Lutein from deepoxidation of lutein epoxide replaces zeaxanthin to sustain an enhanced capacity for nonphotochemical chlorophyll fluorescence quenching in avocado shade leaves in the dark

Leaves of avocado (Persea americana) that develop and persist in deep shade canopies have very low rates of photosynthesis but contain high concentrations of lutein epoxide (Lx) that are partially deepoxidized to lutein (L) after 1 h of exposure to 120 to 350 μmol photons m^-2 s^-1, increasing the total L pool by 5% to 10% (ΔL). Deepoxidation of Lx to L was near stoichiometric and similar in kinetics to deepoxidation of violaxanthin (V) to antheraxanthin (A) and zeaxanthin (Z). Although the V pool was restored by epoxidation of A and Z overnight, the Lx pool was not. Depending on leaf age and pretreatment, the pool of ΔL persisted for up to 72 h in the dark. Metabolism of ΔL did not involve epoxidation to Lx. These contrasting kinetics enabled us to differentiate three states of the capacity for nonphotochemical chlorophyll fluorescence quenching (NPQ) in attached and detached leaves: ΔpH dependent (NPQ_ΔpH) before deepoxidation; after deepoxidation in the presence of ΔL, A, and Z (NPQ_ΔLAZ); and after epoxidation of A+Z but with residual ΔL (NPQ_ΔL). The capacity of both NPQ_ΔLAZ and NPQ_ΔL was similar and 45% larger than NPQ_ΔpH, but dark relaxation of NPQ_ΔLAZ was slower. The enhanced capacity for NPQ was lost after metabolism of ΔL. The near equivalence of NPQ_ΔLAZ and NPQ_ΔL provides compelling evidence that the small dynamic pool ΔL replaces A+Z in avocado to "lock in" enhanced NPQ. The results are discussed in relation to data obtained with other Lx-rich species and in mutants of Arabidopsis (Arabidopsis thaliana) with increased L pools.