Manipulation of Photoprotection to Improve Plant Photosynthesis
Year: 2010
Type: review
Abstract: Light is of course essential for photosynthesis and supports most life on earth. However, light intensity and spectral quality are highly variable in space and time according to time of day, season, geography, climate, and the position of leaf within canopy and cell within leaf. This has resulted in the evolution of a remarkable suite of processes within the photosynthetic system to accommodate these fluctuations. In fact, these regulatory mechanisms are tightly integrated with photosynthesis itself, and there is emerging evidence that when these processes are altered, the ability of plants to assimilate carbon over long time periods and to produce biomass may be affected. Photosynthesis begins with the absorption of light by chlorophyll, much of which is located in the light-harvesting complexes (LHCs) of PSII and PSI within the thylakoid membrane of chloroplasts. Chlorophyll enters its singlet excited state, and excitation energy is transferred to PSII and PSI reaction centers where charge separation occurs and photosynthetic electron transport is initiated. Electrons derived from water splitting ultimately reduce NADP+ to NADPH, and the transmembrane ƊpH is used to drive ATP generation by the chloroplastic ATP synthase. NADPH and ATP are then used in the Calvin-Benson cycle and other assimilatory reactions. In addition to this linear electron flow, there is flexibility in the electron transport system with multiple pathways and electron acceptors possible. These include cyclic electron transfer and oxygen as an electron acceptor. Absorbed solar energy may be defined as excessive when it exceeds the capacity of photosynthesis to use it for assimilation. Although excess light is potentially harmful, plants have a plethora of mechanisms that manage the excess absorbed energy on a molecular level in a way that does not result in photooxidative stress. Photoprotection is a rather broad term that can be used to cover mechanisms that prevent light energy from inducing damage via the generation of high levels of reactive oxygen species (ROS). Although ROS are important signaling molecules in plants, they can have deleterious effects on photosynthesis and other leaf processes that ultimately will reduce growth and plant fitness. The most extreme example of this is photobleaching and cell death. Much of our current knowledge about photoprotection comes from studies of mutants and transformants of Arabidopsis (Arabidopsis thaliana) and other plants in which the level of expression of key genes has been altered with subsequent changes to protein level, resulting in changes to the capacity and the kinetics of some photoprotective processes. This work has resulted in advances in understanding the mechanisms and the physiology of these processes. An exciting possibility is that manipulating photoprotective pathways is a means to enhance both stress resistance and photosynthetic productivity of crop plants. However, there may be a balance between the need for photoprotection to limit damage on the one hand and enhancing productivity on the other (Murchie et al., 2009). There seems to be much yet to learn: Here, we review the current state of photoprotection research focusing on mechanisms that are potential targets for manipulation to improve photosynthesis. The response of leaf photosynthesis to light is best demonstrated with a light response curve (Fig. 1). As light (photon flux density) increases, the rate of photosynthesis rises until it is saturated (A max). The slope of the initial linear portion of this curve is the maximum quantum yield (efficiency) of photosynthetic CO2 uptake (ΦCO2) or oxygen evolution (ΦO2). The maximum quantum yield of PSII can be estimated by the ratio of variable chlorophyll fluorescence to maximal fluorescence (F v/F m). A, A concept diagram describing the principle of photoprotection by distinguishing absorbed light used in photosynthesis from excess light that results in excitation energy that needs to be removed. B, A concept diagram describing the effect of photoinhibition on the quantum yield and light-saturated photosynthetic rate (A max). Note that although a reduction in A max is often cited as a product of PSII photoinhibition, in fact it may be caused by processes associated with photoinhibitory conditions other than PSII function, e.g. stomatal closure or Rubisco inactivation at high temperature. Hence, it is drawn as a dotted line. Plants are subject to a huge variety of factors that limit growth and photosynthetic rate. These can be imposed by the environment, such as water and nutrient deficiency and temperature, or they may be intrinsically enforced by low sink strength or a genetically determined growth rate. As a direct result, light may be frequently in excess of that required for CO2 assimilation, thereby necessitating photoprotective responses to avoid severe photoinhibition. As described in detail below, photoprotection includes mechanisms that regulate absorption and dissipation of light energy. Plants have a limited ability to regulate the amount of sunlight they absorb through changes in leaf area, leaf angle, chloroplast movement, and, on a molecular level, through acclimatory adjustments in LHC antenna size. Once excess light has been absorbed, it can be dissipated via several routes, including thermal dissipation of excess excitation energy. A number of other reactions within the chloroplast can act as photochemical sinks for excess electrons. In addition, plants have efficient