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ABSTRACT
Study on the temperature effect on plant photosynthesis is essential for proper understanding of physiology of plants as well as designing of crops that are able to cope-up with temperatures greater as well as lower than optimum growth temperatures. Any fluctuation in temperatures from the optimum temperature affects the overall growth and productivity of plants. Any temperature fluctuation from permissible values have known to affect the PSII, OEC, PQ, PSI, Cytochrome b559 as well as he primary enzyme of dark reaction Rubisco and Rubisco activase. Production of ROS, HSP generation and production of secondary metabolites are the results of temperature stress in plants. In this review I aim to discuss the physiological, biochemical and molecular changes in the photosynthetic apparatus during temperature stress as well as the protective mechanism devised by plants against it.
INTRODUCTION
Any adverse environmental factor affecting the normal growth and yield and productivity of the plant is known as stress. Several abiotic stress factors like temperature, drought, light intensity, salinity and heavy metal accumulation, tend to reduce the plant productivity and growth by reducing the photosynthetic rate and accumulation of ROS.
Among the abiotic factors, temperature stress plays an important part in the functioning of photosynthetic machinery. Temperatures above and below the optimum levels are known to cause heat and cold stress in plants. In nature, there no particular ideal temperature that prevails throughout the life cycle of plants. There are fluctuations in temperature throughout the growth period of plants. Since plants are sessile and unlike other mobile living organisms they have to endure as well as devise certain adoptive measures that helps them to adopt to the situation. The plant productivity is affected in a number of ways by high temperature stress. Several physiological, biochemical, and molecular processes contribute towards the plant growth with photosynthesis being the central pathway contributing towards crop yield and productivity. High temperature stress primarily inhibits the plant photosynthesis before impairing any other cell functions. Low temperature and freezing stress also limits the plant productivity of the plants belonging to majorly tropical and sub-tropical regions where the plants are generally adapted to grow in relatively higher temperatures
In order to to adapt to the temperature fluctuations, there is increased synthesis of antioxidants for the mitigation of ROS produced during the stress. Along with the production of antioxidants there is also increased synthesis of HSP, modifications in the photosynthetic antennae complex and electron transfer rates.
HIGH TEMPERATURE STRESS
Temperatures more than 35 degrees are known to cause inhibitory effects on plant photosynthesic chemical reactions as well as affects the structural organisation. High temperature stress leads to the overproduction and accumulation of reactive oxygen species (ROS) that in turn leads to lipid peroxidation and accumulation of malondialdehyde (MDA). Along with it, there is also reduction or inhibition of photosynthesis, protein denaturation, and accumulation of compatible solutes. some of the effects of high temperature stress on plants are summarised below.
Effect on High temperature stress on the photosynthetic pigments
Plant chloroplast pigments play an important role in capturing the light energy as well as electron excitation leading to the photochemical reactions and photolysis of water that mainly drives photosynthesis. Pigments constitute an important constituent in the LHC complexes as well as RC of the photosystems. High temperature stress induced plants have known to show a reduction in the chlorophyll biosynthesis. Decrease in chlorophyll biosynthesis due to high temperature stress is the result of the inactivation of chlorophyll biosynthesic enzymes like ALAD under high temperature stress. 5-aminolevulinate dehydratase (ALAD) is the first enzyme involved in pyrrole synthesis. Also, in response to high temperature there is decrease in 18% of total chlorophyll content, 7% decrease in chlorophyll a content, 3% decrease in chlorophyll a/b ratio, 9% decrease in sucrose content, along with an increase in 47% and 36% of soluble sugar content and leaf soluble sugar content respectively in soyabean. The decrease in the amount in chlorophyll pigments was due to the increased production of ROS, thereby indirectly representing the heat stress level in plants. while there was an increased action of Carotenoids along with APX and CAT that function as major antioxidants for the scavenging of H2O2 produced during the heat stress. Carotenoids not only acts as an accessory light-harvesting pigment but also helps in protecting the photosynthetic systems as nonenzymatic mediated antioxidant against reactive oxygen species generated during heat or high temperature stress.
