Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests

Abstract

During winter and early spring, evergreen boreal conifers are severely stressed because light energy cannot be used when photosynthesis is pre-empted by low ambient temperatures. To study photosynthetic performance dynamics in a severe boreal climate, seasonal changes in photosynthetic pigments, chloroplast proteins and photochemical efficiency were studied in a Scots pine forest near Zotino, Central Siberia. In winter, downregulation of photosynthesis involved loss of chlorophylls, a twofold increase in xanthophyll cycle pigments and sustained high levels of the light stress-induced zeaxanthin pigment. The highest levels of xanthophylls and zeaxanthin did not occur during the coldest winter period, but rather in April when light was increasing, indicating an increased capacity for thermal dissipation of excitation energy at that time. Concomitantly, in early spring the D1 protein of the photosystem II (PSII) reaction centre and the light-harvesting complex of PSII dropped to their lowest annual levels. In April and May, recovery of PSII activity, chloroplast protein synthesis and rearrangements of pigments were observed as air temperatures increased above 0 1C. Nevertheless, severe intermittent low-temperature episodes during this period not only halted but actually reversed the physiological recovery. During these spring low-temperature episodes, protective processes involved a complementary function of the PsbS and early lightinduced protein thylakoid proteins. Full recovery of photosynthesis did not occur until the end of May. Our results show that even after winter cold hardening, photosynthetic activity in evergreens responds opportunistically to environmental change throughout the cold season. Therefore, climate change effects potentially improve the sink capacity of boreal forests for atmospheric carbon. However, earlier photosynthesis in spring in response to warmer temperatures is strongly constrained by environmental variation, counteracting the positive effects of an early recovery process. PPFD 5 photosynthetic photon flux density (mmol photons m À2 s À1 ) PSI or PSII 5 photosystem I or photosystem II, respectively PsbS 5 protein involved in nonphotochemical quenching RC 5 reaction centre of the photosystems V 5 violaxanthin Z 5 zeaxanthin

Annual cycle of Scots pine photosynthesis

“…The needle metabolism also has a clear annual cycle that alternates between the cold tolerance and very low metabolic activity during winter and the strong metabolism and cold vulnerability in summer. The annual cycle is particularly strong in photosynthesis (Ens- G G G G G G G G G G G G G G G G G G G G G G , 2004b;Kolari et al, 2014;Öquist and Huner, 2003;Pelkonen and Hari, 1980). We have worked decades with the annual cycle of vegetation from the analysis of daily shoot elongation (Hari and Leikola, 1972;Hari et al, 1977), bud burst of trees (Hari and Häkkinen, 1991) and photosynthesis (Pelkonen and Hari, 1980).…”

“…This seasonality has been closely connected to variations in ambient temperatures (Mäkelä et al, 2004;Pelkonen and Hari, 1980) and photoperiod or light intensity changes (Ensminger et al, 2004a;Porcar-Castell et al, 2008). A delayed effect of temperature on photosynthesis recovery in spring is introduced (Mäkelä et al, 2004;Pelkonen and Hari, 1980) and tested with field measurements (Kolari et al, 2009).…”

“…The maintenance of the proper concentrations of the components in this machinery is taken care of by a very powerful biological regulation system that has emerged through evolution to match the cellular metabolism with the regular annual cycle of solar light and temperature and is capable of modifying the processes within the normal range of conditions but also provides sufficient resilience under sudden (short-term) extreme conditions during the transition from winter to spring (Ensminger et al, 2004a;Zarter et al, 2006). This system synthesises, activates, decomposes and deactivates the critical photosynthetic machinery over timescales of days (Nelson et al, 2014), and it is an acclimation system affecting the activation and deactivation of transcriptional modules responsive to light and temperature cues (e.g.…”

Expression of LHC Genes and their Relation to Photo-Oxidative Stress Tolerance Tolerance in Solanum lycopersicum L. and Solanum chilense (Dunal) Reiche

“…Interestingly, there are reports that under certain conditions (e.g. high-light) there is a differential expression of LHCI genes (Bailey et al, 2001;Ensminger et al, 2004;Gáspár et al, 2006). On the other hand, Wehner et al (2004) suggested that the zeaxanthin formed in LHCI proteins is involved in an antioxidative mechanism implicated in suppression of ROS-triggered lipid peroxidation rather than heat energy dissipation (NPQ), which could be consistent with our observations on the accumulation of zeaxanthin ( Figure 3B) which can function as antioxidant, as evidenced by the amount of peroxidized lipids (Figure 4) and the invariable value of NPQ ( Figure 2C).…”

“…from a state of efficient light harvesting to a state of high thermal energy dissipation; Nelson and Yocum, 2006). This change is related to differential expression of genes encoding LHC proteins (Demmig-Adams et al, 1996;Savitch et al, 2002;Ensminger et al, 2004). It was proposed that PsbS, a distant member of the LHC family, might play a protective role within the thylakoids under photoinhibitory conditions, with a central role in NPQ (Li et al, 2000).…”