antioxidant systems for the removal of ROS (see Foyer and Shigeoka, 2011; this issue). Photoinhibition is a term that is often used to refer to a light-induced decrease in ΦCO2 and/or A max. However, some flexible photoprotective processes will also unavoidably reduce ΦCO2 and F v/F m, resulting in symptoms of moderate photoinhibition (Fig. 1B) that are usually transient. More severe photoinhibition causes a sustained reduction in ΦCO2, F v/F m, and even A max (Fig. 1B) that requires repair of photooxidative damage, in contrast with flexible photoprotective responses that have a duration of a few minutes. It should be emphasized that changes in A max are usually associated with more severe photoinhibition and multiple stresses, so it can be difficult to link reductions in A max with photoinhibition directly. Because photoprotection and photoinhibition processes can give similar symptoms, it can be difficult to distinguish them. Even some cases of severe environmental stress and long-term photoinhibition have been attributed to sustained photoprotective responses, for example, in overwintering evergreen leaves that cannot photosynthesize at extremely low temperatures (Demmig-Adams and Adams, 2006). Many plants position their leaves to optimize light absorption: this can occur by movement or positioning during development and growth. In high light, leaves of some species turn or develop so that they reduce the angle of incidence and increase reflection, thereby reducing the amount of light absorbed (Raven, 1994) and reducing leaf temperature (Pastenes et al., 2004). This is known to be an important attribute of crop physiology. In the case of tropical rice (Oryza sativa), upright leaves are common, and they do not affect the saturation of photosynthesis but do reduce the amount of light absorbed around the hours of mid-day, substantially reducing photoinhibition (Murchie et al., 1999). Upright cereal leaves theoretically give a higher rate of canopy photosynthesis. Leaf angle in crop plants specifically in relation to photoprotection is an area deserving more attention. Chloroplasts in low light typically position themselves where they can maximize light interception, toward the periclinal walls perpendicular to the incident light. In high light, they move toward the anticlinal walls where absorption is reduced (Kasahara et al., 2002) to decrease the amount of excess excitation energy and presumably to minimize the saturation of photosynthesis. This process can occur on a timescale of minutes to hours, and the velocity of movement depends on light fluence rate. The exact mechanism is still unknown, although it involves the blue light photoreceptor phototropin and movement along actin filaments (Suetsugu and Wada, 2007). Recent progress has been made in identifying the genes that confer movement away and toward light sources. The physiological advantage of such subcellular movements is clear; after all, photosynthesis takes place on the level of the single chloroplast, and such microscale movements could match microvariation in light intensity. There may be mileage in optimizing chloroplast movement in leaves for both light harvesting and photoprotection; however, more quantification is required regarding the energetic cost/benefit of movement. The impact on gas exchange in the leaf also needs to be taken into account because there is evidence that the anticlinal movement impairs CO2 diffusion (Tholen et al., 2008). The amount and proportion of photosynthetic components are typically altered on a timescale of days to match the prevailing light intensity in a process that is termed photoacclimation. This involves changes in amounts of soluble enzymes of photosynthesis, electron transport components, and pigment-protein complexes and has a number of effects, one of which is to match the amount of available light with the plant’s capacity to absorb it and use it for carbohydrate synthesis. For example, if a shift to high light intensity occurs, the capacity for CO2 assimilation and electron transport rises, but there is a net degradation of LHCs. This represents an economy of resources, but it also results in an increase in the capacity for photosynthesis that maintains the in situ rate at a point that is below A max, thus reducing the level of photoprotection required and the risk of photooxidative stress. There is evidence that some crop plants may be impaired in some aspects of photoacclimation, and this area is in need of further work to identify factors that might be altered to improve photosynthesis (Murchie et al., 2009). Adjustment of antenna size is reviewed elsewhere in this special issue (Ort et al., 2011; this issue). Photoacclimation may have an impact on growth and development. Plants that were compromised in their ability to acclimate dynamically to growth light intensity by altering the protein and pigment composition of their photosynthetic apparatus were grown in controlled environment and natural conditions. The wild-type plants (able to acclimate) had a higher fitness than the mutants, indicating that the dynamic responses of photosynthesis are indeed important in determining yield (Athanasiou et al., 2010) After light has been absorbed, the first site of photoprotection is within the LHCs themselves. If light is excessive and excited chlorophyll is unable to drive photochemistry, then the lifetime of the singlet state is extended, resulting in a higher yield of triplet state formation. This is undesirable because energy transfer from triplet chlorophyll to oxygen generates singlet oxygen, a highly reactive