Sensing environmental temperature change through imbalances between energy supply and energy consumption: Redox state of photosystem II

A basic requirement of all photosynthetic organisms is a balance between overall energy supply through temperature-independent photochemical reactions and energy consumption through the temperature-dependent biochemical reactions of photosynthetic electron transport and contiguous metabolic pathways. Since the turnover of photosystem II (PSII) reaction centers is a limiting step in the conversion of light energy into ATP and NADPH, any energy imbalance may be sensed through modulation of the redox state of PSII. This can be estimated in vivo by chlorophyll a fluorescence as changes in the redox state of PSII, or photosystem II excitation pressure, which reflects changes in the redox poise of intersystem electron transport carriers. Through comparisons of photosynthetic adjustment, we show that growth at low temperature mimics growth at high light. We conclude that terrestrial plants, green algae and cyanobacteria do not respond to changes in growth temperature or growth irradiance per se, but rather, respond to changes in the redox state of intersystem electron transport as reflected by changes in PSII excitation pressure, We suggest that this chloroplastic redox sensing mechanism may be an important component for sensing abiotic stresses in general. Thus, in addition to its role in energy transduction, the chloroplast may also be considered a primary sensor of environmental change through a redox sensing/signalling mechanism that acts synergistically with other signal transduction pathways to elicit the appropriate molecular and physiological responses.     

Acclimation of Arabidopsis thaliana to the light environment: Changes in composition of the photosynthetic apparatus

Acclimation to changes in the light environment was investigated in Arabidopsis thaliana (L.) Heynh. cv. Landsberg erecta. Plants grown under four light regimes showed differences in their development, morphology, photosynthetic performance and in the composition of the photosynthetic apparatus. Plants grown under high light showed higher maximum rates of oxygen evolution and lower levels of light-harvesting complexes than their low light-grown counterparts; plants transferred to low light showed rapid changes in maximum photosynthetic rate and chlorophyll-a/b ratio as they became acclimated to the new environment. In contrast, plants grown under lights of differing spectral quality showed significant differences in the ratio of photosystem II to photosystem I. These changes are consistent with a model in which photosynthetic metabolism provides signals which regulate the composition of the thylakoid membrane.Abbreviations Aac1 gene encoding actin - Chl chlorophyll - F far-red-enriched light (R:FR = 0.72) - FR far-red light - H high light (400 mol · m^–2 · s^–1) - L low light (100 ml · m^–2 · s^–1) - LHCII light-harvesting complex of PSII - Lhcb genes encoding the proteins of LHCII - R red light - Rbcs genes encoding the small subunit of Rubisco - Rubisco ribulose-1,5-bisphosphate carboxylase/oxygenase - W white light (R:FR = 1.40) This work was supported by Natural Environment Research Council Grant No. GR3/7571A. We would like to thank H. Smith (Botany Department, University of Leicester) and E. Murchie (University of Sheffield) for helpful discussions.     

Regulation of the photosynthetic apparatus under fluctuating growth light

Safe and efficient conversion of solar energy to metabolic energy by plants is based on tightly inter-regulated transfer of excitation energy, electrons and protons in the photosynthetic machinery according to the availability of light energy, as well as the needs and restrictions of metabolism itself. Plants have mechanisms to enhance the capture of energy when light is limited for growth and development. Also, when energy is in excess, the photosynthetic machinery slows down the electron transfer reactions in order to prevent the production of reactive oxygen species and the consequent damage of the photosynthetic machinery. In this opinion paper, we present a partially hypothetical scheme describing how the photosynthetic machinery controls the flow of energy and electrons in order to enable the maintenance of photosynthetic activity in nature under continual fluctuations in white light intensity. We discuss the roles of light-harvesting II protein phosphorylation, thermal dissipation of excess energy and the control of electron transfer by cytochrome b₆f, and the role of dynamically regulated turnover of photosystem II in the maintenance of the photosynthetic machinery. We present a new hypothesis suggesting that most of the regulation in the thylakoid membrane occurs in order to prevent oxidative damage of photosystem I.     

