In plants, carotenoids define fruit pigmentation and are involved in the processes of photo-oxidative stress defense and phytohormone production; a key enzyme responsible for carotene synthesis in fruit is phytoene synthase 1 (PSY1). Tomatoes (Solanum section Lycopersicon) comprise cultivated (Solanum lycopersicum) as well as wild species with different fruit color and are a good model to study carotenogenesis in fleshy fruit. In this study, we identified homologous PSY1 genes in five Solanum section Lycopersicon species, including domesticated red-fruited S. lycopersicum and wild yellow-fruited S. cheesmaniae and green-fruited S. chilense, S. habrochaites and S. pennellii. PSY1 homologs had a highly conserved structure, including key motifs in the active and catalytic sites, suggesting that PSY1 enzymatic function is similar in green-fruited wild tomato species and preserved in red-fruited S. lycopersicum. PSY1 mRNA expression directly correlated with carotenoid content in ripe fruit of the analyzed tomato species, indicating differential transcriptional regulation. Analysis of the PSY1 promoter and 5′-UTR sequence revealed over 30 regulatory elements involved in response to light, abiotic stresses, plant hormones, and parasites, suggesting that the regulation of PSY1 expression may affect the processes of fruit senescence, seed maturation and dormancy, and pathogen resistance. The revealed differences between green-fruited and red-fruited Solanum species in the structure of the PSY1 promoter/5′-UTR, such as the acquisition of ethylene-responsive element by S. lycopersicum, could reflect the effects of domestication on the transcriptional mechanisms regulating PSY1 expression, including induction of carotenogenesis during fruit ripening, which would contribute to red coloration in mature fruit.
The fruits of various pepper cultivars are characterized by a different colour, which is determined by the pigment ratio; carotenoids dominate in ripe fruits, while chlorophylls, in immature fruits. A key regulator of carotenoid biosynthesis is the phytoene synthase encoded by the PSY gene. The Capsicum annuum genome contains two isoforms of this enzyme, localized in leaf (PSY2) and fruit (PSY1) plastids. In this work, the complete PSY1 and PSY2 genes were identified in nine C. annuum cultivars, which differ in ripe fruit colour. PSY1 and PSY2 sequence variability was 2.43 % (69 SNPs) and 1.21 % (36 SNPs). The most variable were PSY1 proteins of the cultivars ‘Maria’ (red-fruited) and ‘Sladkij shokolad’ (red-brown-fruited). All identified PSY1 and PSY2 homologs contained the phytoene synthase domain HH-IPPS and the transit peptide. In the PSY1 and PSY2 HH-IPPS domains, functionally significant sites were determined. For all accessions studied, the active sites (YAKTF and RAYV), aspartate-rich substrate-Mg2+-binding sites (DELVD and DVGED), and other functional residues were shown to be conserved. Transit peptides were more variable, and their similarity in the PSY1 and PSY2 proteins did not exceed 78.68 %. According to the biochemical data obtained, the largest amounts of chlorophylls and carotenoids across the cultivars studied were detected in immature and ripe fruits of the cv. ‘Sladkij shokolad’ and ‘Shokoladnyj’. Also, ripe fruits of the cv. ‘Nesozrevayuschij’ (green-fruited) were marked by significant chlorophyll content, but a minimum of carotenoids. The PSY1 and PSY2 expression patterns were determined in the fruit pericarp at three ripening stages in ‘Zheltyj buket’, ‘Sladkij shokolad’, ‘Karmin’ and ‘Nesozrevayuschij’, which have different ripe fruit colours: yellow, red-brown, dark red and green, respectively. In the leaves of the cultivars studied, PSY1 expression levels varied significantly. All cultivars were characterized by increased PSY1 transcription as the fruit ripened; the maximum transcription level was found in the ripe fruit of ‘Sladkij shokolad’, and the lowest, in ‘Nesozrevayuschij’. PSY2 transcripts were detected not only in the leaves and immature fruits, but also in ripe fruits. Assessment of a possible correlation of PSY1 and PSY2 transcription with carotenoid and chlorophyll content revealed a direct relationship between PSY1 expression level and carotenoid pigmentation during fruit ripening. It has been suggested that the absence of a typical pericarp pigmentation pattern in ‘Nesozrevayuschij’ may be associated with impaired chromoplast formation.
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.
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