TY - JOUR
AU1 - Maseyk,, Kadmiel
AU2 - Lin,, Tongbao
AU3 - Cochavi,, Amnon
AU4 - Schwartz,, Amnon
AU5 - Yakir,, Dan
AB - Abstract Photoprotection strategies in a Pinus halepensis Mill. forest at the dry timberline that shows sustained photosynthetic activity during 6–7 month summer drought were characterized and quantified under field conditions. Measurements of chlorophyll fluorescence, leaf-level gas exchange and pigment concentrations were made in both control and summer-irrigated plots, providing the opportunity to separate the effects of atmospheric from soil water stress on the photoprotection responses. The proportion of light energy incident on the leaf surface ultimately being used for carbon assimilation was 18% under stress-free conditions (irrigated, winter), declining to 4% under maximal stress (control, summer). Allocation of absorbed light energy to photochemistry decreased from 25 to 15% (control) and from 50% to 30% (irrigated) between winter and summer, highlighting the important role of pigment-mediated energy dissipation processes. Photorespiration or other non-assimilatory electron flow accounted for 15–20% and ~10% of incident light energy during periods of high and low carbon fixation, respectively, representing a proportional increase in photochemical energy going to photorespiration in summer but a decrease in the absolute amount of photorespiratory CO2 loss. Resilience of the leaf photochemical apparatus was expressed in the complete recovery of photosystem II (PSII) efficiency (ΦPSII) and relaxation of the xanthophyll de-epoxidation state on the diurnal cycle throughout the year, and no seasonal decrease in pre-dawn maximal PSII efficiency (Fv/Fm). The response of CO2 assimilation and photoprotection strategies to stomatal conductance and leaf water potential appeared independent of whether stress was due to atmospheric or soil water deficits across seasons and treatments. The range of protection characteristics identified provides insights into the relatively high carbon economy under these dry conditions, conditions that are predicted for extended areas in the Mediterranean and other regions due to global climate change. Introduction Water stress, in terms of both soil water availability and atmospheric vapor pressure deficits (D), is a key limitation to plant productivity (Boyer 1982, Novick et al. 2016). Consistent features of climate change predictions are a decrease in summer rainfall and an increase in evaporative demand, increasing the drought risk and drought frequency across many areas globally, including the Mediterranean Basin (Naumann et al. 2018). The response of plants adapted to warm and dry conditions can provide valuable insights into growth under drought conditions (Peñuelas et al. 2001, Flexas and Medrano 2002, Grünzweig et al. 2003, Garcia-Plazaola et al. 2008, Maseyk et al. 2008a, 2008b, Grossiord et al. 2017, Raz-Yaseef et al. 2010), and are essential for reliable assessments of vegetation dynamics under future climate scenarios (Breshears et al. 2005, Combourieu-Nebout et al. 2015, Adams et al. 2017). The combination of high irradiance and stomatal closure during drought brings the risk of damage to the photosynthetic apparatus due to the over-reduction of the photosynthetic apparatus. The excess of electrons forms reactive oxygen species that can cause protein damage and membrane peroxidation (Smirnoff 1993, Long et al. 1994). Protection strategies against oxidative damage include mechanisms that reduce energy transfer to the photosystems and provide alternative sinks for photochemical energy to CO2 fixation, and systems for scavenging active oxygen species. Pigment-mediated processes include a reduction in chlorophyll to reduce the initial solar energy absorption (Kyparissis et al. 1995, Elvira et al. 1998) and the synthesis of carotenoid pigments, including carotenes and xanthophylls (Demmig-Adams 1990, Tracewell et al. 2001). An important energy dissipation process involves the de-epoxidation of violaxanthin (V) via antherxanthin (A) to zeaxanthin (Z) in the highly dynamic xanthophyll cycle, and non-radiative (thermal) dissipation of energy (Demmig et al. 1987, Demmig-Adams and Adams 2006). The process of photorespiration, or other non-assimilatory electron flow such as the Mehler-peroxidase pathway, while typically considered a cost to plant carbon balance, provides an additional sink for photochemical energy, facilitating continual electron flow through the electron transport system and serving to maintain photosystem functionality under drought and other stressful conditions (Kozaki and Takeba 1996, Wingler et al. 2000, Eisenhut et al. 2017). While these various photoprotection responses during drought have been well documented in controlled and, to a lesser extent, field studies, systematic analysis and quantification of the relative contribution of the various pathways under natural conditions remain rare (Valentini et al. 1995, Flexas and Medrano 2002, Beis and Patakas 2012). Furthermore, the relative importance of the different processes may depend on the functional plant type and the nature of the stress (Demmig-Adams and Adams 2006), with a shift from more flexible and reversible xanthophyll cycle processes to more sustained dissipation under prolonged stress. In this context, the effects of high vapor pressure deficits and low soil water contents may induce different responses, and recent studies have demonstrated the importance of high D VPD even without low soil moisture content on tree physiology (Novick et al. 2016, Grossiord et al. 2017). Atmospheric vapor pressure deficits, while showing an average increase through summer, can have high daily and synoptic scale variations that result in more transient and short-term effects on photosynthetic capacity. Increasing soil water deficits, on the other hand, reduce stomatal conductance (gs) and photosynthetic rate (A) in a progressive manner resulting in lowered photosynthetic capacity over a prolonged period of time. In this study, we present results of a field study that quantified the role of primary photochemical protection strategies in mature Pinus halepensis Mill. (Allepo pine) at the arid limit of the Mediterranean climate region (Grünzweig et al. 2003). Pinus halepensis is a highly drought-tolerant species (Schiller 2000) that is a key species of the Mediterranean region, with an extensive natural distribution (Quézel 2000) and widespread use in reforestation and land reclamation efforts (Pausas et al. 2004). Even at the arid limit of distribution, it has been shown that ongoing photosynthetic activity during extensive summer drought contributes to both new needle growth (Klein et al. 2005, Maseyk et al. 2008b) and the relatively high productivity observed in this forest (Grünzweig et al. 2003, Maseyk et al. 2008a, Rotenberg and Yakir 2010). Therefore, understanding the role of the various photoprotection mechanisms in this system can provide valuable insight into the successful adaptation of evergreen species to warm and dry conditions. Measurements were made on both summer-irrigated (alleviating dry-season soil moisture deficit but maintaining high D VPD) and non-irrigated trees (high soil moisture deficit combined with high D VPD during the dry season) through wet and dry seasons, providing an opportunity to better identify the interactions of high irradiance and temperature with moisture stress in the soil or in the atmosphere. Materials and methods Site description and meteorological measurements The study was conducted in a 2800 ha mature (35–40 years old) P. halepensis forest in southern Israel (31°21′ N, 35° 03′ E, 650 m above sea level) and spanned two dry and one wet season (from June 2001 to October 2002). The forest is located in a transitional climate zone between the Mediterranean and semi-arid climates and experiences long hot rain free periods of up to ~8 months over summer and an average annual rainfall of ~280 mm in a wet season generally between November and March. Tree density was 300–350 trees ha−1, mean tree height 10 m and leaf area index 1.5, on a shallow soil (0.2–1 m deep Rendzina above chalk and limestone) with a deep (~300 m) ground water table (Grünzweig et al. 2007). Measurements