Partitioning controls on Amazon forest photosynthesis between environmental and biotic factors at hourly to interannual timescales

Gross ecosystem productivity (GEP) in tropical forests varies both with the environment and with biotic changes in photosynthetic infrastructure, but our understanding of the relative effects of these factors across timescales is limited. Here, we used a statistical model to partition the variability of seven years of eddy covariance‐derived GEP in a central Amazon evergreen forest into two main causes: variation in environmental drivers (solar radiation, diffuse light fraction, and vapor pressure deficit) that interact with model parameters that govern photosynthesis and biotic variation in canopy photosynthetic light‐use efficiency associated with changes in the parameters themselves. Our fitted model was able to explain most of the variability in GEP at hourly (R² = 0.77) to interannual (R² = 0.80) timescales. At hourly timescales, we found that 75% of observed GEP variability could be attributed to environmental variability. When aggregating GEP to the longer timescales (daily, monthly, and yearly), however, environmental variation explained progressively less GEP variability: At monthly timescales, it explained only 3%, much less than biotic variation in canopy photosynthetic light‐use efficiency, which accounted for 63%. These results challenge modeling approaches that assume GEP is primarily controlled by the environment at both short and long timescales. Our approach distinguishing biotic from environmental variability can help to resolve debates about environmental limitations to tropical forest photosynthesis. For example, we found that biotically regulated canopy photosynthetic light‐use efficiency (associated with leaf phenology) increased with sunlight during dry seasons (consistent with light but not water limitation of canopy development) but that realized GEP was nonetheless lower relative to its potential efficiency during dry than wet seasons (consistent with water limitation of photosynthesis in given assemblages of leaves). This work highlights the importance of accounting for differential regulation of GEP at different timescales and of identifying the underlying feedbacks and adaptive mechanisms.     

Acclimation of photosynthesis to light and canopy nitrogen distribution: an interpretation

BACKGROUND AND AIMS: Acclimation of photosynthesis to light and its connection with canopy nitrogen (N) distribution are considered. An interpretation of a proportionality between light-saturated photosynthesis and local averaged leaf irradiance is proposed by means of a simple model. MODEL: The model assumes (a) local irradiance drives synthesis of photosynthetic protein from metabolic N; (b) photosynthetic N is slowly degraded over approx. 5-7 d; (c) metabolic N is equally available through the canopy. CONCLUSIONS: The kinetics of acclimation at different light levels may provide a way of parameterizing and testing the model. The model provides a rationale for the proportionality assumption mentioned above, which, while it is consistent with much experimental work, is valuable because it allows canopy photosynthesis to be calculated analytically.     

Response of photosynthetic apparatus to moderate high temperature in contrasting wheat cultivars at different oxygen concentrations

The photosynthetic responses to moderately high temperatures (38 degrees C, imposed at 21% or 2% O(2) in air and 1500 mumol m(-2) s(-1)) were compared in wheat (Triticum aestivum L.) cultivars grown in northern regions of Ukraine and expected to be relatively sensitive to high temperatures ('North' cultivars) and in cultivars grown in southern regions and expected to be relatively heat-tolerant ('South' cultivars). Heating intact leaves in 21% O(2) for 1 h decreased CO(2) assimilation by c. 63% in 'North' cultivars and only c. 32% in 'South' cultivars, with a decrease in PSII activity being observed in only one of the 'North' cultivars. Carboxylation efficiency was decreased by about 2.7-fold in 'North' cultivars with no significant effect in 'South' cultivars. The maximum rates of carboxylation by Rubisco in vivo, V(cmax), estimated from Farquhar's model, increased more than 2-fold in 'South' cultivars and remained unchanged in 'North' cultivars while the maximum rate of RuBP regeneration, J(max), decreased by 53% and 21% in 'North' and 'South' cultivars, respectively. Where the heat treatment was imposed in 2% O(2) this increased (as compared with treatment at 21% O(2)) the inhibitory effect on CO(2) assimilation in tolerant cultivars, but decreased it in sensitive ones. The results suggested that differences in tolerance of moderately high temperatures in wheat relate to the stability of the Rubisco function and to RuBP regeneration activity rather than to the effects on PSII activity or stomatal control.     

Modifications to the photosynthetic apparatus of higher plants in response to changes in the light environment

A brief review of the photosynthetic apparatus of higher plants is given, followed by a consideration of the modifications induced in this apparatus by changes in light intensity and light quality. Possible strategies by which plants may optimize photosynthetic activity by both long- and short-term modifications of their photosynthetic apparatus in response to changing light regimes are discussed.     

植物光合机构对光环境的适应机制: 状态转换

在自然条件下,植物接受的照光量经常变化,而植物在进化过程中已形成了相应的适应机制,用以维持光环境变化过程中2个光反应之间光能转换的能量平衡.植物的调控系统不但能通过调控叶片和叶绿体的运动以及光合色素的积累调节光的吸收,还可以通过光系统的状态转换灵活地调节捕光色素蛋白复合体吸收的能量分配.特别是在低光强下,植物通过可对电子传递链的氧化还原状态做出响应的激酶和磷酸酶调控光系统Ⅱ捕光色素蛋白复合体(LHCⅡ)的可逆磷酸化,从而调节激发能在PSⅠ与PSⅡ之间的分配.植物的状态转换机制是植物适应光质等光环境变化的重要机制.本文综述了植物状态转换机制的研究进展,阐述了LHCⅡ的磷酸化及其在PSⅠ与PSⅡ两个光系统间的移动及其状态转换在植物适应光环境变化中的生理意义,并展望了今后的主要研究方向.     

