Increased air temperature during simulated autumn conditions does not increase photosynthetic carbon gain but affects the dissipation of excess energy in seedlings of the evergreen conifer Jack pine

Abstract

Temperature and daylength act as environmental signals that determine the length of the growing season in boreal evergreen conifers. Climate change might affect the seasonal development of these trees, as they will experience naturally decreasing daylength during autumn, while at the same time warmer air temperature will maintain photosynthesis and respiration. We characterized the down-regulation of photosynthetic gas exchange and the mechanisms involved in the dissipation of energy in Jack pine (Pinus banksiana) in controlled environments during a simulated summer-autumn transition under natural conditions and conditions with altered air temperature and photoperiod. Using a factorial design, we dissected the effects of daylength and temperature. Control plants were grown at either warm summer conditions with 16-h photoperiod and 22 degrees C or conditions representing a cool autumn with 8 h/7 degrees C. To assess the impact of photoperiod and temperature on photosynthesis and energy dissipation, plants were also grown under either cold summer (16-h photoperiod/7 degrees C) or warm autumn conditions (8-h photoperiod/22 degrees C). Photosynthetic gas exchange was affected by both daylength and temperature. Assimilation and respiration rates under warm autumn conditions were only about one-half of the summer values but were similar to values obtained for cold summer and natural autumn treatments. In contrast, photosynthetic efficiency was largely determined by temperature but not by daylength. Plants of different treatments followed different strategies for dissipating excess energy. Whereas in the warm summer treatment safe dissipation of excess energy was facilitated via zeaxanthin, in all other treatments dissipation of excess energy was facilitated predominantly via increased aggregation of the light-harvesting complex of photosystem II. These differences were accompanied by a lower deepoxidation state and larger amounts of beta-carotene in the warm autumn treatment as well as by changes in the abundance of thylakoid membrane proteins compared to the summer condition. We conclude that photoperiod control of dormancy in Jack pine appears to negate any potential for an increased carbon gain associated with higher temperatures during the autumn season.

Figure 1.

The effect of daylength and temperature on needle level CO₂ assimilation and respiration per needle area. Bars indicate light-saturated net CO₂ assimilation, measured at 1,000 μmol photons m⁻² s⁻¹ PPFD (A_sat), CO₂ assimilation at growth light conditions of 350 μmol photons m⁻² s⁻¹ PPFD (A₃₅₀). Black bars indicate dark respiration measured after 20 min of dark acclimation. All measurements were performed at growth temperature (22°C in LD/HT and SD/HT, 7°C in LD/LT and SD/LT plants). Each bar represents the average of n = 7 to 8 ± se biological replicates. •, ▪, and *, Significant differences due to daylength, temperature, and their interactive effect, respectively. Two symbols, P ≤ 0.01; three symbols, P ≤ 0.001.

Figure 2.

A, The effect of daylength and temperature on quantum yield of PSII under steady-state condition at 1,000 μmol photons m⁻² s⁻¹ PPFD. B, Estimated q_P. C, q_O/q_N as an estimate of the amount of q_O. All measurements were performed at growth temperature (22°C for LD/HT and SD/HT and 7°C for LD/LT and SD/LT). Each bar represents the average of n = 8 ± se biological replicates. •, ▪, and *, Significant differences due to daylength, temperature, and their interactive effect, respectively. Two symbols, P ≤ 0.01; three symbols, P ≤ 0.001.

Figure 3.

The effect of daylength and temperature on the degree of aggregation of LHCII. Bars indicate the ratio of LHCII³ and LHCII² to LHCII¹ as determined from nondenaturing SDS-PAGE. Each bar represents the average of n = 4 ± se biological replicates.

Figure 4.

The effect of daylength and temperature on the composition of photosynthetic pigments in needles of Jack pine. A, Total Chl per fresh weight; Chl b was affected by temperature. B, Chl a to Chl b ratio. C, Total carotenoids per total Chl. D, Deepoxidation status of the xanthophyll cycle pigments, calculated as (0.5A + Z)/(V + A + Z). Each bar represents the average of n = 8 ± se biological replicates. •, ▪, and *, Significant differences due to daylength, temperature, and their interactive effect, respectively. One symbol, P ≤ 0.05; two symbols, P ≤ 0.01; three symbols, P ≤ 0.001.

Figure 5.

The effect of daylength and temperature on the carotenoid composition in needles of Jack pine. Each carotenoid component is normalized to the total amount of carotenoids. The relative size of each pie reflects the amount of carotenoids based on a per total Chl basis. βC, β-carotene; V, violaxanthin; A, antheraxanthin; Z, zeaxanthin; L, lutein; N, neoxanthin. Values represent the average of n = 8 ± se biological replicates.

Figure 6.

The effect of daylength and temperature on the expression levels of key proteins of photosynthesis in needles of Jack pine. The average optical density of the LD/HT treatment was arbitrarily scaled to 1. Typical bands from the original western blots are shown next to the values, with each lane loaded on an equal protein basis. Each value represents the average of n = 8 ± se biological replicates. Two-way ANOVA analysis indicates statistically significant differences due to daylength, temperature, or an interactive effect of both factors. •, ▪, and *, Significant differences due to daylength, temperature, and their interactive effect, respectively. One symbol, P ≤ 0.05; two symbols, P ≤ 0.01; three symbols, P ≤ 0.001; n.s., not significant.

Figure 7.

Model of extended energy quenching including LHCII aggregation. The model depicts the amount of photochemical and NPQ controlled by the deepoxidation state of the xanthophyll cycle and the aggregation state of LHCII, based on the model of Horton et al. (2005). Energy absorbed (yellow arrows) is quenched either nonphotochemically (black arrows) in the antenna complex (green rectangles) or photochemically through the photosystems (white parts, open RCs; hatched parts, closed RCs) and used for CO₂ fixation (gray arrows). Depending on the aggregation state of LHCII (represented by the proximity of the green rectangles) and the xanthophyll configuration, energy is preferentially quenched one way or the other (the thickness of the arrows marks the efficiency of the respective processes). State A refers to the situation found in our LD/HT treatment, with a low aggregation state of LHCII in combination with a high deepoxidation state. State B is dominant in the SD/HT treatment, where high aggregation of LHCII coincides with a very low zeaxanthin concentration. This results in nonphotochemical and photochemical quenching that compares to the situation observed in state A, except that not all of the energy provided through the photochemical quenching process is used for CO₂ fixation. In this situation, alternative electron sinks, including photorespiration, water-water cycle, and charge recombination, play a prominent photoprotective role to support the photochemical quenching process. State C refers to both the LD/LT and SD/LT treatments, with high aggregation and high deepoxidation states; a large portion of the incident light is quenched in the antenna, photochemical quenching is relatively small. See text for further details.