of meteorological parameters and carbon and water fluxes have been made at the forest since 2001 (Grünzweig et al. 2003), and show that annual evapotranspiration closely balances precipitation and the aridity index (ratio of precipitation to potential evapotranspiration) is ~0.18, typical of arid regions (Raz-Yaseef et al. 2010). Monthly mean daytime air temperatures range between 11.2 ± 2.0 °C (January) and 28.3 ± 0.9 °C (August). Soil water content reaches field capacity during the wet season and declines to below 10% (volumetric) during the rain-free period. Measurements of photosynthetically active radiation (PAR), air temperature, vapor pressure deficit and precipitation monitored continuously 5 m above the canopy at the flux site (within 1 km from the study site) for the study period are shown in Figure 1. Figure 1. Open in new tabDownload slide Environmental conditions and plant water status at the study site. (A) Daytime average (black line) and maximum (gray line) air temperature; (B) daily average (black line) and daily total (gray line) PAR; (C) daytime average (black line) and maximum (gray line) atmospheric vapor pressure deficit (D) and leaf D on measurement days (circles); (D) rainfall and (E) branch water potential measured predawn (PD, circles) and at midday (MD, squares) in the control (solid symbols) and irrigated (open symbols) trees. Water potential values are the mean of three samples, error bars are the standard error. Figure 1. Open in new tabDownload slide Environmental conditions and plant water status at the study site. (A) Daytime average (black line) and maximum (gray line) air temperature; (B) daily average (black line) and daily total (gray line) PAR; (C) daytime average (black line) and maximum (gray line) atmospheric vapor pressure deficit (D) and leaf D on measurement days (circles); (D) rainfall and (E) branch water potential measured predawn (PD, circles) and at midday (MD, squares) in the control (solid symbols) and irrigated (open symbols) trees. Water potential values are the mean of three samples, error bars are the standard error. Irrigation treatment Starting in May 2001, supplementary summertime irrigation was provided to a plot of 15 trees in order to maintain soil water at close to field capacity throughout the year (Klein et al. 2005). Drip irrigation was provided around the base of the trees at a rate of 3.4–4.0 mm day−1 for the two dry seasons, but was reduced once natural precipitation resumed in the intervening autumn, was suspended over winter once the non-irrigated soil had reached field capacity and resumed according to rainfall intensity in spring. Trees adjacent to the irrigated plot, but receiving no influence of the irrigation, were used as control non-irrigated trees. Needle gas exchange Measurements of projected area-based (from measured needle widths) needle net photosynthetic rates (A), leaf transpiration (E) and stomatal conductance to water vapor (gs) were measured in situ with an LI-6400 photosynthesis system (LI-COR, Inc., Lincoln, Nebraska USA) as described in Maseyk et al. (2008b). Diurnal patterns of needle gas exchange were made on relatively cloud-free days on 10 occasions over the course of the study period. Needle growth occurs during April–October, and the first measurements on the current year needles were made in late May or June, when needles were ~50% of their final length. Needles of this age class were designated y0 needles, and the older age class (previous year needles) were designated y1 needles (P. halepensis generally retains 2–4 age cohorts of needles on the tree). Needles remained in their age class until the first measurements on the new needles the following year. Measurements were made on the two youngest (y0 and y1) age classes of needles on four to six trees from both the irrigated and control group five to six times over the course of the photoperiod, maintaining ambient conditions of temperature, relative humidity, PAR and CO2 concentration in the leaf cuvette. Chlorophyll fluorescence and energy partitioning Chlorophyll a fluorescence measurements were made in parallel to the gas exchange measurements on the same needle cohort, using a pulse-modulated excitation and detection fluorometer (PAM-2000 Portable Fluorometer, Heinz Walz GmbH, Effeltrich Germany). Measurements were made on a group of attached needles, aligned parallel to each other in the probe clip, using the saturation pulse technique. Needles were maintained in their aligned arrangement during the day by lightly clamping them with toothpicks, and the fluorescence probe clip was centered on the aligned needles to ensure that repeat measurements were made on the same needle area and at the same distance from the needles. Fluorescence yields that were monitored included the minimum and maximum yield with full closure of photosystem II (PSII) reaction centers (following application of the saturation pulse) in the dark-adapted state (Fo and Fm, respectively, measured predawn) and steady-state, minimum and maximum yields the light adapted state (F′, Fo′ and Fm′, respectively). To determine the minimal fluorescence yield of a pre-illuminated sample (Fo′), the sample was briefly shaded with a black cloth following the saturation pulse and Fm′ determination to exclude ambient light, followed by a brief application of far-red light (peak of about 735 nm) to excite photosystem I only and re-oxidize PSII quinine acceptors (QA). The steady state Fo′ was then recorded while the far-red light was on. The fluorescence signals were monitored graphically in real-time to ensure steady-state levels of Fo, F and Fo′. When Fm′ was reduced to low levels that made it difficult to separate from the signal noise of F (e.g., at midday (MD) under high light), the measuring beam frequency was increased from the standard setting of 600 kHz to 20 kHz just prior to applying the saturation pulse. The maximum quantum efficiency of electron transport through PSII to QA was determined from the predawn measurements as Fv/Fm, where Fv = Fm − Fo. In the light acclimated state, light energy absorbed by the photosystem antenna was partitioned between photochemistry and non-photochemical quenching processes. The effective quantum efficiency of PSII in the light-acclimated state (ΦPSII) was determined as (Genty et al. 1989): $$\begin{equation} {\varPhi}_{PSII}=\frac{{F_\textrm{m}}^{\prime}-F^{\prime}}{{F_\textrm{m}}^{\prime}}. \end{equation}$$ (1) Based on a ‘lake model’ of interconnected reaction centers and antenna matrix, the quantum efficiencies of non-photochemical processes can be partitioned into those associated with constitutive non-light induced thermal dissipation (ΦNO) and the regulated thermal non-photochemical dissipation (ΦNPQ) as (Kramer et al. 2004): $$\begin{equation} {\varPhi}_{NO}=\frac{1}{\textrm{NPQ}+1+{q}_\textrm{L}\left({F}_m/{F}_o-1\right)}, \end{equation}$$ (2) and, because the sum of ΦPSII, ΦNO and ΦNPQ is unity: $$\begin{equation} {\varPhi}_{NPQ}=1-{\varPhi}_{PSII}-{\varPhi}_{NO}, \end{equation}$$ (3) where NPQ = (Fm - Fm′)/Fm′ describes the reduction, or quenching, of maximal fluorescence between the dark and light states due to non-photochemical processes, and qL = (Fm′ – F′)/(Fm′ – Fo’)·(Fo’/F′) is the fraction of QA in the oxidized state (open reaction centers). The fractional allocation of absorbed light energy between ΦPSII, ΦNPQ and ΦNO was estimated at MD on a number of days through the study period, and for the entire diurnal cycle on days with sufficient data. From the values of ΦPSII, estimates of the non-cyclic electron transport rate (ETR; in μmol e− m−2 s−1) through PSII can be made according to $$\begin{equation} \textrm{ETR}={\varPhi}_{PSII}\times I\times 0.5\times \alpha, \end{equation}$$ (4) where I is the level of PAR incident on the leaf, α is leaf absorbance and 0.5 is the estimate of the fraction of absorbed light received by PSII (i.e., assuming an equal distribution between PSI and PSII). Estimates of leaf absorbance were made from measurements of chlorophyll content (see below), following Evans and Poorter (2001): $$\begin{equation} \alpha =\chi /\left(\chi +76\right)\!, \end{equation}$$ (5) where χ is the chlorophyll content per unit leaf area (μmol