Acclimation of the respiration/photosynthesis ratio to temperature: insights from a model

Based on short-term experiments, many plant growth models – including those used in global change research – assume that an increase in temperature stimulates plant respiration (R) more than photosynthesis (P), leading to an increase in the R/P ratio. Longer-term experiments, however, have demonstrated that R/P is relatively insensitive to growth temperature. We show that both types of temperature response may be reconciled within a simple substrate-based model of plant acclimation to temperature, in which respiration is effectively limited by the supply of carbohydrates fixed through photosynthesis. The short-term, positive temperature response of R/P reflects the transient dynamics of the nonstructural carbohydrate and protein pools; the insensitivity of R/P to temperature on longer time-scales reflects the steady-state behaviour of these pools. Thus the substrate approach may provide a basis for predicting plant respiration responses to temperature that is more robust than the current modelling paradigm based on the extrapolation of results from short-term experiments. The present model predicts that the acclimated R/P depends mainly on the internal allocation of carbohydrates to protein synthesis, a better understanding of which is therefore required to underpin the wider use of a constant R/P as an alternative modelling paradigm in global change research.     

Acclimation of Arabidopsis thaliana to the light environment: regulation of chloroplast composition

The regulation by light of the composition of the photosynthetic apparatus was investigated in Arabidopsis thaliana (L.) Heynh. cv. Landsberg erecta. When grown in high- and low-irradiance white light, wild-type plants and photomorphogenic mutants showed large differences in their maximum photosynthetic rate and chlorophyll a/b ratios; such changes were abolished by growth in red light. Photosystem I (PSI) and PSII levels were measured in wild-type plants grown under a range of light environments; the results indicate that regulation of photosystem stoichiometry involves the specific detection of blue light. Supplementing red growth lights with low levels of blue light led to large increases in PSII content, while further increases in blue irradiance had the opposite effect; this latter response was abolished by the hy4 mutation, which affects certain events controlled by a blue-light receptor. Mutants defective in the phytochrome photoreceptors retained regulation of photosystem stoichiometry. We discuss the results in terms of two separate responses controlled by blue-light receptors: a blue-high-fluence response which controls photosystem stoichiometry; and a blue-low-fluence response necessary for activation of such control. Variation in the irradiance of the red growth light revealed that the blue-high-fluence response is attenuated by red light; this may be evidence that photosystem stoichiometry is controlled not only by photoreceptors, but also by photosynthetic metabolism.Abbreviations BHF blue-high-fluence - BLF blue-low-fluence - Chl chlorophyll - FR far-red light - LHCII light-harvesting complex of PSII - P_max maximum photosynthetic rate - R red light - Rubisco ribulose-1,5-bisphosphate carboxylase/oxygenase This work was supported by Natural Environment Research Council Grant No. GR3/7571A. We would like to thank H. Smith (Botany Department, University of Leicester) and E. Murchie (INRA, Versailles) for helpful discussions.     

高温伤害光合机构原初位点的研究进展

本文介绍了高温伤害光合机构原初位点的研究进展,分析了不同观点产生的可能原因,为进一步研究高温对植物光合作用的影响提供思路。     

热带雨林三种树苗叶片光合机构对光强的适应

对生长在不同光强(自然日光的8％,25％,50％)下西双版纳热带雨林3种木本植物团花(Anthocephalus chinensis)、玉蕊(Barringtonia pendala)和藤黄(Garrcinia hanburyi)幼苗光合机构的研究表明,随着生长光强的升高,植物叶片的光饱和点、补偿点、净光合速率和非光化学淬灭系数(NPQ)升高,而表现量子效率(AQY)、有效光化学量子产量(Fv／Fm)、光化学淬灭系数(qP)下降．在抗氧化系统中,超氧化物歧化酶(SOD)、抗坏血酸过氧化酶(APX)活性随着光强的升高而升高,而过氢化物酶(CAT)活性与生长光强的变化不一致．抗坏血酸(AsA)含量随着光强的升高而急剧上升。最能反映PFD的变化．可以认为,除与叶黄素循环有关的热耗散增大之外,植物叶片抗氧化系统的加强也是响应强光的一种保护措施．     

