Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits

IntroductionLipoic acid (LA) is a key, yet overlooked player in primary metabolism, due to its role as a cofactor for various multi enzymatic complexes such as the E2 subunits of pyruvate dehydrogenase (PDH) and alpha-ketoglutarate dehydrogenase (kGDH). In recent years, this molecule has seen renewe...

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Main Authors: María Paz Covarrubias, Felipe Uribe, Daniela Arias-G, Pamela Cabedo, Michael Handford
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1545011/full
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author María Paz Covarrubias
Felipe Uribe
Daniela Arias-G
Pamela Cabedo
Michael Handford
author_facet María Paz Covarrubias
Felipe Uribe
Daniela Arias-G
Pamela Cabedo
Michael Handford
author_sort María Paz Covarrubias
collection DOAJ
description IntroductionLipoic acid (LA) is a key, yet overlooked player in primary metabolism, due to its role as a cofactor for various multi enzymatic complexes such as the E2 subunits of pyruvate dehydrogenase (PDH) and alpha-ketoglutarate dehydrogenase (kGDH). In recent years, this molecule has seen renewed interest given its strong antioxidant properties and its applications as a dietary supplement. The mechanisms behind the synthesis of LA in vivo have been elucidated, identifying lipoyl synthase (LIP1) as the key enzyme required for this process.MethodsTherefore, in this work, we used the fruit-specific polygalacturonase (PG) promoter to guide Solanum lycopersicum (tomato) LIP1 (SlLIP1) overexpression in stably transformed tomatoes.ResultsThe resulting plants presented higher transcript levels of SlLIP1 in a fruit-specific manner, accumulated more bound and unbound LA yet lacked major phenotypic defects at both the vegetative and reproductive growth stages. Furthermore, changes in the expression of genes related to LA synthesis were explored and a metabolomic study was carried out. Specific metabolite patterns were clearly distinguishable between untransformed and stably transformed lines. For instance, trehalose 6-phosphate, GABA and proline levels were generally higher, whilst glucose 6-phosphate and UDP-glucose levels were lower in fruits of the SlLIP1 transformants.DiscussionIn addition, as the overexpression of SlLIP1 results in lower transcript levels of E2 PDH and E2 kGDH, and enhanced amounts of LA-bound targets, we speculate that the proportion of unlipoylated E2 subunits of PDH and kGDH may have decreased. This work could assist in obtaining crops with a higher LA content and therefore improved health benefits.
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spelling doaj-art-8664ca16e5624f15bebf43bca19dfc962025-08-20T01:52:14ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-05-011610.3389/fpls.2025.15450111545011Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruitsMaría Paz CovarrubiasFelipe UribeDaniela Arias-GPamela CabedoMichael HandfordIntroductionLipoic acid (LA) is a key, yet overlooked player in primary metabolism, due to its role as a cofactor for various multi enzymatic complexes such as the E2 subunits of pyruvate dehydrogenase (PDH) and alpha-ketoglutarate dehydrogenase (kGDH). In recent years, this molecule has seen renewed interest given its strong antioxidant properties and its applications as a dietary supplement. The mechanisms behind the synthesis of LA in vivo have been elucidated, identifying lipoyl synthase (LIP1) as the key enzyme required for this process.MethodsTherefore, in this work, we used the fruit-specific polygalacturonase (PG) promoter to guide Solanum lycopersicum (tomato) LIP1 (SlLIP1) overexpression in stably transformed tomatoes.ResultsThe resulting plants presented higher transcript levels of SlLIP1 in a fruit-specific manner, accumulated more bound and unbound LA yet lacked major phenotypic defects at both the vegetative and reproductive growth stages. Furthermore, changes in the expression of genes related to LA synthesis were explored and a metabolomic study was carried out. Specific metabolite patterns were clearly distinguishable between untransformed and stably transformed lines. For instance, trehalose 6-phosphate, GABA and proline levels were generally higher, whilst glucose 6-phosphate and UDP-glucose levels were lower in fruits of the SlLIP1 transformants.DiscussionIn addition, as the overexpression of SlLIP1 results in lower transcript levels of E2 PDH and E2 kGDH, and enhanced amounts of LA-bound targets, we speculate that the proportion of unlipoylated E2 subunits of PDH and kGDH may have decreased. This work could assist in obtaining crops with a higher LA content and therefore improved health benefits.https://www.frontiersin.org/articles/10.3389/fpls.2025.1545011/fullantioxidantlipoylationpolygalacturonase promoterSolanum lycopersicumTCA cycle
spellingShingle María Paz Covarrubias
Felipe Uribe
Daniela Arias-G
Pamela Cabedo
Michael Handford
Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
Frontiers in Plant Science
antioxidant
lipoylation
polygalacturonase promoter
Solanum lycopersicum
TCA cycle
title Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
title_full Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
title_fullStr Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
title_full_unstemmed Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
title_short Fruit-specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
title_sort fruit specific overexpression of lipoyl synthase increases both bound and unbound lipoic acid and alters the metabolome of tomato fruits
topic antioxidant
lipoylation
polygalacturonase promoter
Solanum lycopersicum
TCA cycle
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1545011/full
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