Cytochrome P450 CitCYP97B modulates carotenoid accumulation diversity by hydroxylating β-cryptoxanthin in Citrus.

Carotenoids in plant foods function as provitamin A for health benefits. One of the vital provitamin A carotenoids, β-cryptoxanthin, is typically plentiful in citrus fruits. However, the genetic basis underlying the accumulation of β-cryptoxanthin in citrus remains largely elusive. Here, we performed a widely targeted metabolomic analysis of 65 major carotenoids and carotenoid derivatives to characterize the carotenoid accumulation in Citrus and determined the taxonomic profile of β-cryptoxanthin. We newly sequenced 81 representative accessions and additionally collected 69 previous Citrus cultivars to uncover the genetic basis of β-cryptoxanthin accumulation using a genome-wide association study (GWAS). We identified a causal gene, CitCYP97B, which encodes a cytochrome P450 protein, but its substrate and metabolic pathways in land plants are undetermined. Therefore, we validated that CitCYP97B functions as a novel monooxygenase that specifically hydroxylates the β-ring of β-cryptoxanthin in a heterologous expression system. In planta experiments further supported that CitCYP97B negatively regulated β-cryptoxanthin content. Based on the Citrus sequencing accessions, we found that two critical structural cis-element variations contribute to the elevated expression of CitCYP97B, thereby altering the β-cryptoxanthin accumulation in fruits. Hybridization/introgression contributes to the prevalence of two cis-element variations in different Citrus types during the citrus evolution. Overall, our findings extend the regulation and diversity of carotenoid metabolism in fruit crops and provide a genetic target for generating β-cryptoxanthin biofortified products.

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