m−2). Similarly, the rate of energy dissipation via regulatory thermal processes (TDR) is $$\begin{equation} \textrm{TDR}={\varPhi}_{NPQ}\times I\times \alpha. \end{equation}$$ (6) Photorespiration rates From the relationship between PSII ETRs and CO2 assimilation (A), rates of photorespiratory CO2 release (Rl) can be calculated according to Valentini et al. (1995): $$\begin{equation} {R}_\textrm{l}={J}_\textrm{o}/8, \end{equation}$$ (7) where Jo is the rate of electron flow to photorespiration, and is calculated as $$\begin{equation} {J}_\textrm{o}=2/3\left( \textrm{ETR}-4\left(A+{R}_\textrm{d}\right)\right)\!, \end{equation}$$ (8) where Rd is the rate of needle dark respiration, measured at the end of the day after sunset. Estimates of the allocation of photochemical energy to photorespiration were made from measurements of gas exchange and chlorophyll fluorescence around MD when PAR > 1000 μmol m−2 s−1. Chlorophyll and carotenoid content On select days in 2002, mature needle samples were collected for chlorophyll and carotenoid content determination from three trees of each treatment at six points in the photoperiod. The samples were immediately frozen in liquid nitrogen and kept at −70 °C until the analysis. The samples were homogenized with a pestle and mortar and the pigments were extracted from the homogenate in a cold room and under dim light. The extracts were centrifuged at 4000g to remove cell debris and the supernatant was filtered through a 0.45-μm mesh filter. Chlorophyll was extracted in 80% acetone (v/v) and chlorophyll concentration was determined spectrophotometrically. The carotenoid pigments (xanthophylls V, A, Z, lutein (L) and neoxanthin (N) and α- and β-carotene) were extracted twice with 90% acetone and analyzed by high-performance liquid chromatography (HPLC) (Merck Hitachi 6200) equipped with a diode array detector. The compounds were separated on a LiChrospher 100 RP-18 (4 × 250 mm, 5 μm) HPLC column using the following acetone/water (a/w) gradient: from 0 to 3 min a/w was isocratically maintained at 40/60, then the percent of acetone was linearly increased from 40% to 95% over 20 min, and finally the column was washed with a/w 95/5 for 10 min. The flow rate was 1 ml min-1 and the volume of injection was 20 μl. The pigments were identified by co-chromatography with standards obtained from DHI Water and Environment (Horsholm, Denmark). Branch water potential Plant water status was monitored by measuring the predawn (ΨPD) and MD (ΨMD) water potential on apical twigs containing the y0 and y1 needle cohorts from the same trees as the gas exchange and florescence measurements. The measurements were made using a Scholander-type pressure chamber (Arimad 2, A.I.R., Kfar-Charuv, Israel) with moist paper inside to avoid humidity changes during measurement. System-level incident PAR energy allocation To provide an integrated leaf-level view of the PAR energy allocation strategies across the various pathways and sinks detailed above, we provide a system summary that compares allocation under low stress and maximal CO2 assimilation rates (irrigated trees in spring and winter) with allocation under maximal stress and minimal CO2 assimilation rates (summer in the control trees). The proportion of incident PAR absorbed by the leaf was calculated from chlorophyll content (Eq. 5), with the balance being either transmitted or reflected. The distribution of this absorbed PAR between photochemistry, constitutive and regulated thermal dissipation was calculated from Eqs 1–3, and the distribution of photochemical energy between CO2 assimilation and photorespiration was determined from the measurements of A and calculations of Rl (Eq. 7 and 8). Statistical analyses Statistical differences in pre-dawn Fv/Fm values and the daily energy allocation between control and irrigated trees was tested for using unpaired non-directional t-tests of the daily mean values on the day of measurement. The tests were only conducted between control and irrigated trees for the measurement day, under the null hypothesis assumption of a difference in means of 0, and not between different days within the season (either within or between treatments). Statistical analyses were performed using R version 3.5.3 ‘Great Truth’ (The R Foundation for Statistical Computing, 2016). Linear regression and curve fitting analysis was performed using Origin data analysis and graphing software (OriginLab Corporation, Northampton, MA, USA). Results Meteorological conditions and plant water status The environmental conditions over the study period were typical for this site (Figure 1). Mean daytime air temperature was about 28 °C in July and August and dropped to 5–10 °C in January, with maximum daytime temperatures reaching 35–40 °C in summer. Mean daytime D often reached values of 4000 Pa or more over summer. Rainfall for the 2001–02 wet season was ~10% above average at 313 mm but was within one standard deviation (88 mm) of the long-term mean. The irrigation treatment was effective at relieving soil water stress, as ΨPD values in the irrigated trees were stable over the study period and similar to those in the control trees in the wet months (−0.8 to −1.2 MPa in December–March, Figure 1E). During the summer drought period ΨPD values in the non-irrigated trees declined to values of −2.3 MPa, when summertime volumetric soil water contents in the forest reach ~8%. The lowest (summer time) ΨMD values were −2.7 MPa and −2.4 MPa in the control and irrigated trees, respectively, while ΨMD was highest and similar between treatments at about −2.3 MPa in March. Net CO2 assimilation patterns Diurnal and seasonal patterns of net CO2 assimilation in the control trees (Figure 2A and B) were consistent with those described for this forest site (Maseyk et al. 2008b). There was persistence of photosynthetic activity throughout the year, but rates were greatly reduced in the non-irrigated trees in summer and autumn, with MD depressions confining net leaf-level carbon gain to the early morning and late afternoon (e.g., Aug ’02 in Figure 2A). Assimilation rates in the irrigated trees exceeded those in the control trees for much of the year but rates were still lower in summer relative to winter despite the high soil water availability. Results from biweekly measurements of gas exchange throughout the season made during the hours of peak activity showed that the control and irrigated trees had similar photosynthetic rates for the period between January to April, when annual photosynthesis was maximal (rates of ~18 μmol m−2 s−1, results not shown, but see March 2002 in Table 1). Daily maximal photosynthetic rates and total leaf-level CO2 assimilation during the photoperiod (from integration of the diurnal assimilation data) were reduced by up to 95% in summer in the control trees relative to the winter–spring maximum, while in the irrigated trees the summer rates were reduced by up to 50% (Table 1). Assimilation rates in both control and irrigated trees were closely coupled with stomatal conductance (Figure 3) and a robust relationship between A and gs (A = −0.634 + 18.14(1 — e−8.0*gs), r2 = 0.94) was evident across the data of both treatments over the range of temporal scales (diurnal and seasonal), climatic parameters (e.g. D, temperature and PAR; Figure 1) and needle age classes. Figure 2. Open in new tabDownload slide Representative diurnal patterns of CO2 assimilation (A, B) and photochemical efficiency of PSII (ΦPSII) (C, D) from different dates in the control and irrigated trees. The symbols are the same for each panel as shown in the legend in panel (A). Figure 2. Open in new tabDownload slide Representative diurnal patterns of CO2 assimilation (A, B) and photochemical efficiency of PSII (ΦPSII) (C, D) from different dates in the control and irrigated trees. The symbols are the same for each panel as shown in the legend in panel (A). Table 1 Seasonal values of quantum efficiencies daily carbon gain in control and irrigated P. halepensis trees. Values are mean (SD) of y0 and y1 age classes combined. The Fv/Fm values are pre-dawn maximum PSII efficiency. Whole-day PAR-weighted quantum efficiencies are the diurnal integrations of energy allocation to the various dissipation pathways from