Revealing Missing Links in the Downsizing of the Photosystem II Antenna in Higher Plants Under Stress Conditions

Chloroplast-to-nucleus ROS retrograde signaling is essential for acclimation of the photosynthetic apparatus to environmental stresses. One of the key mechanisms is the regulation of the photosystem II antenna size depending on light conditions and other environmental factors. However, the molecular components linking chloroplast redox status to nuclear gene regulation remain poorly defined. Here, we demonstrate that H₂O₂, generated in chloroplasts, in particular with involvement of the plastoquinone pool components, enhances the protease activity in the chloroplast envelope. As it is known, protease activity leads to the processing of the chloroplast envelope-bound transcription factor PTM, enabling its relocation to the nucleus, where it induces ABI4 expression. ABI4, in turn, represses transcription of lhcb genes, resulting in downsizing of the PS II antenna. Gene expression analysis confirms the coordinated upregulation of ABI4, and PTM, as well as metallo-ASP and serine SPPA1 envelope proteases in high light. We further show that H₂O₂ at physiologically relevant concentrations specifically stimulates the serine protease activity, since this activation is inhibited by PMSF. Our findings indicate a link between redox changes in the plastoquinone pool and the H₂O₂ level in chloroplasts with protease-mediated signaling cascades. Therefore, the obtained data reveal the connection between chloroplast and nuclear control of photosynthetic light harvesting, highlighting a signaling strategy for the photosystem II antenna size regulation in higher plants.