Higher order photoprotection mutants reveal the importance of ΔpH-dependent photosynthesis-control in preventing light induced damage to both photosystem II and photosystem I

Although light is essential for photosynthesis, when in excess, it may damage the photosynthetic
apparatus, leading to a phenomenon known as photoinhibition. Photoinhibition was thought as a
light-induced damage to photosystem II; however, it is now clear that even photosystem I may become
very vulnerable to light. One main characteristic of light induced damage to photosystem II (PSII) is
the increased turnover of the reaction center protein, D1: when rate of degradation exceeds the rate of
synthesis, loss of PSII activity is observed. With respect to photosystem I (PSI), an excess of electrons,
instead of an excess of light, may be very dangerous. Plants possess a number of mechanisms able
to prevent, or limit, such damages by safe thermal dissipation of light energy (non-photochemical
quenching, NPQ), slowing-down of electron transfer through the intersystem transport chain
(photosynthesis-control, PSC) in co-operation with the Proton Gradient Regulation (PGR) proteins,
PGR5 and PGRL1, collectively called as short-term photoprotection mechanisms, and the redistribution
of light between photosystems, called state transitions (responsible of fluorescence quenching at PSII,
qT), is superimposed to these short term photoprotective mechanisms. In this manuscript we have
generated a number of higher order mutants by crossing genotypes carrying defects in each of the
short-term photoprotection mechanisms, with the final aim to obtain a direct comparison of their role
and efficiency in photoprotection. We found that mutants carrying a defect in the ΔpH-dependent
photosynthesis-control are characterized by photoinhibition of both photosystems, irrespectively of
whether PSBS-dependent NPQ or state transitions defects were present or not in the same individual,
demonstrating the primary role of PSC in photoprotection. Moreover, mutants with a limited capability
to develop a strong PSBS-dependent NPQ, were characterized by a high turnover of the D1 protein and
high values of Y(NO), which might reflect energy quenching processes occurring within the PSII reaction
center.