five to six measurements through the photoperiod, weighted by PAR at each time step. Significance difference in mean values (t-test) between control and irrigation trees on the same date are indicated where P < 0.05 (*), P < 0.01 (**) and P < 0.001 (***) Whole-day PAR-weighted quantum efficiency Daily C gain (mgC m−2 day−1) Date Fv/Fm |$\Phi$|PSII |$\Phi$|NPQ |$\Phi$|NO Control trees 12-Jun-01 0.804 (0.011) 185 23-Jul-01 0.803 (0.012) 102 22-Aug-01 0.825 (0.008) 0.233 (0.097) *** 0.600 (0.094) *** 0.167 (0.002) 143 14-Nov-01 0.837 (0.007) 0.249 (0.018) *** 0.611 (0.024) *** 0.140 (0.020) 108 18-Dec-01 0.802 (0.006) 0.262 (0.003) ** 0.562 (0.001) ** 0.176 (0.003) *** 466 14-Mar-02 0.821 (0.007) 867 28-May-02 0.823 (0.011) 0.262 (0.017) *** 0.642 (0.020) *** 0.097 (0.003) *** 265 14-Jul-02 0.818 (0.014) 0.182 (0.062) *** 0.645 (0.036) *** 0.173 (0.026) 84 30-Aug-02 0.810 (0.013) 0.121 (0.023) *** 0.773 (0.039) *** 0.105 (0.016) *** 33 23-Oct-02 0.796 (0.030) 0.149 (0.035) *** 0.671 (0.019) *** 0.181 (0.017) 97 Irrigated trees 12-Jun-01 0.814 (0.016) 669 23-Jul-01 0.833 (0.016) 562 22-Aug-01 0.850 (0.005) 0.478 (0.059) 0.358 (0.070) 0.164 (0.011) 844 14-Nov-01 0.845 (0.011) 0.573 (0.024) 0.295 (0.026) 0.133 (0.002) 655 18-Dec-01 0.823 (0.008) 0.422 (0.089) 0.417 (0.085) 0.161 (0.004) 823 14-Mar-02 0.810 (0.005) 991 28-May-02 0.813 (0.039) 0.369 (0.035) 0.487 (0.041) 0.144 (0.006) 892 14-Jul-02 0.832 (0.010) 0.336 (0.000) 0.501 (0.018) 0.163 (0.018) 505 30-Aug-02 0.831 (0.033) 0.298 (0.018) 0.550 (0.018) 0.152 (0.001) 426 23-Oct-02 0.820 (0.019) 0.293 (0.067) 0.515 (0.059) 0.192 (0.008) 632 Whole-day PAR-weighted quantum efficiency Daily C gain (mgC m−2 day−1) Date Fv/Fm |$\Phi$|PSII |$\Phi$|NPQ |$\Phi$|NO Control trees 12-Jun-01 0.804 (0.011) 185 23-Jul-01 0.803 (0.012) 102 22-Aug-01 0.825 (0.008) 0.233 (0.097) *** 0.600 (0.094) *** 0.167 (0.002) 143 14-Nov-01 0.837 (0.007) 0.249 (0.018) *** 0.611 (0.024) *** 0.140 (0.020) 108 18-Dec-01 0.802 (0.006) 0.262 (0.003) ** 0.562 (0.001) ** 0.176 (0.003) *** 466 14-Mar-02 0.821 (0.007) 867 28-May-02 0.823 (0.011) 0.262 (0.017) *** 0.642 (0.020) *** 0.097 (0.003) *** 265 14-Jul-02 0.818 (0.014) 0.182 (0.062) *** 0.645 (0.036) *** 0.173 (0.026) 84 30-Aug-02 0.810 (0.013) 0.121 (0.023) *** 0.773 (0.039) *** 0.105 (0.016) *** 33 23-Oct-02 0.796 (0.030) 0.149 (0.035) *** 0.671 (0.019) *** 0.181 (0.017) 97 Irrigated trees 12-Jun-01 0.814 (0.016) 669 23-Jul-01 0.833 (0.016) 562 22-Aug-01 0.850 (0.005) 0.478 (0.059) 0.358 (0.070) 0.164 (0.011) 844 14-Nov-01 0.845 (0.011) 0.573 (0.024) 0.295 (0.026) 0.133 (0.002) 655 18-Dec-01 0.823 (0.008) 0.422 (0.089) 0.417 (0.085) 0.161 (0.004) 823 14-Mar-02 0.810 (0.005) 991 28-May-02 0.813 (0.039) 0.369 (0.035) 0.487 (0.041) 0.144 (0.006) 892 14-Jul-02 0.832 (0.010) 0.336 (0.000) 0.501 (0.018) 0.163 (0.018) 505 30-Aug-02 0.831 (0.033) 0.298 (0.018) 0.550 (0.018) 0.152 (0.001) 426 23-Oct-02 0.820 (0.019) 0.293 (0.067) 0.515 (0.059) 0.192 (0.008) 632 Open in new tab Table 1 Seasonal values of quantum efficiencies daily carbon gain in control and irrigated P. halepensis trees. Values are mean (SD) of y0 and y1 age classes combined. The Fv/Fm values are pre-dawn maximum PSII efficiency. Whole-day PAR-weighted quantum efficiencies are the diurnal integrations of energy allocation to the various dissipation pathways from five to six measurements through the photoperiod, weighted by PAR at each time step. Significance difference in mean values (t-test) between control and irrigation trees on the same date are indicated where P < 0.05 (*), P < 0.01 (**) and P < 0.001 (***) Whole-day PAR-weighted quantum efficiency Daily C gain (mgC m−2 day−1) Date Fv/Fm |$\Phi$|PSII |$\Phi$|NPQ |$\Phi$|NO Control trees 12-Jun-01 0.804 (0.011) 185 23-Jul-01 0.803 (0.012) 102 22-Aug-01 0.825 (0.008) 0.233 (0.097) *** 0.600 (0.094) *** 0.167 (0.002) 143 14-Nov-01 0.837 (0.007) 0.249 (0.018) *** 0.611 (0.024) *** 0.140 (0.020) 108 18-Dec-01 0.802 (0.006) 0.262 (0.003) ** 0.562 (0.001) ** 0.176 (0.003) *** 466 14-Mar-02 0.821 (0.007) 867 28-May-02 0.823 (0.011) 0.262 (0.017) *** 0.642 (0.020) *** 0.097 (0.003) *** 265 14-Jul-02 0.818 (0.014) 0.182 (0.062) *** 0.645 (0.036) *** 0.173 (0.026) 84 30-Aug-02 0.810 (0.013) 0.121 (0.023) *** 0.773 (0.039) *** 0.105 (0.016) *** 33 23-Oct-02 0.796 (0.030) 0.149 (0.035) *** 0.671 (0.019) *** 0.181 (0.017) 97 Irrigated trees 12-Jun-01 0.814 (0.016) 669 23-Jul-01 0.833 (0.016) 562 22-Aug-01 0.850 (0.005) 0.478 (0.059) 0.358 (0.070) 0.164 (0.011) 844 14-Nov-01 0.845 (0.011) 0.573 (0.024) 0.295 (0.026) 0.133 (0.002) 655 18-Dec-01 0.823 (0.008) 0.422 (0.089) 0.417 (0.085) 0.161 (0.004) 823 14-Mar-02 0.810 (0.005) 991 28-May-02 0.813 (0.039) 0.369 (0.035) 0.487 (0.041) 0.144 (0.006) 892 14-Jul-02 0.832 (0.010) 0.336 (0.000) 0.501 (0.018) 0.163 (0.018) 505 30-Aug-02 0.831 (0.033) 0.298 (0.018) 0.550 (0.018) 0.152 (0.001) 426 23-Oct-02 0.820 (0.019) 0.293 (0.067) 0.515 (0.059) 0.192 (0.008) 632 Whole-day PAR-weighted quantum efficiency Daily C gain (mgC m−2 day−1) Date Fv/Fm |$\Phi$|PSII |$\Phi$|NPQ |$\Phi$|NO Control trees 12-Jun-01 0.804 (0.011) 185 23-Jul-01 0.803 (0.012) 102 22-Aug-01 0.825 (0.008) 0.233 (0.097) *** 0.600 (0.094) *** 0.167 (0.002) 143 14-Nov-01 0.837 (0.007) 0.249 (0.018) *** 0.611 (0.024) *** 0.140 (0.020) 108 18-Dec-01 0.802 (0.006) 0.262 (0.003) ** 0.562 (0.001) ** 0.176 (0.003) *** 466 14-Mar-02 0.821 (0.007) 867 28-May-02 0.823 (0.011) 0.262 (0.017) *** 0.642 (0.020) *** 0.097 (0.003) *** 265 14-Jul-02 0.818 (0.014) 0.182 (0.062) *** 0.645 (0.036) *** 0.173 (0.026) 84 30-Aug-02 0.810 (0.013) 0.121 (0.023) *** 0.773 (0.039) *** 0.105 (0.016) *** 33 23-Oct-02 0.796 (0.030) 0.149 (0.035) *** 0.671 (0.019) *** 0.181 (0.017) 97 Irrigated trees 12-Jun-01 0.814 (0.016) 669 23-Jul-01 0.833 (0.016) 562 22-Aug-01 0.850 (0.005) 0.478 (0.059) 0.358 (0.070) 0.164 (0.011) 844 14-Nov-01 0.845 (0.011) 0.573 (0.024) 0.295 (0.026) 0.133 (0.002) 655 18-Dec-01 0.823 (0.008) 0.422 (0.089) 0.417 (0.085) 0.161 (0.004) 823 14-Mar-02 0.810 (0.005) 991 28-May-02 0.813 (0.039) 0.369 (0.035) 0.487 (0.041) 0.144 (0.006) 892 14-Jul-02 0.832 (0.010) 0.336 (0.000) 0.501 (0.018) 0.163 (0.018) 505 30-Aug-02 0.831 (0.033) 0.298 (0.018) 0.550 (0.018) 0.152 (0.001) 426 23-Oct-02 0.820 (0.019) 0.293 (0.067) 0.515 (0.059) 0.192 (0.008) 632 Open in new tab Figure 3. Open in new tabDownload slide The relationship between assimilation rate (A) and stomatal conductance (gs) in the control (solid symbols) and irrigated (open symbols) trees. Data are from measurements made throughout the photoperiod (for PAR >1000 μmol m−2 s−1) on the different measurement dates and are the average values of previous and current year needles. The fit (r2 = 0.94) is to all data combined. Figure 3. Open in new tabDownload slide The relationship between assimilation rate (A) and stomatal conductance (gs) in the control (solid symbols) and irrigated (open symbols) trees. Data are from measurements made throughout the photoperiod (for PAR >1000 μmol m−2 s−1) on the different measurement dates and are the average values of previous and current year needles. The fit (r2 = 0.94) is to all data combined. Photosystem efficiencies and pigment content Photosystem II efficiency (ΦPSII) showed characteristic diurnal patterns in both treatments, with a decrease during the morning to a MD minimum as radiation increased, followed by recovery in the afternoon (Figure 2C and D). The initial points of each ΦPSII curve in Figure 2 are the pre-dawn, dark-adapted Fv/Fm values or maximal efficiencies. In all cases the PSII efficiencies had returned to near their pre-dawn values by the end of the photoperiod, and the Fv/Fm values remained high through the seasons in all samples (Table 1). There was no difference in mean Fv/Fm values across the study period between age classes within a treatment (paired sample t-test between age classes on the same individual), but the mean Fv/Fm value was slightly higher in the irrigated trees (0.815 ± 0.012 and 0.827 ± 0.014 in the control and irrigated samples, respectively, for mean ± SD, n = 10, significantly different at the 0.05 level, unpaired t-test of treatment means). Concurrent with the diurnal changes in ΦPSII were changes in the efficiency of regulated thermal