type of ROS. However, there is more than one route for deexcitation of singlet chlorophyll: in addition to driving photochemistry, a singlet state chlorophyll molecule energy can return to the ground state by the emission of light (chlorophyll fluorescence) or by the harmless emission of heat (thermal dissipation). The latter route is a major component of photoprotection, termed nonphotochemical quenching (NPQ; Müller et al., 2001; Horton et al., 2008). A number of processes contribute to the induction and relaxation of NPQ over time. One component, termed qE, is turned on and off rapidly (seconds to minutes) and depends on the formation of the ƊpH across the thylakoid membrane (Fig. 2). A second component, recently named qZ (Nilkens et al., 2010), is induced and reversed on a slower timescale of tens of minutes, correlated with the synthesis and disappearance of zeaxanthin. Another component, termed qI, is slower to relax (hours or longer) and has similarities (e.g. lowered F v/F m) with more severe types of photoinhibition, and it may also be associated with accumulation of zeaxanthin. A highly schematic figure summarizing the thylakoid processes involved in photoprotection. CP24, CP26, and CP29 refer to the minor LHC. OEC, Oxygen-evolving complex; PC, plastocyanin; vio, violaxanthin; zea, zeaxanthin. The 4H+ and 8H+ refer to linear electron flow only. In higher plants, there are two well-characterized molecules that regulate qE. First, it has long been known that the development of qE is associated with the accumulation of the xanthophyll cycle (XC) carotenoid zeaxanthin (Demmig-Adams, 1990). The XC is a reversible interconversion of zeaxanthin and violaxanthin that is directly linked to the energization of the thylakoid membrane during the induction of photosynthesis in the light. As light saturation is reached, the rise in ƊpH increases the proton concentration within the thylakoid lumen. This has a number of effects, including the activation of the enzyme violaxanthin deepoxidase, which converts violaxanthin to zeaxanthin and increases the deepoxidation state of the XC pool. The reverse reaction, converting zeaxanthin to violaxanthin, is catalyzed by zeaxanthin epoxidase. Although there is no doubt that zeaxanthin plays a key role in qE, there is still discussion over whether zeaxanthin is a direct quencher of singlet excited chlorophyll or an allosteric effector that alters the sensitivity of qE to the ƊpH: evidence exists for both mechanisms. The second component is the PSII protein PsbS, whose role in qE was discovered by screening mutant populations of Arabidopsis for altered chlorophyll fluorescence quenching (Li et al., 2000). Mutants lacking PsbS are specifically defective in qE, are more sensitive to photoinhibition (Li et al., 2002), and show decreased fitness (measured as seed yield) under fluctuating light conditions in the field or in the laboratory (Külheim et al., 2002; and Although PsbS is a of the LHC protein it does not to and as a of that is for the induction and relaxation of qE (Li et al., 2004). NPQ with similar to qE can be induced on a much slower timescale in the of PsbS and A LHC was recently to be for qE in the et al., 2009). This protein is not in higher plants, but both the and qE systems are in the where the two types of qE to and et al., qE capacity might improve photoprotection and crop in 2000). The PsbS protein has been to act in a in the more PsbS the higher the capacity for qE (Li et al., Hence, of PsbS be one to enhance photoprotection. grown in a light with a single of high light, Arabidopsis plants that PsbS et al., 2008). Although higher carbon at the level is the most it is that an shift to signaling could be involved et al., 2009). An way to increase qE capacity in crop plants be to the which was presumably after the of and higher plants. Because NPQ ΦCO2, the kinetics of NPQ components means that there will be when the relaxation of NPQ does not match the of light intensity changes in conditions that result in plant rapidly qE is usually the major component of but there are when qZ and more In the it is also important to that plant in plant are systems Arabidopsis The absorption of light can often be described where leaves as in However, the of direct in canopy space over time is more difficult to can a carbon for the but they can also the more sustained components of A et al., to the and of NPQ during and after formation by that there is a in the of ΦCO2 that impairs carbon assimilation during the low light a solar movement, the to canopy carbon was estimated to be between and on prevailing temperature. the of NPQ could enhance canopy photosynthesis It seems to the kinetics of NPQ by altering the An increase in the XC size was by the expression of et al., However, these plants had slower of formation and relaxation of to in the in deepoxidation state resulting from of XC et al., 2007). Another possibility is manipulation of the of the XC enzymes themselves. A violaxanthin mutant of Arabidopsis does not zeaxanthin in high light and has an impaired ability to NPQ et al., the other mutants that zeaxanthin zeaxanthin these plants still ƊpH to however, their response during photosynthetic induction is more as the kinetics of formation of zeaxanthin and violaxanthin, altering XC seems via of the of the enzymes of violaxanthin was to increase the initial rate not the of both zeaxanthin synthesis and NPQ induction in et al., the rate of of zeaxanthin to violaxanthin is one route to the relaxation of qZ and This might be by zeaxanthin however, it be to minimize with violaxanthin to