Abstract
Isomerization of 9,15,9′-tri-cis-ζ-carotene mediated by 15-cis-ζ-carotene isomerase Z-ISO is a critical step in the biosynthesis of carotenoids, which define fruit color. The tomato clade (Solanum section Lycopersicon) comprises the cultivated tomato (Solanum lycopersicum) and 12 related wild species differing in fruit color and, thus, represents a good model for studying carotenogenesis in fleshy fruit. In this study, we identified homologous Z-ISO genes, including 5′-UTRs and promoter regions, in 12 S. lycopersicum cultivars and 5 wild tomato species (red-fruited Solanum pimpinellifolium, yellow-fruited Solanum cheesmaniae, and green-fruited Solanum chilense, Solanum habrochaites, and Solanum pennellii). Z-ISO homologs had a highly conserved structure, suggesting that Z-ISO performs a similar function in tomato species despite the difference in their fruit color. Z-ISO transcription levels positively correlated with the carotenoid content in ripe fruit of the tomatoes. An analysis of the Z-ISO promoter and 5′-UTR sequences revealed over 130 cis-regulatory elements involved in response to light, stresses, and hormones, and in the binding of transcription factors. Green- and red/yellow-fruited Solanum species differed in the number and position of cis-elements, indicating changes in the transcriptional regulation of Z-ISO expression during tomato evolution, which likely contribute to the difference in fruit color.
Highlights
Carotenoids are yellow, orange, and red pigments that are essential for plant development and survival, and that play an important role in healthy human nutrition [1,2]
The following sequential reactions catalyzed by phytoene desaturase (PDS), ζ-carotene desaturase (ZDS), and two carotene cis-trans isomerases (CRTISO) yield trans-lycopene—a red pigment serving as a precursor for the synthesis of orange α- and β-carotenes, which can be converted to yellow lutein and xanthophyll, respectively [3,4,5,6]
A total of 21 complete sequences of Z-ISO homologous genes, including 5 -UTR and promoter regions, were amplified from 12 S. lycopersicum cultivars, differing in fruit color, and eight accessions of five wild tomato species: red-fruited (RF) Solanum pimpinellifolium, yellow-fruited (YF) Solanum cheesmaniae, and green-fruited (GF) Solanum chilense, Solanum habrochaites, and Solanum pennellii; their GenBank accession numbers are listed in Table 1 and Supplementary Table S2)
Summary
Carotenoids are yellow, orange, and red pigments that are essential for plant development and survival, and that play an important role in healthy human nutrition [1,2]. The catalytic function of Z-ISO, which belongs to the nitrite and nitric oxide reductase U (NnrU) family, requires heme cofactor b that, in the reduced state, triggers conformational changes in the active site of the enzyme to allow substrate binding [6]. Such dependence of Z-ISO activity on the redox status of the plastids, which is subjected to changes in response to various internal and external signals, makes Z-ISO a key enzyme in the dynamic control of carotenoid biosynthesis and flux [6,9,10,11]. Z-ISO plays a critical role in carotenoid production in the absence of light exposure [6,7,10], and at temperature fluctuations [12,13], indicating possible involvement of this enzyme in the evolutionary adaptation of plants to environmental changes [6] and in the breeding of cultivars with consolidated valuable traits
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