Effect of High temperature stress on PSII structure and function
Higher temperature affects the thylakoid membrane fluidity changing its physiochemical properties and functional organisation. Among the two photosystems, PSII is most sensitive to high temperature stress. Depending on the type of photoautotrophic plant cell (cyanobacteria, monocot, dicot), the sensitivity of PSII varies. Variations among acclimation of PSII to high temperature stress also varies among organisms. PSII reaction centre and light harvesting complexes are primarily damaged by high temperature or heat stress. The organisation and composition of PSII subunits and cofactors are equal in higher plants and cyanobacteria. Photosystems constitute both LHC and Core complex proteins. The intrinsic light-harvesting proteins of PSII are LHCII, LHCb4 (CP29), LHCb5 (CP26), and LHCb6 (CP24). The core complex has four intrinsic subunits namely, D1(PsbA), D2 (PsbD), CP43 (PsbC) and CP47 (PsbB). Among these, D1 and D2 constitute the Reaction Centre of PSII contributing towards charge separation and photochemical electron transfer while the rest two contribute in the transfer of light energy from peripheral antenna molecules to the Reaction Centre. The Reaction Centre is also surrounded by 12 low molecular mass subunits namely PsbE, PsbF, PsbH, PsbI, PsbJ, PsbK, PsbL, Psb M, PsbTc, PsbW, PsbX, and PsbZ. These subunits help in dimerization and stabilization of the core complex, association of the core complex with the peripheral antenna complex and binding of cytochrome b-559 in order to protect PSII complex from the photo-damage. PsbO, PsbP, PsbQ. PsbR, PsbU and PsbV are the associated extrinsic proteins of the PSII. High temperature stress results in the loss of cofactors as well as the dissociation of PsbO, PsbQ and PsbP subunits. Likewise, there is also damage to the D1 protein leading to photoinhibition and production of ROS during high temperature stress. It is well known that high temperature stress increases membrane fluidity of plastids as well as cause granal de-stacking. High temperature stress also affects the phosphorylation of proteins. One such example being the phosphorylation of D1 protein in PSII that is cleaved by FtsH activity. FtsH is initially located in the stromal region of thylakoid and after high temperature stress degrades the D1 protein. Migration of phosphorylated LHCII from PSII towards PSI is reported in plants under elevated temperatures. Heat stress also affects the electron transfer from QA to QB as a result of the damage to the intrinsic proteins D1 and D2. These processes may further contribute to decreased Quantum efficiency of PSII.
Effect of High temperature stress on Oxygen Evolving Complex
The OEC contains three protein subunits, PsbO, PsbP and PsbQ mainly. PsbO is present in every oxygen evolving organism and involved in the stabilization of the Mn complex of OEC. while PsbP and PsbQ are involved in optimizing the oxygen evolution at physical concentration of calcium and chloride ions. Manganese and Calcium binds to the core of the OEC, with the empirical formula for the inorganic core of Mn4Ca1OxCl12(HCO3)y. This cluster is coordinated by D1 and CP43 subunits. The peripheral membrane proteins help in the stabilization of the cluster as well. At temperatures around 47°C, there is the release of 18 kDa protein that is associated with the loss of Ca ion from the Mn4Ca complex.
Cytochrome b559 (Cytb559) is an iron containing compound linked to PSII whose c terminus had a 33KDa protein that stabilizes Mn atoms. During Heat stress, the 33 KDa Mn-stabilizing protein dissociates from the reaction centre of PSII followed by the release of Mn atoms that might cause the thermal inactivation of OEC. Cytb559 is present in two forms, a dominant high potential form and other low potential form. Studies have shown that, mild temperature stress causes rapid interconversion of HP to LP form. Under high temperature stress, there is complete absence of HP form of cytb559. Heat stress may cause CEF around PSII involving the cytb559. Photosynthetic action is halted when the OEC gets damaged due to heat. Under such conditions the electron is donated from PSII acceptor side through the CEF to P680+ or Yz ox. This way the normal photochemical activity can be carried on without any halt. Two redox active tyrosines, YD and YZ, with different functions are present in PSII. These tyrosine residues Yz and Yd are found in D1 and D2 polypeptide in 161 and 160 positions of PSII respectively. Yd tyrosine is involved in the OEC assembly and is oxidised via p680+. According to some authors, the Redox state of Yd can be used to determine the damage amount caused in the PS due to high temperature stress since the electron donation from YD to P+680 increases under high temperature stress.