dissipation (ΦNPQ) that balanced the changes in ΦPSII, with constitutive dissipation (ΦNO) remaining stable during the day (Figure 4). Non-photochemical quenching as parameterized by both ΦNPQ and NPQ were similarly correlated with diurnal changes in the de-epoxidation state of the xanthophyll-cycle pigments (DPS = (A + Z)/(V + A + Z), Figure 4). The coefficients of determination (r2) values ranged between 0.46 and 0.94 for the relationship between NPQ and DPS (data not shown) and were significant in both treatments for August and October. For all data (treatments and dates combined) the relationships were ΦNPQ = 0.817·DPS + 0.17 (r2 = 0.63, P < 0.0001) and NPQ = 8.86·DPS – 0.15 (r2 = 0.69, P < 0.0001). Figure 4. Open in new tabDownload slide Diurnal time courses of the quantum efficiency of regulated thermal dissipation (ΦNPQ, black circles) and constitutive dissipation (ΦNO, open circles) and the de-epoxidated state of xanthophyll cycle pigments (DPS, gray squares) for control (A–C) and irrigated (D–F) trees for three dates in the year. Figure 4. Open in new tabDownload slide Diurnal time courses of the quantum efficiency of regulated thermal dissipation (ΦNPQ, black circles) and constitutive dissipation (ΦNO, open circles) and the de-epoxidated state of xanthophyll cycle pigments (DPS, gray squares) for control (A–C) and irrigated (D–F) trees for three dates in the year. Seasonal changes in pigment contents were correlated between the two treatments (Table 2). No clear diurnal patterns were observed in the pigments other than those of the xanthophyll cycle. Both chlorophyll and total carotenoid content was higher in the irrigated trees, but chlorophyll content decreased seasonally in both the irrigated and non-irrigated trees (Table 2). Total chlorophyll content decreased by 53% in the control and by 46% in the irrigated samples between March and August, resulting in reductions in leaf absorbance (α) from 0.87 to 0.76 (control) and from 0.89 to 0.81 (irrigated) between March and October. The total carotenoid content was variable, but also at a minimum in August in both treatments. The carotenoid pigments were evenly divided between the xanthophylls and carotenes in March and May, but the xanthophyll component increased to 86% (control) and 72% (irrigated) in August. Although lutein typically comprised the largest part of the xanthophyll pool (between 40% and 60%), the seasonal xanthophyll increase was driven by a fourfold to fivefold increase in the xanthophyll-cycle pigments (V, A, Z), with similar decreases in the precursor β-carotene. A common relationship between the carotene and xanthophyll components of the carotenoids was present across both treatments, with Xan = 0.67.Car + 0.17 (r2 = 0.82, P = 0.002), where Xan and Car are the total xanthophyll and carotene contents, respectively. Table 2 Pigment concentrations (mg gDW−1) and ratios in the control and irrigated P. halepensis trees at different points in the season. Values are means (se), n = 12. (V: violaxanthin; A: antheraxanthin; Z: zeaxanthin) Pigment contents (mg g DW-1) Chlorophyll (a + b) Total carotenoids V + a + z Neoxanthin Lutein A-carotene B-carotene Date Control trees 14-Mar-02 2.499 (0.146) 0.452 (0.025) 0.025 (0.002) 0.058 (0.039) 0.131 (0.032) 0.048 (0.027) 0.190 (0.042) 28-May-02 2.069 (0.040) 0.620 (0.017) 0.083 (0.003) 0.064 (0.035) 0.144 (0.053) 0.082 (0.124) 0.247 (0.081) 30-Aug-02 1.438 (0.031) 0.230 (0.021) 0.069 (0.005) 0.044 (0.203) 0.086 (0.137) 0.010 (0.261) 0.041 (0.282) 23-Oct-02 1.166 (0.038) 0.366 (0.031) 0.096 (0.007) 0.033 (0.066) 0.085 (0.050) 0.020 (0.210) 0.128 (0.034) Irrigated trees 14-Mar-02 2.819 (0.112) 0.491 (0.036) 0.023 (0.003) 0.069 (0.048) 0.170 (0.053) 0.050 (0.076) 0.179 (0.051) 28-May-02 2.291 (0.028) 0.690 (0.025) 0.075 (0.004) 0.071 (0.063) 0.166 (0.074) 0.094 (0.103) 0.266 (0.061) 30-Aug-02 1.649 (0.011) 0.271 (0.019) 0.042 (0.004) 0.049 (0.074) 0.105 (0.073) 0.014 (0.163) 0.074 (0.170) 23-Oct-02 1.528 (0.028) 0.435 (0.023) 0.108 (0.008) 0.044 (0.046) 0.100 (0.078) 0.049 (0.202) 0.137 (0.060) Pigment ratios Carotenoid/chlorophyll Xanthophyll/chlorophyll Carotene/chlorophyll Xanthophyll/carotenoid Carotene/carotenoid Control trees 14-Mar-02 0.181 0.085 0.095 0.473 0.527 28-May-02 0.299 0.141 0.159 0.470 0.530 30-Aug-02 0.160 0.138 0.036 0.864 0.222 23-Oct-02 0.314 0.184 0.127 0.586 0.405 Irrigated trees 14-Mar-02 0.174 0.093 0.081 0.535 0.465 28-May-02 0.301 0.136 0.157 0.453 0.523 30-Aug-02 0.164 0.119 0.053 0.723 0.324 23-Oct-02 0.285 0.165 0.122 0.580 0.428 Pigment contents (mg g DW-1) Chlorophyll (a + b) Total carotenoids V + a + z Neoxanthin Lutein A-carotene B-carotene Date Control trees 14-Mar-02 2.499 (0.146) 0.452 (0.025) 0.025 (0.002) 0.058 (0.039) 0.131 (0.032) 0.048 (0.027) 0.190 (0.042) 28-May-02 2.069 (0.040) 0.620 (0.017) 0.083 (0.003) 0.064 (0.035) 0.144 (0.053) 0.082 (0.124) 0.247 (0.081) 30-Aug-02 1.438 (0.031) 0.230 (0.021) 0.069 (0.005) 0.044 (0.203) 0.086 (0.137) 0.010 (0.261) 0.041 (0.282) 23-Oct-02 1.166 (0.038) 0.366 (0.031) 0.096 (0.007) 0.033 (0.066) 0.085 (0.050) 0.020 (0.210) 0.128 (0.034) Irrigated trees 14-Mar-02 2.819 (0.112) 0.491 (0.036) 0.023 (0.003) 0.069 (0.048) 0.170 (0.053) 0.050 (0.076) 0.179 (0.051) 28-May-02 2.291 (0.028) 0.690 (0.025) 0.075 (0.004) 0.071 (0.063) 0.166 (0.074) 0.094 (0.103) 0.266 (0.061) 30-Aug-02 1.649 (0.011) 0.271 (0.019) 0.042 (0.004) 0.049 (0.074) 0.105 (0.073) 0.014 (0.163) 0.074 (0.170) 23-Oct-02 1.528 (0.028) 0.435 (0.023) 0.108 (0.008) 0.044 (0.046) 0.100 (0.078) 0.049 (0.202) 0.137 (0.060) Pigment ratios Carotenoid/chlorophyll Xanthophyll/chlorophyll Carotene/chlorophyll Xanthophyll/carotenoid Carotene/carotenoid Control trees 14-Mar-02 0.181 0.085 0.095 0.473 0.527 28-May-02 0.299 0.141 0.159 0.470 0.530 30-Aug-02 0.160 0.138 0.036 0.864 0.222 23-Oct-02 0.314 0.184 0.127 0.586 0.405 Irrigated trees 14-Mar-02 0.174 0.093 0.081 0.535 0.465 28-May-02 0.301 0.136 0.157 0.453 0.523 30-Aug-02 0.164 0.119 0.053 0.723 0.324 23-Oct-02 0.285 0.165 0.122 0.580 0.428 Open in new tab Table 2 Pigment concentrations (mg gDW−1) and ratios in the control and irrigated P. halepensis trees at different points in the season. Values are means (se), n = 12. (V: violaxanthin; A: antheraxanthin; Z: zeaxanthin) Pigment contents (mg g DW-1) Chlorophyll (a + b) Total carotenoids V + a + z Neoxanthin Lutein A-carotene B-carotene Date Control trees 14-Mar-02 2.499 (0.146) 0.452 (0.025) 0.025 (0.002) 0.058 (0.039) 0.131 (0.032) 0.048 (0.027) 0.190 (0.042) 28-May-02 2.069 (0.040) 0.620 (0.017) 0.083 (0.003) 0.064 (0.035) 0.144 (0.053) 0.082 (0.124) 0.247 (0.081) 30-Aug-02 1.438 (0.031) 0.230 (0.021) 0.069 (0.005) 0.044 (0.203) 0.086 (0.137) 0.010 (0.261) 0.041 (0.282) 23-Oct-02 1.166 (0.038) 0.366 (0.031) 0.096 (0.007) 0.033 (0.066) 0.085 (0.050) 0.020 (0.210) 0.128 (0.034) Irrigated trees 14-Mar-02 2.819 (0.112) 0.491 (0.036) 0.023 (0.003) 0.069 (0.048) 0.170 (0.053) 0.050 (0.076) 0.179 (0.051) 28-May-02 2.291 (0.028) 0.690 (0.025) 0.075 (0.004) 0.071 (0.063) 0.166 (0.074) 0.094 (0.103) 0.266 (0.061) 30-Aug-02 1.649 (0.011) 0.271 (0.019) 0.042 (0.004) 0.049 (0.074) 0.105 (0.073) 0.014 (0.163) 0.074 (0.170) 23-Oct-02 1.528 (0.028) 0.435 (0.023) 0.108 (0.008) 0.044 (0.046) 0.100 (0.078) 0.049 (0.202) 0.137 (0.060) Pigment ratios Carotenoid/chlorophyll Xanthophyll/chlorophyll Carotene/chlorophyll Xanthophyll/carotenoid Carotene/carotenoid Control trees 14-Mar-02 0.181 0.085 0.095 0.473 0.527 28-May-02 0.299 0.141 0.159 0.470 0.530 30-Aug-02 0.160 0.138 0.036 0.864 0.222 23-Oct-02 0.314 0.184 0.127 0.586 0.405 Irrigated trees 14-Mar-02 0.174 0.093 0.081 0.535 0.465 28-May-02 0.301 0.136 0.157 0.453 0.523 30-Aug-02 0.164 0.119 0.053 0.723 0.324 23-Oct-02 0.285 0.165 0.122 0.580 0.428 Pigment contents (mg g DW-1) Chlorophyll (a + b) Total carotenoids V + a + z Neoxanthin Lutein A-carotene B-carotene Date Control trees 14-Mar-02 2.499 (0.146) 0.452 (0.025) 0.025 (0.002) 0.058 (0.039) 0.131 (0.032) 0.048 (0.027) 0.190 (0.042) 28-May-02 2.069 (0.040) 0.620 (0.017) 0.083 (0.003) 0.064 (0.035) 0.144 (0.053) 0.082 (0.124) 0.247 (0.081) 30-Aug-02 1.438 (0.031) 0.230 (0.021) 0.069 (0.005) 0.044 (0.203) 0.086 (0.137) 0.010 (0.261) 0.041 (0.282) 23-Oct-02 1.166 (0.038) 0.366 (0.031) 0.096 (0.007) 