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Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes

Type-VI glandular trichomes of wild tomato Solanum habrochaites PI127826 produce high levels of the sesquiterpene 7-epizingiberene and its derivatives, making the plant repellent and toxic to several pest insects and pathogens. How wild tomato trichomes achieve such high terpene production is still...

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Autores principales: Kortbeek, Ruy W. J., Galland, Marc D., Muras, Aleksandra, Therezan, Rodrigo, Maia, Sofia, Haring, Michel A., Schuurink, Robert C., Bleeker, Petra M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10020594/
https://www.ncbi.nlm.nih.gov/pubmed/36938050
http://dx.doi.org/10.3389/fpls.2023.1139274
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author Kortbeek, Ruy W. J.
Galland, Marc D.
Muras, Aleksandra
Therezan, Rodrigo
Maia, Sofia
Haring, Michel A.
Schuurink, Robert C.
Bleeker, Petra M.
author_facet Kortbeek, Ruy W. J.
Galland, Marc D.
Muras, Aleksandra
Therezan, Rodrigo
Maia, Sofia
Haring, Michel A.
Schuurink, Robert C.
Bleeker, Petra M.
author_sort Kortbeek, Ruy W. J.
collection PubMed
description Type-VI glandular trichomes of wild tomato Solanum habrochaites PI127826 produce high levels of the sesquiterpene 7-epizingiberene and its derivatives, making the plant repellent and toxic to several pest insects and pathogens. How wild tomato trichomes achieve such high terpene production is still largely unknown. Here we show that a cross (F1) with a cultivated tomato produced only minute levels of 7-epizingiberene. In the F2-progeny, selected for the presence of the 7-epizingiberene biosynthesis genes, only three percent produced comparable amounts the wild parent, indicating this trait is recessive and multigenic. Moreover, trichome density alone did not explain the total levels of terpene levels found on the leaves. We selected F2 plants with the “high-production active-trichome phenotype” of PI127826, having trichomes producing about 150 times higher levels of terpenes than F2 individuals that displayed a “low-production lazy-trichome phenotype”. Terpene quantities in trichomes of these F2 plants correlated with the volume of the storage cavity and shape of the gland. We found that trichome morphology is not a predetermined characteristic, but cavity volume rather depended on gland-cell metabolic activity. Inhibitor assays showed that the plastidial-precursor pathway (MEP) is fundamental for high-level production of both cytosolic as well as plastid-derived terpenes in tomato trichomes. Additionally, gene expression profiles of isolated secretory cells showed that key enzymes in the MEP pathway were higher expressed in active trichomes. We conclude that the MEP pathway is the primary precursor-supply route in wild tomato type-VI trichomes and that the high-production phenotype of the wild tomato trichome is indeed a multigenic trait.
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spelling pubmed-100205942023-03-18 Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes Kortbeek, Ruy W. J. Galland, Marc D. Muras, Aleksandra Therezan, Rodrigo Maia, Sofia Haring, Michel A. Schuurink, Robert C. Bleeker, Petra M. Front Plant Sci Plant Science Type-VI glandular trichomes of wild tomato Solanum habrochaites PI127826 produce high levels of the sesquiterpene 7-epizingiberene and its derivatives, making the plant repellent and toxic to several pest insects and pathogens. How wild tomato trichomes achieve such high terpene production is still largely unknown. Here we show that a cross (F1) with a cultivated tomato produced only minute levels of 7-epizingiberene. In the F2-progeny, selected for the presence of the 7-epizingiberene biosynthesis genes, only three percent produced comparable amounts the wild parent, indicating this trait is recessive and multigenic. Moreover, trichome density alone did not explain the total levels of terpene levels found on the leaves. We selected F2 plants with the “high-production active-trichome phenotype” of PI127826, having trichomes producing about 150 times higher levels of terpenes than F2 individuals that displayed a “low-production lazy-trichome phenotype”. Terpene quantities in trichomes of these F2 plants correlated with the volume of the storage cavity and shape of the gland. We found that trichome morphology is not a predetermined characteristic, but cavity volume rather depended on gland-cell metabolic activity. Inhibitor assays showed that the plastidial-precursor pathway (MEP) is fundamental for high-level production of both cytosolic as well as plastid-derived terpenes in tomato trichomes. Additionally, gene expression profiles of isolated secretory cells showed that key enzymes in the MEP pathway were higher expressed in active trichomes. We conclude that the MEP pathway is the primary precursor-supply route in wild tomato type-VI trichomes and that the high-production phenotype of the wild tomato trichome is indeed a multigenic trait. Frontiers Media S.A. 2023-03-03 /pmc/articles/PMC10020594/ /pubmed/36938050 http://dx.doi.org/10.3389/fpls.2023.1139274 Text en Copyright © 2023 Kortbeek, Galland, Muras, Therezan, Maia, Haring, Schuurink and Bleeker https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Kortbeek, Ruy W. J.
Galland, Marc D.
Muras, Aleksandra
Therezan, Rodrigo
Maia, Sofia
Haring, Michel A.
Schuurink, Robert C.
Bleeker, Petra M.
Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title_full Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title_fullStr Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title_full_unstemmed Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title_short Genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
title_sort genetic and physiological requirements for high-level sesquiterpene-production in tomato glandular trichomes
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10020594/
https://www.ncbi.nlm.nih.gov/pubmed/36938050
http://dx.doi.org/10.3389/fpls.2023.1139274
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