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

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 (<i>Solanum</i> section Lycopersicon) compris...

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Main Authors: Gleb I. Efremov, Maria A. Slugina, Anna V. Shchennikova, Elena Z. Kochieva
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/9/9/1169
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author Gleb I. Efremov
Maria A. Slugina
Anna V. Shchennikova
Elena Z. Kochieva
author_facet Gleb I. Efremov
Maria A. Slugina
Anna V. Shchennikova
Elena Z. Kochieva
author_sort Gleb I. Efremov
collection DOAJ
description 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 (<i>Solanum</i> section Lycopersicon) comprise cultivated (<i>Solanum lycopersicum</i>) 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 <i>PSY1</i> genes in five <i>Solanum</i> section Lycopersicon species, including domesticated red-fruited <i>S. lycopersicum</i> and wild yellow-fruited <i>S. cheesmaniae</i> and green-fruited <i>S. chilense</i>, <i>S. habrochaites</i> and <i>S. pennellii</i>. 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 <i>S. lycopersicum</i>. <i>PSY1</i> mRNA expression directly correlated with carotenoid content in ripe fruit of the analyzed tomato species, indicating differential transcriptional regulation. Analysis of the <i>PSY1</i> 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 <i>PSY1</i> expression may affect the processes of fruit senescence, seed maturation and dormancy, and pathogen resistance. The revealed differences between green-fruited and red-fruited <i>Solanum</i> species in the structure of the <i>PSY1</i> promoter/5′-UTR, such as the acquisition of ethylene-responsive element by <i>S. lycopersicum</i>, could reflect the effects of domestication on the transcriptional mechanisms regulating <i>PSY1</i> expression, including induction of carotenogenesis during fruit ripening, which would contribute to red coloration in mature fruit.
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spelling doaj.art-924a712298514d2ca692153eee1b296d2023-11-20T13:05:52ZengMDPI AGPlants2223-77472020-09-0199116910.3390/plants9091169Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)Gleb I. Efremov0Maria A. Slugina1Anna V. Shchennikova2Elena Z. Kochieva3Institute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, 119071 Moscow, RussiaInstitute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, 119071 Moscow, RussiaInstitute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, 119071 Moscow, RussiaInstitute of Bioengineering, Research Center of Biotechnology, Russian Academy of Sciences, 119071 Moscow, RussiaIn 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 (<i>Solanum</i> section Lycopersicon) comprise cultivated (<i>Solanum lycopersicum</i>) 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 <i>PSY1</i> genes in five <i>Solanum</i> section Lycopersicon species, including domesticated red-fruited <i>S. lycopersicum</i> and wild yellow-fruited <i>S. cheesmaniae</i> and green-fruited <i>S. chilense</i>, <i>S. habrochaites</i> and <i>S. pennellii</i>. 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 <i>S. lycopersicum</i>. <i>PSY1</i> mRNA expression directly correlated with carotenoid content in ripe fruit of the analyzed tomato species, indicating differential transcriptional regulation. Analysis of the <i>PSY1</i> 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 <i>PSY1</i> expression may affect the processes of fruit senescence, seed maturation and dormancy, and pathogen resistance. The revealed differences between green-fruited and red-fruited <i>Solanum</i> species in the structure of the <i>PSY1</i> promoter/5′-UTR, such as the acquisition of ethylene-responsive element by <i>S. lycopersicum</i>, could reflect the effects of domestication on the transcriptional mechanisms regulating <i>PSY1</i> expression, including induction of carotenogenesis during fruit ripening, which would contribute to red coloration in mature fruit.https://www.mdpi.com/2223-7747/9/9/1169carotenogenesisfruit color<i>Solanum</i> section Lycopersiconphytoene synthase 1
spellingShingle Gleb I. Efremov
Maria A. Slugina
Anna V. Shchennikova
Elena Z. Kochieva
Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
Plants
carotenogenesis
fruit color
<i>Solanum</i> section Lycopersicon
phytoene synthase 1
title Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
title_full Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
title_fullStr Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
title_full_unstemmed Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
title_short Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species (<i>Solanum</i> section Lycopersicon)
title_sort differential regulation of phytoene synthase psy1 during fruit carotenogenesis in cultivated and wild tomato species i solanum i section lycopersicon
topic carotenogenesis
fruit color
<i>Solanum</i> section Lycopersicon
phytoene synthase 1
url https://www.mdpi.com/2223-7747/9/9/1169
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AT mariaaslugina differentialregulationofphytoenesynthasepsy1duringfruitcarotenogenesisincultivatedandwildtomatospeciesisolanumisectionlycopersicon
AT annavshchennikova differentialregulationofphytoenesynthasepsy1duringfruitcarotenogenesisincultivatedandwildtomatospeciesisolanumisectionlycopersicon
AT elenazkochieva differentialregulationofphytoenesynthasepsy1duringfruitcarotenogenesisincultivatedandwildtomatospeciesisolanumisectionlycopersicon