0.033 (0.066) 0.085 (0.050) 0.020 (0.210) 0.128 (0.034) Irrigated trees 14-Mar-02 2.819 (0.112) 0.491 (0.036) 0.023 (0.003) 0.069 (0.048) 0.170 (0.053) 0.050 (0.076) 0.179 (0.051) 28-May-02 2.291 (0.028) 0.690 (0.025) 0.075 (0.004) 0.071 (0.063) 0.166 (0.074) 0.094 (0.103) 0.266 (0.061) 30-Aug-02 1.649 (0.011) 0.271 (0.019) 0.042 (0.004) 0.049 (0.074) 0.105 (0.073) 0.014 (0.163) 0.074 (0.170) 23-Oct-02 1.528 (0.028) 0.435 (0.023) 0.108 (0.008) 0.044 (0.046) 0.100 (0.078) 0.049 (0.202) 0.137 (0.060) Pigment ratios Carotenoid/chlorophyll Xanthophyll/chlorophyll Carotene/chlorophyll Xanthophyll/carotenoid Carotene/carotenoid Control trees 14-Mar-02 0.181 0.085 0.095 0.473 0.527 28-May-02 0.299 0.141 0.159 0.470 0.530 30-Aug-02 0.160 0.138 0.036 0.864 0.222 23-Oct-02 0.314 0.184 0.127 0.586 0.405 Irrigated trees 14-Mar-02 0.174 0.093 0.081 0.535 0.465 28-May-02 0.301 0.136 0.157 0.453 0.523 30-Aug-02 0.164 0.119 0.053 0.723 0.324 23-Oct-02 0.285 0.165 0.122 0.580 0.428 Open in new tab Seasonal energy dissipation patterns Seasonally, the MD minimum ΦPSII values were lower in the summer than in winter in both treatments and were always lower in the control samples compared with the irrigated plants (Figure 5), while constitutive dissipation (ΦNO) remained at between 15–20% of absorbed irradiance in both treatments through the seasons. The proportion of light absorbed at MD and used in photochemical electron transport declined from 30% in winter to 6% in summer in the control trees, while in the irrigated trees, MD ΦPSII remained at 25–30% for much of the year and reached up to 50% in the cooler wet season (Figure 5). From the days where measurements covered the full diurnal cycle, estimates of the total daily allocation of absorbed energy to the various dissipation pathways were made by weighting the efficiencies at each time step by the incident PAR (Table 1). This weighting provided the actual energy allocation to the various sinks at the integrated daily scale. The whole day allocation to photochemistry in summer was about half of that in winter in the control trees and 60–70% of winter values in the irrigated trees, showing less reduction over the diurnal cycle than from the MD measurements. The inversely proportional increases in ΦNPQ relative to the decreases in ΦPSII resulted in ~50% and up to nearly 80% of the daily absorbed energy being dissipated through regulated thermal mechanisms in summer in the irrigated and control trees, respectively. The daily mean values of ΦPSII and ΦNPQ were statistically different between the control and irrigated trees on each day of measurement in the season (Table 1, unpaired t-test between treatment means). Figure 5. Open in new tabDownload slide The proportional allocation of absorbed light energy at MD to the various photosystem dissipation pathways within in the control (left) and irrigated trees (right) across the experimental period. Open symbols, gray shading: constitutive dissipation (ΦNO), open shading, gray symbols: photochemical dissipation (ΦPSII), hatched shading, black symbols: regulated thermal dissipation (ΦNPQ). Circles: current year (y0) needles, squares: previous year (y1) needles. The lines are through the average values of the needle age classes, and the area of shading represents the energy allocation to that pathway. Figure 5. Open in new tabDownload slide The proportional allocation of absorbed light energy at MD to the various photosystem dissipation pathways within in the control (left) and irrigated trees (right) across the experimental period. Open symbols, gray shading: constitutive dissipation (ΦNO), open shading, gray symbols: photochemical dissipation (ΦPSII), hatched shading, black symbols: regulated thermal dissipation (ΦNPQ). Circles: current year (y0) needles, squares: previous year (y1) needles. The lines are through the average values of the needle age classes, and the area of shading represents the energy allocation to that pathway. The response to incident PAR of ETR and thermal dissipation rate (TDR) derived from the ΦPSII and ΦNPQ data show a separation of the control data into two groups (Figure 6): one associated with the wet season (December—May) and the other the dry season (including early autumn, i.e., June–November). The ETRs were similar between treatments at low PAR (up to ~300 μmol m−2 s−1), above which the rates in the dry period were lower than the wet period and irrigated data (Figure 6A). The initial slopes of the curves (where response was linear, at PAR less than 100 μmol m−2 s−1) were 0.25 ± 0.01, 0.29 ± 0.004 and 0.30 ± 0.006 for the dry season, wet season and irrigated data, respectively. At high PAR (above ~1200 μmol m−2 s−1), ETR started to decrease in the dry season. Maximal (light saturated) ETR was about 150 μmol m−2 s−1 in the wet period and 50–75 μmol m−2 s−1 in the dry period in the control trees. Maximal ETR in the irrigated trees was quite variable, between about 150 and 250 μmol m−2 s−1. The TDR rates were ~70% of the incident photon flux at the high light levels in the dry season control trees, compared with about 40–50% in the irrigated trees (Figure 6B). Figure 6. Open in new tabDownload slide The dependence on PAR of ETR (A), TDR (B) and photorespiratory CO2 release (Rl, C) from diurnal measurements at different periods in the season. The control trees data are separated into dry season (black circles) and wet season (gray circles) data, the irrigated data (open circles) are from all dates. Figure 6. Open in new tabDownload slide The dependence on PAR of ETR (A), TDR (B) and photorespiratory CO2 release (Rl, C) from diurnal measurements at different periods in the season. The control trees data are separated into dry season (black circles) and wet season (gray circles) data, the irrigated data (open circles) are from all dates. Estimates of the rate of photorespiratory CO2 release (Rl) were calculated from the estimates of non-assimilatory electron flow derived from the values of ETR and gas exchange measurements (Figure 6C). Overall, photorespiratory CO2 release was greater in the irrigated trees as a result of the overall higher ETR in the irrigated samples, and again there was similarity between wet season control trees and the irrigated trees. However, photorespiration rates in summer were about half those observed in the wet period in the control trees. Energy allocation in response to leaf water stress The proportional allocation of absorbed light energy to photosynthesis, non-assimilatory electron flow or pigment-mediated thermal dissipation mechanisms under saturating light have non-linear responses to stomatal conductance (Figure 7). At a stomatal conductance above ~0.1 mol m−2 s−1 there was little variation in the energy allocation between the pathways, (Figure 7A–C) and the allocation of total electron transport to non-assimilatory electron flow (Jo/ETR, Figure 7D). However, at gs below this apparent critical level there was an increase in thermal dissipation (from ~50 to 70%) resulting in a steep decrease in allocation to CO2 fixation and a lesser decrease in the allocation to non-assimilatory electron sinks, such that there was an increase in Jo/ETR. The nature of the response to water potential differs in that the allocation to Rubisco activity was sigmoidal in nature, with a rapid transition between a water potential of −2.3 to −2.5 MPa, while the allocation to thermal dissipation and the Jo/ETR ratio increased more linearly as stress increased. Figure 7. Open in new tabDownload slide Relationships between energy dissipation parameters and stomatal conductance (A–D) and branch MD water potential (E–H) in the control (solid symbols) and irrigated (open symbols) trees. Proportional energy allocation is the proportion on photochemical energy allocated to CO2 fixation (A, E) or photorespiration (B, F) or the proportion of absorbed light energy allocated to thermal dissipation (C, G). The Jo/ETR ratio is the proportion of total electron transport going to photorespiration. Fitted curves are exponential (A–D) or sigmoidal (E, F) and regression r2 values are 0.87 (A), 0.63 (B), 0.78 (0.78), 0.91 (D), 0.75 (E) and 0.78 (F). The gray shading bars indicate the apparent threshold region in which the transition in