Manipulation of Photoprotection to Improve Plant Photosynthesis

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 an