Flavodiiron proteins in Physcomitrium patens: navigating the edge between photoprotection and efficiency

Abstract

Sunlight is the primary energy source for photosynthetic organisms, driving electron transport that supports the synthesis of ATP and NADPH. In dynamic environmental conditions, photosynthetic electron transport requires continuous modulation to prevent over-reduction and safeguard against potential damage. Flavodiiron proteins (FLV) contribute to photoprotection by accepting electrons downstream of Photosystem I, reducing oxygen to water. FLV were shown to have a seminal role in response to abrupt changes in illumination intensity in various photosynthetic organisms, such as cyanobacteria, green algae, mosses, and gymnosperms but were lost during evolution of angiosperms. In this work, Physcomitrium patens plants with strong FLV accumulation, up to 20 times higher than WT, were isolated. Overexpressor plants exhibited faster activation of electron transport but did not gain additional tolerance to light fluctuations, suggesting that the contribution to photoprotection from the FLV was already saturated in WT plants. On the contrary, strong protein overexpression caused a growth penalty under steady low or high light intensity suggesting that FLV overaccumulation can be detrimental, at least in some conditions, opening hypotheses to explain why these proteins were lost during the evolution of angiosperms.