Effects of environmental parameters on net photosynthesis of a free-living brown seaweed,Cystoseira barbata formarepens: determination of optimal photosynthetic culture conditions

The net photosynthesis of the Mediterranean brown seaweedCystoseira barbata f.repens is measured according to irradiance, temperature and salinity. There is not only, a good utilization of low light intensities (light-shade adaptation), but also a specific ability to use a broad range of irradiance, which corresponds in the photosynthesis-irradiance curves to a high initial slope and an extended light saturation level from 300 to 1500 mol photon m^–2 s^–1; only very high irradiances induce photoinhibition. Maximum net photosynthesis occurred at temperatures ranging from 20 °C to 30 °C. The alga tolerates not only a low level of salinity, but also a slight increase in salinity; however, at more than 47.5 g 1^–1 NaCl, oxygen exchange is significantly reduced.Light, temperature and salinity requirements are discussed, taking into account ecological considerations. Yields and quality of alginic acid are presented according to the irradiance and yearly evolutionin situ in order to aid future cultivation of this species.     

The photosynthetic apparatus of Rhodopseudomonas palustris: structures and organization

The structural analysis of the individual components of the photosynthetic apparatus of Rhodopseudomonas palustris, or those of related species, is almost complete. To shed light on the assembly and organization of this machinery, we have studied native membranes of Rps.palustris grown under different light conditions using atomic force microscopy (AFM). The organization of the complexes in the membranes is different from any previously observed: with areas of crystalline core-complexes, crystalline peripheral antennae, mixed domains, and apparently pure lipid membranes devoid of protein. Examination of antennae structure shows that chromatic adaptation is associated with modifications in absorption and size of the peripheral light harvesting complexes (LH2) as light intensity is reduced. The core-complex is observed to contain a reaction centre (RC) surrounded by an elliptical assembly of 15 LH1 subunits and a "gap" attributed to the W-subunit. The localization of the W-subunit is not restricted to the periapsis of the core-complex but randomly located with respect to the RC imposed axis.     

Redox signalling and the structural basis of regulation of photosynthesis by protein phosphorylation

In photosynthesis in chloroplasts and cyanobacteria, redox control of thylakoid protein phosphorylation regulates distribution of absorbed excitation energy between the two photosystems. When electron transfer through chloroplast photosystem II (PSII) proceeds at a rate higher than that through photosystem I (PSI), chemical reduction of a redox sensor activates a thylakoid protein kinase that catalyses phosphorylation of light-harvesting complex II (LHCII). Phosphorylation of LHCII increases its affinity for PSI and thus redistributes light-harvesting chlorophyll to PSI at the expense of PSII. This short-term redox signalling pathway acts by means of reversible, post-translational modification of pre-existing proteins. A long-term equalisation of the rates of light utilisation by PSI and PSII also occurs: by means of adjustment of the stoichiometry of PSI and PSII. It is likely that the same redox sensor controls both state transitions and photosystem stoichiometry. A specific mechanism for integration of these short- and long-term adaptations is proposed. Recent evidence shows that phosphorylation of LHCII causes a change in its 3-D structure, which implies that the mechanism of state transitions in chloroplasts involves control of recognition of PSI and PSII by LHCII. The distribution of LHCII between PSII and PSI is therefore determined by the higher relative affinity of phospho-LHCII for PSI, with lateral movement of the two forms of the LHCII being simply a result of their diffusion within the membrane plane. Phosphorylation-induced dissociation of LHCII trimers may induce lateral movement of monomeric phospho-LHCII, which binds preferentially to PSI. After dephosphorylation, monomeric, unphosphorylated LHCII may trimerize at the periphery of PSII.     

Quantification of excitation energy distribution between photosystems based on a mechanistic model of photosynthetic electron transport

Absorbed light energy is converted into excitation energy. The excitation energy is distributed to photosystems depending on the wavelength and drives photochemical reactions. A non‐destructive, mechanistic and quantitative method for estimating the fraction of the excitation energy distributed to photosystem II (f) was developed. For the f values for two simultaneously provided actinic lights (ALs) with different spectral distributions to be estimated, photochemical yields of the photosystems were measured under the ALs and were then fitted to an electron transport model assuming the balance between the electron transport rates through the photosystems. For the method to be tested using leaves with different properties in terms of the long‐term and short‐term acclimation (adjustment of photosystem stoichiometry and state transition, respectively), the f values for red and far‐red light (R and FR) were estimated in leaves grown (~1 week) under white light without and with supplemental FR and adapted (~10 min) to R without and with supplemental FR. The f values for R were clearly greater than those for FR and those of leaves grown with and adapted to supplemental FR tended to be higher than the controls. These results are consistent with previous studies and therefore support the validity of the proposed method.     

