Light-harvesting complexes access analogue emissive states in different environments

The light-harvesting complexes (LHCs) of plants can regulate the level of excitation in the photosynthetic membrane under fluctuating light by switching between different functional states with distinct fluorescence properties. One of the most fascinating yet obscure aspects of this regulation is how the vast conformational landscape of LHCs is modulated in different environments. Indeed, while in isolated antennae the highly fluorescent light-harvesting conformation dominates, LHC aggregates display strong fluorescence quenching, representing therefore a model system for the process of energy dissipation developed by plants to avoid photodamage in high light. This marked difference between the isolated and oligomeric conditions has led to the widespread belief that aggregation is the trigger for the photoprotective state of LHCs. Here, a detailed analysis of time-resolved fluorescence experiments performed on aggregates of CP29 – a minor LHC of plants – provides new insights into the heterogeneity of emissive states of this antenna. A comparison with the data on isolated CP29 reveals that, though aggregation can stabilize short-lived conformations to a certain extent, the massive quenching upon protein clustering is mainly achieved by energetic connectivity between complexes that maintain the same long-lived and dissipative states accessed in the isolated form. Our results also explain the typical far-red enhancement in the emission of antenna oligomers in terms of a sub-population of long-lived redshifted complexes competing with quenched complexes in the energy trapping. Finally, the role of selected chlorophylls in shaping the conformational landscape of the antenna is also addressed by studying mutants lacking specific pigments.