Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (Solanum section Lycopersicon)

Abstract

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.

High-Throughput Chlorophyll and Carotenoid Profiling Reveals Positive Associations with Sugar and Apocarotenoid Volatile Content in Fruits of Tomato Varieties in Modern and Wild Accessions

“…In summary, the total amount of carotenoids in tomato fruits can vary depending on PSY1 expression, but the ratio of lycopene among the varieties may remain constant by controlling downstream pathways. It is known that carotenoid content in tomato fruit is largely influenced by changes in growth conditions (e.g., light, temperature, season, drought stress, salinity stress, and pedoclimatic conditions) [ 9 , 38 , 39 , 40 , 41 ]. Analyzing associations between carotenoid and AC-VOC content in tomato fruits grown under different growth conditions may reveal further clues for improving AC-VOC production.…”

Characterization of 15-cis-ζ-Carotene Isomerase Z-ISO in Cultivated and Wild Tomato Species Differing in Ripe Fruit Pigmentation

“…Several studies have investigated transcriptional regulation of the genes involved in carotenoid biosynthesis in tomato. Thus, it has been shown that in S. lycopersicum and S. pennellii the upstream regions of the PSY1 gene contain at least 37 types of regulatory elements, indicating that PSY1 transcription may be altered in response to light, abiotic stresses, and hormones [28,29]. Our analysis revealed that the upstream regions of Z-ISO also contained cis-elements associated with response to light, hormones, and stresses and did not significantly differ between RF S. lycopersicum cv.…”

“…The conversion of chloroplasts to chromoplasts, which store the carotenoid pigments, is essential for fruit ripening process in tomato and is the primary factor in tomato fruit coloring [34,35]. The other factor is the expression of PSY1, which catalyzes the first stage of carotenoid biosynthesis and defines the content of colored carotenoids [29]. In this scenario, Z-ISO, which determines the switch from the production of colorless carotene to that of colored carotenoids, should contribute to the difference in the color of ripe fruit between YF/RF and GF tomato species.…”

“…Total carotenoid content was measured by spectrophotometry in two biological and three technical replicates using a modified Folch method [47,48]. Briefly, 0.2 g of plant tissue was homogenized in Folch solution (2:1 chloroform-methanol [v/v]) in the presence of trace amounts of Mg 2 CO 3 [46], incubated at 4 • C for 1 h, and centrifuged at 4000 rpm for 10 min at 4 • C. The lower chloroform phase was collected, and lycopene, β-carotene, and total carotenoid contents (xanthophylls plus carotenes) were measured as previously described [49] using a spectrophotometer (Basic, Eppendorf, Hamburg, Germany) and calculated according to the published formulas [29].…”

Characterization of RIN Isoforms and Their Expression in Tomato Fruit Ripening

“…(red fruit) [ 9 , 10 ]. The difference in fruit color between wild green-fruited (GF) tomatoes and S. lycopersicum cultivars is defined by carotenoid content [ 11 ], and that in taste by preferential accumulation of sucrose instead of glucose and fructose, respectively [ 12 ]. However, S. lycopersicum variants carrying the rin mutation are similar to GF species in fruit morphology and biochemical composition [ 2 ].…”