Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants

Abstract

Lutein, a dihydroxy β,ε-carotenoid, is the predominant carotenoid in photosynthetic plant tissue and plays a critical role in light-harvesting complex assembly and function. To further understand lutein synthesis and function, we isolated four lutein-deficient mutants of Arabidopsis that define two loci, lut1 and lut2 (for lutein deficient). These loci are required for lutein biosynthesis but not for the biosynthesis of β,β- carotenoids. The lut1 mutations are recessive, accumulate high levels of zeinoxanthin, which is the immediate precursor of lutein, and define lut1 as a disruption in ε ring hydroxylation. The lut2 mutations are semidominant, and their biochemical phenotype is consistent with a disruption of ε ring cyclization. The lut2 locus cosegregates with the recently isolated ε cyclase gene, thus providing additional evidence that the lut2 alleles are mutations in the ε cyclase gene. It appears likely that the ε cyclase is a key step in regulating lutein levels and the ratio of lutein to β,β- carotenoids. Surprisingly, despite the absence of lutein, neither the lut1 nor lut2 mutation causes a visible deleterious phenotype or altered chlorophyll content, but both mutants have significantly higher levels of β,β-carotenoids. In particular, there is a stable increase in the xanthophyll cycle pigments (violexanthin, antheraxanthin, and zeaxanthin) in both lut1 and lut2 mutants as well as an increase in zeinoxanthin in lut1 and β-carotene in lut2. The accumulation of specific carotenoids is discussed as it pertains to the regulation of carotenoid biosynthesis and incorporation into the photosynthetic apparatus. Presumably, particular β,β-carotenoids are able to compensate functionally and structurally for lutein in the photosystems of Arabidopsis.