Multiscale structural basis of photoprotection in plant light-harvesting proteins

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Plant productivity is defined by the ability to efficiently and safely harvest sunlight. Efficient light-harvesting is ensured by the 'antenna', a large assembly of chlorophyll-filled proteins that capture solar energy and deliver it to the few 'reaction centre' proteins that convert solar energy into chemical energy. However, light levels can to go from moderate to dangerously bright within minutes, leading to excess absorption of energy and damage to the delicate reaction centres. This is mitigated by Energy-dependent quenching (or 'qE'), a protective mechanism in which the antenna senses the high intensity of light and switches to a protective state. In this state excess energy is harmlessly dissipated (or 'quenched') before damage occurs. Recently, it was shown that controlling qE at the molecular level is a very promising route to enhancing food production. This is somewhat hindered by the fact that, unlike other important biological mechanisms, the precise workings of qE are unclear. We do know that the major antenna protein, LHCII, plays a central role. High light intensity causes individual LHCII proteins to switch between energy-harvesting and energy-quenching states. They also collectively reorganize themselves to form large, clustered networks in the chloroplast membrane. qE is therefore a 'multi-scale' mechanism involving structural changes inside antenna proteins and in the whole antenna assembly. Unfortunately, we don't have a detailed picture of what these structural changes are which makes experimental data difficult to interpret and has led to many contradictory ideas of how qE works. We will establish the mechanism of qE with greater accuracy than ever possible. We will use a 'bottom-up' approach, first studying how individual, isolated LHCII operate and using this to establish how they collectively operate as an entire 'antenna'. First we will predict the light-harvesting structure of LHCII. Since experimental techniques have failed to do this, we will instead use rigorous computational simulation. This allows us to mimic realistic conditions, in this case LHCII in a membrane under low light, and to see the movement and flexibility of the structure. Using the techniques of theoretical biophysics we will explain how this structure promotes efficient harvesting of energy rather than deliberate protective dissipation. We will then predict the potential protective, energy-dissipating structures of LHCII. The current 3D structure LHCII is often used as a prototype for the protective state but it is likely a poor approximation. We will use our bio-simulation approach to consider high light conditions, predict these structures, and fully characterize how they function protectively. In the final part, we will consider the large networks of LHCII that occur in natural membranes by experimentation as well as theory. Using ultra-high resolution microscopy we will characterize the structures of these networks. At the same time, using high resolution fluorescence imaging, we will directly measure the rate at which energy is being quenched within them. When combined with our LHCII simulations we develop a complete picture of the qE mechanism: how it operates at the molecular level, how it is controlled by protein structure and external conditions, and how this effects the function of the plant antenna as a whole. This will finally answer a long-standing and controversial question in plant science. More importantly, it will provide a molecular foundation to our efforts to understand how plants capture, manage and transform the sun's energy.