Carotenoid cleavage dioxygenases (CCDs) drive carotenoid catabolism to produce various apocarotenoids and immediate derivatives with particular developmental, ecological, and agricultural importance. How CCD genes evolved with species diversification and the resulting functional novelties in cereal crops have remained largely elusive. We constructed a unified four-clade phylogenetic tree of CCDs, revealing a previously unanchored basal clade CCD10 CCD10 underwent highly dynamic duplication or loss events, even in the grass family. Different from cleavage sites of CCD8 and ZAXINONE SYNTHASE (ZAS), maize (Zea mays) ZmCCD10a cleaved differentially structured carotenoids at 5, 6 (5', 6') and 9, 10 (9', 10') positions, generating C8 (6-methyl-5-hepten-2-one) and C13 (geranylacetone, α-ionone, and β-ionone) apocarotenoids in Escherichia coli Localized in plastids, ZmCCD10a cleaved neoxanthin, violaxanthin, antheraxathin, lutein, zeaxanthin, and β-carotene in planta, corroborating functional divergence of ZmCCD10a and ZAS. ZmCCD10a expression was dramatically stimulated in maize and teosinte (Z. mays ssp. parviglumis, Z. mays ssp. huehuetenangensis, Zea luxurians, and Zea diploperennis) roots by phosphate (Pi) limitation. ZmCCD10a silencing favored phosphorus retention in the root and reduced phosphorus and biomass accumulation in the shoot under low Pi. Overexpression of ZmCCD10a in Arabidopsis (Arabidopsis thaliana) enhanced plant tolerance to Pi limitation by preferential phosphorus allocation to the shoot. Thus, ZmCCD10a encodes a unique CCD facilitating plant tolerance to Pi limitation. Additionally, ZmCCD10a silencing and overexpression led to coherent alterations in expression of PHOSPHATE STARVATION RESPONSE REGULATOR 1 (PHR1) and Pi transporters, and cis-regulation of ZmCCD10a expression by ZmPHR1;1 and ZmPHR1;2 implies a probable ZmCCD10a-involved regulatory pathway that adjusts Pi allocation.
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