Chlorophyll a fluorescence of PSII indicates the heat stress amount experienced by a plant. Plants grown under normal growth temperatures 25°C displayed OJIP fluorescence transient curves. While in plants under heat stress, there was an additional k step (OKJIP fluorescence transient). The K step only occurs due to the high temperature stress and indicated that the OEC is damaged completely and at 45 °C. During a strong heat stress, the OEC is blocked and its efficiency decreases. This marks an additional step K-step in the fluorescence transient (now OKJIP). We can conclude from this that the high temperature stress induces the K step since the OEC is unable to donate electron efficiently to the RC of PSII. It is also known that the K step arises due to the imbalance in the electron acceptor and donor sides. There is increase in electron pressure on the acceptor side of the PSII but the donor side is not able to cope up with this flow. This irregularity leads to the oxidation of RC. There is also evidence that the K step also arises due to the inhibition of electron transport from Phaeophytin PQ. From the fluorescence analysis there is decrease in the antenna size, Fm value and Fv/Fm ratio. While the value of Fo increased. These are the common fluorescence values seen in the stressed plants. There is also increase in energy dissipation in the form of heat when plants were exposed above 35°C temperature. This form of non-photochemical chlorophyll a fluorescence quenching led to decreased photochemical efficiency since there was less energy available for photochemistry. Plastohydroquinol (PQH2) oxidation site in the cytb6/f complex is also reported to be inhibited during heat stress.
Effect High Temperature stress on the PQ pool
In oxygenic photosynthesis, both PSI and PSII function in tandem. The electron flow through electron transport chain (ETC) following the path from PSII ’ PQ ’ b6f ’ Pc ’ PSI and finally to NADP+, the terminal electron acceptor of PSI. Similar form of electron transport is seen in higher as well as lower plants. Phycobilisomes (PBS) are the mobile antenna found in synechococcus. Because of its mobile character, it is not bound tightly to RC of Photosystems. During the state transitions, the association or dissociation of PBS with the two photosystems depend on the Redox poise of PQ. Oxidised PQ pool is known to induce PBS to associate with PSII (State1) in order to increase the rate of electron flow. While the reduced pool of PQ induces the PBS to associate with PS1(state2), initiating the withdrawal of electrons from ETS. In the dark condition also, the PBS is associated with PSI since there is reduction of PQ pool due to the operation of respiratory electron flow. Along with the state-transitions, PQ also takes part in the biosynthesis of chlorophyll, LHC accumulation, protein synthesis rate of photosystems and the balance in the photosystem stoichiometry. During high temperature stress the PQ pool is in more reduced form Over reduction of PQ pool causes double reduction of QA to QA2 in the PSII reaction centre, triplet 3P680 and ion-radical pair [_680 + Pheo] formation. Longer Excited states of chlorophyll can damage the photosystem proteins by the formation of ROS. Reduced PQ are known to counteract ROS by scavenging them around PSII through the oxidation of plastoquinol. Similar mechanism is also observed around PSI in which superoxide anion radical is scavenged through oxidation of plastoquinol. Scavenging of ROS through plastoquinol oxidation around both PS can help in faster replenishment of PQ molecules. It is also well known that the reduced PQ pool triggers the CEF around PSI for efficient photosynthesis.
