Abstract
Liriodendron tulipifera, also known as tuliptree, is a popular ornamental horticultural plant with extraordinary tulip-shaped flowers characterized by an orange band near their base. The mechanisms underlying petal band-specific pigmentation during L. tulipifera flower development are unclear. Here, we combined nontargeted and targeted metabolomics and transcriptomics to identify a pathway cascade leading to carotenoid biosynthesis that is specifically activated in the petal band. The comparative analysis of carotenoid metabolites between L. tulipifera and Liriodendron hybrids indicates that γ-carotene, a rare carotene in plants, is the most likely orange pigment responsible for the coloration of the petal band. Phenotypic and transcriptomic analyses of developing petals reveal that the band area is first predefined by the loss of green color. Later, the band is maintained by locally activating and repressing carotenoid and chlorophyll biosynthesis genes, respectively. Two rate-limiting genes of carotene biosynthesis, carotenoid isomerase (CRTISO) and epsilon lycopene cyclase (ε-LCY), encode the core enzymes responsible for petal band-specific orange pigmentation in L. tulipifera. In particular, a putative additional ε-LCY copy specific to L. tulipifera may contribute to the distinct petal coloration pattern, compared with L. chinense. Taken together, our work provides a first glimpse of the metabolome and transcriptome dynamics in tuliptree flower coloration and provides a valuable resource for flower breeding or metabolic engineering as well as for understanding flower evolution in an early woody angiosperm.
Highlights
Petal color is a major floral trait involved in attracting pollinators to ensure reproductive success
Consistent with this, we found that genes that were downregulated on the lower side of petals were significantly enriched for the Gene ontology (GO) term of “chlorophyllide a oxygenase activity,” which is associated with chlorophyll zz biosynthesis[35] (Fig. 3d)
We found that two chlorophyll biosynthesis-related genes, Cluster30529.88746, encoding glutamyl-tRNA reductase[36], and Cluster-30529.75818, encoding Mg-protoporphyrin IX monomethylester cyclase[37], were downregulated on the lower side compared to the upper side of petals
Summary
Petal color is a major floral trait involved in attracting pollinators to ensure reproductive success. Flower color diversity is mainly defined by three major pigment types: flavonoids, carotenoids and betalains[3], and the precise spatiotemporal regulation of the expression of these pigment biosynthesis-related genes generates specific coloration patterns[4]. Flavonoids are arguably the best-characterized plant secondary metabolites and exhibit the widest color range, conferring orange to blue (anthocyanins) and pale-yellow (chalcones, aurones and anthoxanthins) coloration[6]. Cytosol-synthesized and vacuole-localized water-soluble anthocyanins are the main flavonoid group and contribute to color pigmentation in many flowers[7]. The biosynthesis pathway of carotenoids, a class of plastidsynthesized and localized lipid-soluble C40 tetraterpenoids, has been well established, the underlying
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