits varied widely across species. Under light‐saturated conditions, the A, g_s, g_m, and K_leaf were strongly correlated across species. However, the response patterns of A, g_s, g_m, and K_leaf to varying light intensities were highly species dependent. Moreover, stomatal opening upon light exposure of dark‐adapted leaves in the studied ferns and gymnosperms was generally faster than in the angiosperms; however, stomatal closing in light‐adapted leaves after darkening was faster in angiosperms. The present results show that there is a large variability in the coordination of leaf hydraulic and gas exchange parameters across terrestrial plant species, as well as in their responses to changing light.     

In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species

Net photosynthetic carbon uptake of Panamanian lowland tropical forest species is typically optimal at 30–32 °C. The processes responsible for the decrease in photosynthesis at higher temperatures are not fully understood for tropical trees. We determined temperature responses of maximum rates of RuBP‐carboxylation (V_CMax) and RuBP‐regeneration (J_Max), stomatal conductance (G_s), and respiration in the light (R_Light) in situ for 4 lowland tropical tree species in Panama. G_s had the lowest temperature optimum (T_Opt), similar to that of net photosynthesis, and photosynthesis became increasingly limited by stomatal conductance as temperature increased. J_Max peaked at 34–37 °C and V_CMax ~2 °C above that, except in the late‐successional species Calophyllum longifolium, in which both peaked at ~33 °C. R_Light significantly increased with increasing temperature, but simulations with a photosynthesis model indicated that this had only a small effect on net photosynthesis. We found no evidence for Rubisco‐activase limitation of photosynthesis. T_Opt of V_CMax and J_Max fell within the observed in situ leaf temperature range, but our study nonetheless suggests that net photosynthesis of tropical trees is more strongly influenced by the indirect effects of high temperature—for example, through elevated vapour pressure deficit and resulting decreases in stomatal conductance—than by direct temperature effects on photosynthetic biochemistry and respiration.     

Effects of drought on photosynthesis in Mediterranean plants grown under enhanced UV-B radiation

The effects of drought on the photosynthetic characteristics of three Mediterranean plants (olive, Olea europea L.; rosemary, Rosmarinus officinalis L.; lavender, Lavandula stoechas L.) exposed to elevated UV-B irradiation in a glasshouse were investigated over a period of weeks. Drought conditions were imposed on 2-year-old plants by withholding water. During the onset of water stress, analyses of the response of net carbon assimilation of leaves to their intercellular CO2 concentration were used to examine the potential limitations imposed by stomata, carboxylation velocity and capacity for regeneration of ribulose 1,5-bisphosphate on photosynthesis. Measurements of chlorophyll fluorescence were used to determine changes in the efficiency of light utilization for electron transport, the occurrence of photoinhibition of photosystem II photochemistry and the possibility of stomatal patchiness across leaves. The first stages of water stress produced decreases in the light-saturated rate of CO2 assimilation which were accompanied by decreases in the maximum carboxylation velocity and the capacity for regeneration of ribulose 1,5-bisphosphate in the absence of any significant photodamage to photosystem II. Leaves of rosemary and lavender were more sensitive than those of olive during the first stages of the drought treatment and also exhibited increases in stomatal limitation. With increasing water stress, significant decreases in the maximum quantum efficiency of photosystem II photochemistry occurred in lavender and rosemary, and stomatal limitation was increased in olive. No indication of any heterogeneity of photosynthesis was found in any leaves. Drought treatment significantly decreased leaf area in all species, an important factor in drought-induced decreases in photosynthetic productivity. Exposure of plants to elevated UV-B radiation (0.47 W m(-2)) prior to and during the drought treatment had no significant effects on the growth or photosynthetic activities of the plants. Consequently, it is predicted that increasing UV-B due to future stratospheric ozone depletion is unlikely to have any significant impact on the photosynthetic productivity of olive, lavender and rosemary in the field.     

Ozone exposure causes a decoupling of conductance and photosynthesis: implications for the Ball-Berry stomatal conductance model

Industrialization has significantly altered atmospheric chemistry by increasing concentrations of chemicals such as nitrogen oxides (NO( x )) and volatile organic carbon, which react in the presence of sunlight to produce tropospheric ozone (O(3)). Ozone is a powerful oxidant that causes both visual and physiological damage to plants, impairing the ability of the plant to control processes like photosynthesis and transpiration. Damage to photosynthesis and stomatal conductance does not always occur at the same rate, which generates a problem when using the Ball-Berry model to predict stomatal conductance because the calculations directly rely on photosynthesis rates. The goals of this work were to develop a modeling framework to modify Ball-Berry stomatal conductance predictions independently of photosynthesis and to test the framework using experimental data. After exposure to elevated O(3) in open-top chambers, photosynthesis and stomatal conductance in tulip poplar changed at different rates through time. We were able to accurately model observed photosynthetic and stomatal conductance responses to chronic O(3) exposure in a Ball-Berry framework by adjusting stomatal conductance in addition to photosynthesis. This led to a significant improvement in the modeled ability to predict both photosynthesis and stomatal conductance responses to O(3).