The mechanism of a photoprotective molecular switch in the photosynthetic light-harvesting complex of plants

The life of our biosphere is entirely dependent upon photosynthesis. Over millions of years oxygen-evolving organisms have been giving all heterotrophic organisms, including us, air to breathe and a source of food, energy and vital materials. The success of oxygenic photosynthesis on this planet is a great biological phenomenon, that relies first of all upon the efficient design and adaptability to the changing environmental conditions of the molecular machinery of the photosynthetic apparatus. The photosynthetic membrane is the most complex of all biological membranes and is the most enriched in various proteins. The latter bind a number of important co-factors: chlorophylls, carotenoids, lipids, ions and water. Protein tunes and co-ordinates the functions of these co-factors. This co-ordination lies at the heart of their biological function. One of the major pigment-lipoprotein complexes of the photosynthetic membrane is the light harvesting complex of photosystem II (LHCII). It collects the most significant part of the light energy received by the photosynthetic membrane and transfers it to the reaction centers, where charge separation occurs to initiate a chain of events leading to a synthesis of the universal biological fuel ATP and NADPH. LHCII was found to play an important regulatory role by controlling the amount of energy delivered to the reaction center. This is being achieved by dissipation of the excess energy into heat. Recently we have discovered that the currently available structure of LHCII does correspond to the structure of this complex in the rather dissipative state. This is an important finding, since it offers us structural insights of how the photosynthetic membrane is sensing and dealing with the excess light, hence how plants can protect themselves against this type of stress and survive it. The current program is built upon the knowledge of LHCII structure and aims to answer a number of important mechanistic questions. We want to find out what factors lead to the switching of LHCII into the dissipative mode, at what level of protein organization does this switch work: domains of the monomer, trimer or more collective, higher oligomer units? What is the nature of the new energetic parameters like fluorescence, combinational scattering (Raman) and absorption features accompanying the dissipative state and what is the nature of the excitation energy dissipation? What is the role of minor ligands, xanthophyll cycle carotenoids, violaxanthin and zeaxanthin in the regulation of the LHCII switch? The project should provide us with the knowledge of the very fundamental features put into the LHCII antenna design, which allow the light harvesting process in nature to be efficient and flexible at the same time, insuring a high level of plant productivity and adaptability to the light environment on our planet.

This project concerns a molecular aspect of the major regulatory mechanism that controls the efficiency of light utilization in plants, providing either effective collection of light in a shaded environment or efficient photoprotection against damage by excess light. The major LHCII antenna complex will be in the focus of this research. On its own it exhibits the properties of a molecular switch by tuning the excitation energy lifetime from a few nanoseconds to a few hundred picoseconds. The project will combine investigations of the light harvesting/dissipation efficiency of LHCII in crystalline form as well as in different states of aggregation and incorporated into gels. The approach should enable us to distinguish between the contributions of protein aggregation and internal conformational changes within LHCII into the transition between the light harvesting and dissipative modes in the LHC antenna. Application of site-selective, transient absorption, fluorescence and vibrational spectroscopies, should enable us to map the course of molecular events leading to the establishment of the photoprotective state in LHCII and identify the excitation energy quencher.