Acclimation of the photosynthetic apparatus to low light in a thermophilic Synechococcus sp. strain

Depending upon their growth responses to high and low irradiance, respectively, thermophilic Synechococcus sp. isolates from microbial mats associated with the effluent channels of Mushroom Spring, an alkaline siliceous hot spring in Yellowstone National Park, can be described as either high-light (HL) or low-light (LL) ecotypes. Strains isolated from the bottom of the photic zone grow more rapidly at low irradiance compared to strains isolated from the uppermost layer of the mat, which conversely grow better at high irradiance. The LL-ecotypes develop far-red absorbance and fluorescence emission features after growth in LL. These isolates have a unique gene cluster that encodes a putative cyanobacteriochrome denoted LcyA, a putative sensor histidine kinase; an allophycocyanin (FRL-AP; ApcD4-ApcB3) that absorbs far-red light; and a putative chlorophyll a-binding protein, denoted IsiX, which is homologous to IsiA. The emergence of FRL absorbance in LL-adapted cells of Synechococcus sp. strain A1463 was analyzed in cultures responding to differences in light intensity. The far-red absorbance phenotype arises from expression of a novel antenna complex containing the FRL-AP, ApcD4-ApcB3, which is produced when cells were grown at very low irradiance. Additionally, the two GAF domains of LcyA were shown to bind phycocyanobilin and a [4Fe-4S] cluster, respectively. These ligands potentially enable this photoreceptor to respond to a variety of environmental factors including irradiance, redox potential, and/or oxygen concentration. The products of the gene clusters specific to LL-ecotypes likely facilitate growth in low-light environments through a process called Low-Light Photoacclimation.

     

Acclimation to irradiance of leaf photosynthesis and associated nitrogen reallocation in photosynthetic apparatus in the year following thinning of a young stand of Chamaecyparis obtusa

In order to quantify the effects of thinning on photosynthetic parameters and associated change in leaf nitrogen (N) contents, half of the trees in a 10-year-old Chamaecyparis obtusa (Sieb. et Zucc.) Endl. stand (36° 3′N, 140°7′E) were removed, giving a final density of 1 500 trees ha⁻¹, in May 2004. Photosynthetic photon flux density (PPFD) and leaf N and carbon (C) contents in the lower (L), middle (M), and upper (U) crowns were monitored one, three, and five months after thinning in both the thinned stand and a non-thinned control stand. In addition, leaves’ photosynthetic responses to CO₂ concentration were simultaneously measured in situ to estimate the maximum rates of carboxylation (V_cmax) and electron transport (J_max). Thinning increased PPFD in the L and M crowns but not in the U crown. V_cmax in both the L and M crowns of the thinned stand increased significantly in comparison with the same crown position of the control stand in the three and five months following thinning. In addition, the thinned stand exhibited an increase in N partitioned to ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) in the L and M crowns relative to the control stand three and five months after thinning, indicating that N had been redistributed within the photosynthetic machinery. Thinning did not affect N per unit area at any of the crown positions, but significantly increased the content of N as a fraction of the total leaf dry mass in the L and M crowns three and five months after thinning. This was a consequence of a decrease in leaf dry mass due to rapid shoot growth. Thus thinning did not cause a redistribution of N between leaves. Thinning improved irradiance in the L and M crowns of C. obtusa, leading to photosynthetic acclimation. Photosynthetic acclimation in the first year mainly occurred via redistribution of N within but not between leaves.     

Rapid light curves: A new fluorescence method to assess the state of the photosynthetic apparatus

Photosynthetic electron transport rates (ETR), calculated from chlorophyll fluorescence parameters, were compared in long term light and dark adapted as well as photoinhibited Pisum sativum leaves using a novel chlorophyll fluorescence method and a new instrument: rapid light curves (RLC) generated with the MINI-PAM. RLCs are plots of ETRs versus actinic irradiances applied for 10 s. Large changes in maximum electron transport rates (ETR_max) were observed when leaves were shifted from dark to moderate light, or from dark to photoinhibitory light and vice versa. Maximum ETRs were very low following long term dark adaptation, but increased to maximum levels within 8 to 15 minutes of illumination. It took more than 3 hours, however, to return irradiance-exposed leaves to the fully dark adapted state. Quenching analysis of RLCs revealed large q_E development in long-term dark adapted leaves accounting for the low ETRs. Leaves photoinhibited for 3 hours had similarly reduced ETRs. In these leaves, however, q_I was largely responsible for this reduction. Actinic irradiance exposures and saturating flashes affected leaves with different irradiance histories differently.