avoid a of NPQ It has long been known that the which is of the within the reaction of is by light and 2006). This inactivation of PSII is to be caused by and is by a repair cycle that includes of the PSII degradation of and repair of by and This type of damage results in an and sustained of the quantum yield of PSII and has similar to the type of It seems that the rate of repair can limit the from this type of photoinhibition and that the maximum rate depends on environmental conditions and on the species under in or such as low or high repair is to contribute to sensitivity in some species but not in such as and could from the rate of However, an understanding and of the involved are and 2006). are involved in both the and degradation of et al., 2002; et al., 2009). Recent evidence that a of is also involved in degradation of et al., The protein in that is involved in repair synthesis of is to and and is thus a for In efficient sink for by water splitting in PSII a photochemical has the potential to decrease the reduction state of PSII and the risk of photooxidative stress. It is to include the mechanism of CO2 assimilation In with evergreen species with low photosynthetic to have a higher capacity for NPQ when grown in high light (Demmig-Adams and Adams, 2006). Many processes photosynthetic electron transport have been to act in such a photoprotective including cyclic electron and the reaction electron flow to electron flow around PSI that results in ATP synthesis and does not a electron (see also and this issue). Electrons are from or to the ƊpH (Fig. 2). The role of cyclic electron transport is First, it is of the ratio in the chloroplast to the of the Calvin-Benson it has a photoprotective qE via ƊpH electron flow may increase when linear electron flow is or during such as a light to high light. pathways are known to the and the route 2007). plants both but the is to be the Recent evidence toward cyclic electron flow a more role in the of plant photosynthesis than The of the two pathways and the complexes involved are still but current knowledge has in the few was as a mutant in Arabidopsis and was to be more to photoinhibition, although it growth at low light et al., is a thylakoid protein and when a effect on the rate of cyclic electron transport in but during from low to high light and not at state et al., 2007). is still Mutants the protein have a similar to that of et al., and have been where the two act as for cyclic electron flow by with and the to the of electron transport such as it to the photoprotective of plants via the amount of linear cyclic electron However, more on the role of cyclic in a of physiological and its impact on growth and it is which components need to be The cycle occurs by the of one molecule of to two molecules of water at the reducing of PSI via from two molecules of water in The reaction involves and of this reaction are elsewhere and Foyer and Shigeoka, The is the of and to prevent reactions in the However, it also PSII excitation energy and in of the cycle have that it is during such as and the from to light, CO2 induction occurs, and when the electron transport has the potential to highly In these the of PSI in a state cyclic electron transport and qE The ratio of activation of the Calvin-Benson It has similarities in with cyclic electron There may be for enhancing the of this cycle during conditions. The photoprotective processes described in and fitness in plants. do this via two the of photosynthetic and the of photooxidative is in processes such as one of which is to prevent of the electron transport over periods and light However, this is also a example of a photoprotective process that light conditions and can prevent processes that have not yet the natural that exists for photoprotective processes in it is to whether a process that is and that has a in of carbon is for carbon The issue of the and of photoprotection to plants and plant has been and it is that in some cases it has been to be a major (e.g. In a example the it was that the of high light movements by leaves during were low to the repair of if the leaf not move and photoinhibition a advantage in a Many species have low growth because they are to where is imposed by and other and of stress factors is and so evolution will for and that are not associated with potential of growth and carbon One is because these high are might be high and life The of is It can be that some to often do not a high yield potential in and et al., 2006). An is that the ability to optimize photosynthesis in as plants have to may not be for which often on high of water and that result in of carbon assimilation and growth. It seems to whether photosynthesis in our plants is This is a difficult to because needs to be made conditions that are and and an with which to the impact of components and processes. work has been on plants grown under conditions or in field conditions where environmental is It is important to the of the light environment, and as demonstrated by et that most of the evidence is for the level but not the level, and progress in this area has yet to be it is that we can genetically and enhance a plant’s capacity for photoprotection. This may have effects for in but it be the evidence that such processes have a that could limit carbon in conditions. The should from a of in conditions and that from the molecular level to the
Source: PLANT PHYSIOLOGY
Authors: Erik H. Murchie, Krishna K. Niyogi
Institutions: University of Nottingham, University of California, Berkeley
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W2115805227