Leaves of avocado (Persea americana Mill.) 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 de-epoxidized to lutein (L) after one hour exposure to 120 to 350 μmol photons m-2 s-1 increasing the total L pool by 5-10% (ΔL). De-epoxidation of Lx to L was near stoichiometric and similar in kinetics to de-epoxidation 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 (NPQΔpH) before de-epoxidation; after de-epoxidation in the presence of ΔL, A, and Z (NPQΔLAZ); and after epoxidation of A+Z but with residual ΔL (NPQΔL). The capacity of both NPQΔLAZ and NPQΔL was similar and 45% larger than NPQΔpH but dark relaxation of NPQΔLAZ was slower The enhanced capacity for NPQ was lost after metabolism of ΔL. The near equivalence of NPQΔLAZ and NPQΔL provides compelling evidence that the small dynamic pool ΔL replaces A+Z in avocado to “lock-in” enhanced NPQ. Results are discussed in relation to data obtained with other Lx-rich species and in mutants of Arabidopsis with increased L pools.