Radicals formed from proton loss of carotenoid radical cations: A special form of carotenoid neutral radical occurring in photoprotection

Abstract

In an organized assembly in Arabidopsis thaliana plant, proton loss from the radical cation of zeaxanthin (Zea) was found to occur under intense illumination, a possible component in photoprotection. A stable neutral radical is formed because of the favorable proton loss at C4(4') position(s) of the terminal ends of Zea that extends the unpaired spin density distribution (notation Zea(4) or Zea(4') by symmetry). Proton loss from the radical cation of β-carotene (β-car) to available proton acceptors was also detected in a PSII sample upon irradiation. A controversial optical absorption peak at 750nm predicted by DFT was attributed to β-carotene neutral radical formed by proton loss at C4(4') position(s) situated on the terminal end(s) (notation β-car(4) or β-car(4') by symmetry), also detected in solid copper-containing MCM-41 molecular sieves (Cu-MCM-41) and by hydrogen atom transfer from β-carotene to hydroxyl radical. Unlike the PSII organized assembly where proton loss occurs from the terminal ends of the radical cation, in the Cu-MCM-41 unorganized assembly proton loss occurs from all positions including the methyl groups on the polyene chain forming neutral radicals with different EPR couplings, different unpaired spin density distribution and different optical absorption peaks. We emphasize here the properties of these neutral radicals for various carotenoids formed under high-light conditions and in different media (solution, solid siliceous materials, and photosynthetic samples).

Singlet Oxygen and Free Radical Reactions of Retinoids and Carotenoids—A Review

“…It should be noted that this work established the optical absorption spectrum for the neutral species without using transient absorption spectroscopy. This assignment of the neutral species in the absence of oxygen was confirmed via studies of the effect of pH and this species was linked to a previously unassigned peak reported from spectral studies of Photosystem II (PSII) [ 69 ]. The Kispert group speculate that in PS II itself photoprotection can arise both by the loss of the excess vibrational energy of the radical cation and by quenching of excited chlorophyll by the carotenoid proton loss neutral radical.…”

“…A recent review [ 67 ] has highlighted a significant apparent disagreement concerning the fate of β-carotene radical cation. El-Agamey and co-workers [ 68 ] studied the effect of pH on the decay of the β-carotene radical cation (HCAR •+ ) while the extensive work of Kispert and co-workers used advanced electron paramagnetic resonance techniques and optical measurements beside electrochemical and theoretical studies [ 67 , 69 , 70 , 71 ]. The Kispert group showed that proton loss from β-carotene radical cation leads to the neutral carotenoid radical (CAR • ) HCAR •+ → CAR • + H + with an absorption maximum around 750 nm.…”

“…The Kispert group showed that proton loss from β-carotene radical cation leads to the neutral carotenoid radical (CAR • ) HCAR •+ → CAR • + H + with an absorption maximum around 750 nm. In their studies, Kispert et al form the radicals on silicate-based matrices [ 67 , 69 , 70 , 71 ]. Proton loss from the radical cation to produce a neutral species was identified using both electron paramagnetic resonance and optical detection.…”

“…Hydrogen abstraction from a carotenoid to a free radical leads, of course, to the same carotenoid neutral radical as deprotonation of the corresponding radical cation HCAR → CAR • + H • HCAR •+ → CAR • + H + and, as noted above there is interest in such neutral radicals because of their possible formation in PSII [ 67 , 69 , 70 , 71 ].…”

Photo Protection of Haematococcus pluvialis Algae by Astaxanthin: Unique Properties of Astaxanthin Deduced by EPR, Optical and Electrochemical Studies

“…Carotenoid radicals such as radical cations (Car • + ) formed by electron transfer from carotenoid molecules (see Figure 4 ) and proton loss neutral radicals #Car • formed under high light intensity by deprotonation of Car • + at the most favorable position have been found to occur not only in solution, but in photosynthetic media. The proton loss neutral radical, first observed to occur in irradiated PSII samples as #β-Car • (beta-carotene neutral radical) [ 23 ] and then in the Arabidopsis thaliana plant [ 24 ] as #Zea • (zeaxanthin neutral radical), has been suggested [ 25 , 26 ] to provide additional photo protection of plants to that provided by Car • + . Since the radical cation Zea • + is a weak acid (with pK a 4–7), loss of a proton will occur to a water acceptor and the proton loss neutral radical, #Zea • , is formed.…”