Effect on High temperature stress on the Biological membrane dynamics and functions
Higher temperatures affect the fluidity and permeability of membranes, through changes in the lipid composition and interactions between lipids and specific membrane proteins. Higher temperatures also tend to decrease the hydrophilic interactions between LHC with PSII along with increase in the hydrophilic interactions leading to the increased affinity of pigment-protein complexes towards lipids, leading to their dissociation. There is also increase in the content of saturated and monounsaturated fatty acid during increase in temperatures. Increased ROS production during high temperature stress is known to cause oxidative stress to plants with inhibition of protein synthesis, oxidation of saturated fatty acids and decrease in fatty acid saturation in thylakoid membranes, destabilizing the PSII structure. High temperature stress is also known to cause structural changes in the thylakoid membrane stacking. Temperatures ranging from 35°C-45°C caused unstacking of thylakoid grana membranes. Bleaching experiments demonstrated the disruption of chlorophyll-protein complexes of PS due to temperature induced destacking of thylakoid membranes.
High temperature stress induced changes in the PSII heterogeneity
The heterogeneity of PSII is due to its diverse structure as well as function. The heterogeneity is mainly due to its differences in antenna size as well as the reducing side. Three types of antenna namely, PS II alpha, PS II beta and PS II gamma are present depending on the size of the antenna. QB-reducing and QB-non-reducing centers are proposed due to acceptor/reducing side function. Grana stacking and unstacking is another form of structural heterogeneity found in PSII. This form of heterogeneity depends on the distribution of PSII in grana and stroma lamellar regions of thylakoid membrane. During high temperature stress, alpha centres of PSII declined while there was an increase in the other antenna types. This change in the antenna types during the shift from 25°C to 45°C could be due to the interconversion of alpha to beta and gamma types during onset of high temperature stress. There are also reports in the decrease in the connectivity between antenna molecules at around 40°C. while a rise in 5°C caused complete ungrouping of the antenna molecules in wheat. During the fluorescence kinetics measurements, the heat-treated leaves of apple showed positive L step depicting the ungrouped nature of PSII units. Lowering in the cooperativity during the heat stress indicates the lower stability of PSII units. There was a marked effect of high temperature stress (45°C) on QB non reducing centres. Upon treatment with higher temperatures (45°C) there was an increase in the proportion of QB non reducing centres with respect to growth temperatures. This increase can be related to the inactivation of active QB reducing centres due to heat stress.
Effect of High temperature stress on PSI function.
Unlike PSII, PSI is more resistive to the heat stress in dark. 2.8 Å resolution structure of plant PSI reveals 12 core subunits and 4 LHC proteins (LHCa1, LHCa2, LHCa3, and LHCa4). The prosthetic groups of the complex including the number of chlorophyll molecules, carotenoids and lipids varies from cyanobacteria to higher plants. There is presence of 12 protein subunits, 96 chlorophyll a molecules, 22 carotenoids, three [4Fe4S] clusters and 2 Phylloquinones in the PSI structure of cyanobacteria Synechococcus elongatus. PSI structure of thermophilic cyanobacteria, Thermosynechococcus elongatus is a trimer while the structure of PSI in plants at 4.4 ÚA resolution, is a monomeric unit having 16 protein subunits, 167 Chl, 2 phylloquinones, and 3 Fe4S4 Clusters.
For a proper and efficient way of electron transfer during photosynthesis, the two PS must work in a coordinated way. Electrons can be transferred either through linear electron flow (non-cyclic way LEF) or through cyclic electron flow (CEF). LEF includes PSII, cytochrome b6f and PSI. CEF can occur through PGR5PGRL1 pathway or through NAD(P)H dehydrogenase (NDH) pathway. There are evidences that, moderate increase in temperature activates PSI activity along with increase in CEF of PSI and thylakoid proton conductance. Similar evidences of increased PSI mediated CEF under high temperature stress is reported from plants like pea, tobacco, Arabidopsis, Symbiodinium and grapes. NDH complex lacking transformants of tobacco that were unable to balance the NADPH/ATP ratio during high temperature stress, generated greater amounts of ROS generation. Non photochemical or dark reduction of PQ is reported to be increased during the heat stress. Studies have also shown that during the mild temperature stress, the ATP demand for plant increases due to photorespiration as well as Rubisco activase. Increase in the efficiency of P700+ could be due to high temperature induced structural modifications of PSI, increasing the PSI absorption cross-section.
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