the energy allocation patterns occur. Figure 7. Open in new tabDownload slide Relationships between energy dissipation parameters and stomatal conductance (A–D) and branch MD water potential (E–H) in the control (solid symbols) and irrigated (open symbols) trees. Proportional energy allocation is the proportion on photochemical energy allocated to CO2 fixation (A, E) or photorespiration (B, F) or the proportion of absorbed light energy allocated to thermal dissipation (C, G). The Jo/ETR ratio is the proportion of total electron transport going to photorespiration. Fitted curves are exponential (A–D) or sigmoidal (E, F) and regression r2 values are 0.87 (A), 0.63 (B), 0.78 (0.78), 0.91 (D), 0.75 (E) and 0.78 (F). The gray shading bars indicate the apparent threshold region in which the transition in the energy allocation patterns occur. Combined effects of the various pathways Combining the effects of the changes in absorption, energy dissipation and allocation of electron transport to carbon or non-assimilatory sinks, estimates were made of the proportion of light incident on the leaf surface that had its fate in the various pathways or sinks. Seasonal values for the allocation to the main sinks of thermal dissipation, CO2 fixation and photorespiration are shown in Table 1, and a general summary of the stress-dependent seasonal changes between the periods of maximum and minimum CO2 assimilation is shown in Figure 8. Around 20% of incident light is reflected or transmitted, following which ~30% is dissipated in the pigment bed under low stress conditions, and up to 50–60% is dissipated thermally under high stress. When conditions for CO2 fixation are most favorable, 20–30% of incident light is used in photosynthesis, and about half this value is used for photorespiration or other non-assimilatory electron sinks. When water limitation is most severe, only ~5% of incident light energy goes toward carbon assimilation and similar amounts are used in photorespiration. Figure 8. Open in new tabDownload slide A schematic representation of allocation to the various energy dissipation pathways and sinks as a proportion of total daily integrated light incident on the leaf surface. The top row represents allocation during low stress and maximal CO2 assimilation rates (irrigated trees in spring and winter) and the bottom row allocation during maximal stress and minimal CO2 assimilation rates (summer in the control trees). Figure 8. Open in new tabDownload slide A schematic representation of allocation to the various energy dissipation pathways and sinks as a proportion of total daily integrated light incident on the leaf surface. The top row represents allocation during low stress and maximal CO2 assimilation rates (irrigated trees in spring and winter) and the bottom row allocation during maximal stress and minimal CO2 assimilation rates (summer in the control trees). Discussion Dynamic energy dissipation maintains stability of the photosynthetic apparatus Despite the long period of soil water deficit, high vapor pressure deficit and high radiation loads, there were no indications of significant photoinhibitory damage observed in P. halepensis under either irrigated or non-irrigated conditions. The near complete recovery of ΦPSII by the end of the day (Figure 2), and long-term stability in Fv/Fm in both control and irrigated trees (Table 1) at values typical of non-stressed plants (ca 0.83; Björkman and Demmig 1987), shows there was little cumulative effect of the high light exposure through the long drought period (Baquedano and Castillo 2007). The similarity in the A–gs response between the treatments (Figure 3) indicates that the low assimilation rates under the water and atmospheric stress are due primarily to diffusive limitation to gas exchange, rather than metabolic impairment (Flexas et al. 2004,Klein et al. 2011), supporting the view that PSII is relatively stable under drought (Havaux 1992, Cornic 2000). Overall, the majority of light energy incident on the leaves was excessive to photosynthetic requirements but photosystem integrity was maintained through non-photosynthetic dissipation mechanisms. The main component of the non-photochemical energy dissipation was the light-regulated thermal dissipation involving pH-mediated xanthophyll-cycle pigments (Figures 4 and 5). Constitutive or basal dissipation remained constant (at ~15% of absorbed light), while the regulated thermal dissipation accounted for at least 50% of absorbed light energy during MD in winter, and reached up to ~80% in summer in the control trees. Non-photochemical quenching parameters are known to be correlated with changes in the xanthophyll cycle pigments (Adams and Demmig-Adams 1994), and we found that both diurnal and seasonal changes in ΦNPQ were highly correlated with xanthophyll-cycle pigment state, and higher levels of xanthophyll cycle pigments were produced in the non-irrigated trees. The low correlation between ΦNPQ and DPS in the irrigated plot during May and October may be attributed to the contribution of different mechanisms of heat dissipation, including proton pumping to decrease the pH gradient from excess light energy (Ruban 2016), thylakoid protein composition and phosphorylation (Demmig-Adams et al. 2012), or reuse of excess energy through cyclic electron transport (Kramer and Evans 2011). Sustained photoinhibition effects can decrease plant productivity and distribution under semi-arid conditions (Werner et al. 2001, Valladares et al. 2005). Investing in a reliance on regulated thermal dissipation over the extensive drought period, rather than increasing basal dissipation, can be advantageous in terms of productivity (Kornyeyev et al. 2004,Murchie and Niyogi 2011,Kromdijk et al. 2016). The stable level of basal dissipation maintains a high potential to utilize energy in photochemistry, and diurnal-scale regulation of pre-PSII energy dissipation enables photochemistry and CO2 fixation to respond to changes in environmental conditions, including less stressful hours of the day (Figure 2), early or late seasonal rainfall, or milder periods. As an example, average D during the August 2001 campaign was 2.9 kPa, compared with 4.1 kPa in 2002 (Figure 1). Net carbon uptake was maintained throughout the photoperiod in August 2001, but not in 2002 (not shown), resulting in leaf-level carbon gain an order of magnitude higher in 2001 than 2002 (Table 1). The milder conditions could be utilized through maintaining a high potential capacity of the photosystems. The dynamic response of the system can also be seen in the resilience to intense short-term heatwave events (Tatarinov et al. 2016). In this regard, it is interesting to note that the sustained high Fv/Fm and continued reliance on regulated dissipation under these extreme drought conditions contrasts with responses seen to cold winters. Across a range of species and environments, a substantial reduction in Fv/Fm is seen at growth temperatures below 0 °C, and this winter photoinhibition is associated with an increase in DPS xanthophyll pigments (Míguez et al. 2015). Similarly, during an exceptionally cold winter, a number of Mediterranean evergreen species retained de-epoxidized xanthophylls during the night and showed a sustained decrease in Fv/Fm to values <0.6 (García-Plazaola et al. 2003). Both photosystem stability (Damesin and Rambal 1995,Valentini et al. 1995,Faria et al. 1998,Martínez-Ferri et al. 2000,Eppel et al. 2014) and seasonal reductions in PSII performance during drought (Faria et al. 1998,Castillo et al. 2002,Llorens et al. 2003,Baquedano and Castillo 2006,Peguero-Pina et al. 2009) have been observed in Mediterranean tree and shrub species. Differences in drought duration and extent of rooting depth (and therefore access to water) may underlie much of the observed differences between species (Faria et al. 1998, Baquedano and Castillo 2007), as can be seen clearly in the difference between the irrigated and control trees in our study. Nevertheless, the non-irrigated trees, growing on shallow soil and experiencing a long period without rain, were able to maintain PSII functionality over the entire summer season, showing a high resistance to long-term drought conditions in P. halepensis. This low, but continuous, carbon gain sustains leaf development during the long dry summer (Maseyk et al. 2008b) and minimizes plant carbon losses in the photosynthetic ‘off-season’, contributing to the relatively high annual productivity seen in this system (Grünzweig et al. 2003,Maseyk et al. 2008a). Reduced role but increased efficiency of photorespiration under high stress Despite the significant reductions in photochemistry in summer, low stomatal conductance resulted in proportionally greater reductions in net CO2 assimilation rates and an increase in the proportion of photochemical energy going toward non-assimilatory electron sinks (Figure 7D). The estimated proportion of non-assimilatory electron flow increased from a minimum of 45% (winter, irrigated) to a maximum of 0.64% (non-irrigated summer) of total electron transport. These values compare to values of 40–50% seen in Quercus cerris during the Mediterranean summer (Valentini et al. 1995), and are similar to those seen in the desert shrub Reaumuria soongorica under severe drought (Bai et al. 2008). These results support an important photoprotection role of non-assimilatory electron flow under drought stress, providing a sink for excess radiation energy and metabolites (glycine, serine) for antioxidant systems (Cornic and Briantais 1991, Wingler et al. 2000, Bai et al. 2008, Beis and Patakas 2012). However, the large increase in non-photochemical energy dissipation decreased total ETR between winter and summer (Figure 6). Consequently, although the relative flux of PSII electron transport to non-assimilatory electron flow increased, the absolute CO2 loss through photorespiration (Rl) decreased. These results show that as the level of stress increases, greater emphasis on thermal dissipation mechanisms than alternative electron sinks, and the costs involved with increasing thermal dissipation capacity are less than those associated with photorespiration and other non-assimilatory electron sinks. The lower cost in terms of CO2 but increase in proportional flux through photorespiration shows an increased efficiency in the utilization of photorespiration for energy dissipation as conductance decreases and temperature increases. Despite the proportionally lower rates of non-assimilatory electron flow, photorespiratory CO2 loss in summer in the control trees was equivalent to net CO2 uptake in the less stressful periods, and up to an order of magnitude greater than the concurrent net CO2 uptake. Rates of photorespiratory CO2 loss have been found to be similar to or exceed net CO2 uptake in other Mediterranean and savannah species, and may serve to limit leaf carbon balance under high summer irradiances (Valentini et al. 1995, Franco and Lüttge 2002). The rates of photorespiratory CO2 release were also high in the irrigated trees. In absolute terms, they exceeded the rates from the control trees, and were up to 1.5–2 times the rates of irrigated net CO2 assimilation in summer. We cannot exclude the possibility that photorespiratory CO2 release was overestimated, and that other non-assimilatory reduction processes, such as the Mehler reaction, serve as important alternative electron sinks (Badger et al. 2000,Flexas and Medrano 2002,Ort and Baker 2002). However, the photorespiration rates are estimated from the residual of net gas exchange and chlorophyll fluorescence measurements and show that, overall, a high proportion of PSII electron transport must be accounted for by non-assimilatory electron sinks. The ETR values estimated from the fluorescence data in this study were also consistent with those estimated in this forest from gas exchange CO2 response curves in a previous study (Maseyk et al. 2008b). Soil–plant–atmosphere hydrological drivers of photoprotection responses There appears an important stomatal conductance threshold, at ~0.1 mol m−2 s−1, where the shift in energy allocation patterns occurs. Once stomatal conductance dropped below this threshold was there a marked increase in thermal dissipation and reduction in energy allocation toward Rubisco activity (Figure 7A–C), and a decrease in ETR and photorespiratory CO2 release under saturating light (Figure 6A and C). This observation may support the view that chloroplast CO2 concentration has an important role in controlling dissipation activity (Flexas and Medrano 2002), and may serve as a basis for mechanistic predications of vegetation responses under drought conditions. However, these changes also occurred when leaf water potential declined below approximately −2.3 MPa (Figure 7E–H), in a manner similar to that seen in oaks (Peguero-Pina et al. 2009), and it is difficult to separate the role of these two factors on the observed responses, especially considering their mutual interactions (Klein et al. 2011). The current study also provided a unique opportunity to separate possible effects of the more gradual changes of combined soil and atmospheric water stress (control trees) from the more dynamic atmospheric vapor pressure deficits alone (irrigated trees). Atmospheric vapor pressure deficit will become an increasingly limiting factor for photosynthesis as the atmosphere warms and needs to be considered explicitly in climate and land surface model projections (Novick et al. 2016). We found that alleviating soil moisture limitation increased net photosynthetic rates in the summer, but the high D VPD and air temperatures still resulted in a decrease in net carbon gain by >50% from spring values (Table 1, Figure 2). However, it is interesting to note in this regard that while the soil + atmosphere stress resulted in a lower stomatal conductance on a given day, the energy partitioning as a function of gs (or Ψ) appeared to lie on the same response curve (Figure 7A–D) for the both atmosphere-only and soil + atmosphere deficits. Conclusions This study identified and quantified a range of photoprotection mechanisms that provide insight into the high productivity of a semi-arid pine forest at the dry timberline. Sustained regulated non-photochemical quenching is key for capitalizing on variation in environmental conditions at diurnal, synoptic and seasonal scales, but system-level resilience of the photosynthetic system also involves reductions in chlorophyll content and increased efficiency in photorespiratory energy dissipation. Summer supplemental irrigation, relieving soil water stress, indicated a consistency in leaf-level photoprotection responses to soil- and atmospherically derived stress on the basis of stomatal conductance and leaf water potential. These results support the potential for afforestation and sustainable forest productivity in degraded semi-arid zones that are also predicted to undergo significant drying trends in the coming century. Acknowledgments We thank Y. Moshe and the KKL/JNF for cooperation and logistics at the field site. Emanuela Negreanu, Ruth Ben-Meir, Hagai Sagi and Avraham Pelner provided much appreciated technical assistance for various aspects of this study, and Eyal Rotenberg is thanked for his invaluable role in maintaining the flux tower and meteorological instruments. Conflict of interest None declared. Funding This project was supported by grants from the Israel Science Foundation (695/99) and the Minerva-Avron Photosynthesis Center. The long-term operation of the Yatir Forest Research Field Site is supported by the Cathy Wills and Robert Lewis program in Environmental Science. References Adams HD , Zeppel MJB , Anderegg WRL et al. ( 2017 ) A multi-species synthesis of physiological mechanisms in drought-induced tree mortality . Nat Ecol Evol 1 : 1285 – 1291 . Google Scholar Crossref Search ADS PubMed WorldCat Adams WW3rd , Demmig-Adams B ( 1994 ) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter . Physiol Plant 92 : 451 – 458 . 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TI - Quantification of leaf-scale light energy allocation and photoprotection processes in a Mediterranean pine forest under extensive seasonal drought
JF - Tree Physiology
DO - 10.1093/treephys/tpz079
DA - 2019-10-01
UR - https://www.deepdyve.com/lp/oxford-university-press/quantification-of-leaf-scale-light-energy-allocation-and-WNOeWOckbT
SP - 1767
VL - 39
IS - 10
DP - DeepDyve
ER -