Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)

The genetic basis of type 1 red-flesh color development in apple (Malus domestica) depends upon a particular allele of the MdMYB10 gene. Interestingly, type 1 red-flesh apples are fully red after fruit set, but anthocyanin pigmentation in apple fruit cortex may decrease during fruit growth and matur...

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Main Authors: Pierre Bouillon, Etienne Belin, Anne-Laure Fanciullino, Sandrine Balzergue, Sylvain Hanteville, Yao Letekoma, Maryline Cournol, Fatima Faris, Andréa Bouanich, Dimitri Bréard, Frédéric Bernard, Jean-Marc Celton
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1462545/full
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author Pierre Bouillon
Pierre Bouillon
Etienne Belin
Anne-Laure Fanciullino
Sandrine Balzergue
Sandrine Balzergue
Sylvain Hanteville
Yao Letekoma
Maryline Cournol
Fatima Faris
Andréa Bouanich
Dimitri Bréard
Frédéric Bernard
Jean-Marc Celton
author_facet Pierre Bouillon
Pierre Bouillon
Etienne Belin
Anne-Laure Fanciullino
Sandrine Balzergue
Sandrine Balzergue
Sylvain Hanteville
Yao Letekoma
Maryline Cournol
Fatima Faris
Andréa Bouanich
Dimitri Bréard
Frédéric Bernard
Jean-Marc Celton
author_sort Pierre Bouillon
collection DOAJ
description The genetic basis of type 1 red-flesh color development in apple (Malus domestica) depends upon a particular allele of the MdMYB10 gene. Interestingly, type 1 red-flesh apples are fully red after fruit set, but anthocyanin pigmentation in apple fruit cortex may decrease during fruit growth and maturation, leading to variable red patterning and intensities in the mature cortical flesh. We developed a histogram-based color analysis method to quantitatively estimate pigmentation patterns. This methodology was applied to investigate the phenotypic diversity in four hybrid F1 families segregating for red-flesh color. Pigmentation patterns were found to be heritable allowing the identification of a new locus by QTL analysis. To further investigate the mechanisms involved in the spatial deposition of anthocyanin, metabolome, transcriptome and methylome comparisons between white and red flesh areas within the red-flesh genotype cv. ‘R201’ exhibiting flesh pigmentation patterns, was performed. Wide-targeted analysis showed that white-flesh areas accumulate more dihydrochalcones and hydroxycinnamic acids than red-flesh areas while red-flesh areas accumulate more flavonoids. Anthocyanin biosynthesis genes and anthocyanin positive regulators (MBW complex) were up-regulated in red-flesh areas, while a reduction in anthocyanin storage, transport and stability (increase of pH, down-regulation of MdGSTU22) and an increase in phenolic catabolism were concomitant with color fading process in white-flesh areas. Expression of MdGSTU22 was linked to a differentially methylated region (DMR) suggesting a potential environmental effect on the epigenetic control of gene expression involved in color fading. Altogether, these results provide the first characterization and functional identification of color fading in apple fruit flesh.
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issn 1664-462X
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publisher Frontiers Media S.A.
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spelling doaj-art-cbaf38775cb04d10905356b8896428582025-01-13T06:10:16ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.14625451462545Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)Pierre Bouillon0Pierre Bouillon1Etienne Belin2Anne-Laure Fanciullino3Sandrine Balzergue4Sandrine Balzergue5Sylvain Hanteville6Yao Letekoma7Maryline Cournol8Fatima Faris9Andréa Bouanich10Dimitri Bréard11Frédéric Bernard12Jean-Marc Celton13Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceIFO, Seiches sur le Loir, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceAnalyses des Acides Nucléiques (ANAN), SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceUniv Angers, Substances d’Origine Naturelle et Analogues Structuraux (SONAS), SFR QUASAV, Angers, FranceIFO, Seiches sur le Loir, FranceUniv Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, FranceThe genetic basis of type 1 red-flesh color development in apple (Malus domestica) depends upon a particular allele of the MdMYB10 gene. Interestingly, type 1 red-flesh apples are fully red after fruit set, but anthocyanin pigmentation in apple fruit cortex may decrease during fruit growth and maturation, leading to variable red patterning and intensities in the mature cortical flesh. We developed a histogram-based color analysis method to quantitatively estimate pigmentation patterns. This methodology was applied to investigate the phenotypic diversity in four hybrid F1 families segregating for red-flesh color. Pigmentation patterns were found to be heritable allowing the identification of a new locus by QTL analysis. To further investigate the mechanisms involved in the spatial deposition of anthocyanin, metabolome, transcriptome and methylome comparisons between white and red flesh areas within the red-flesh genotype cv. ‘R201’ exhibiting flesh pigmentation patterns, was performed. Wide-targeted analysis showed that white-flesh areas accumulate more dihydrochalcones and hydroxycinnamic acids than red-flesh areas while red-flesh areas accumulate more flavonoids. Anthocyanin biosynthesis genes and anthocyanin positive regulators (MBW complex) were up-regulated in red-flesh areas, while a reduction in anthocyanin storage, transport and stability (increase of pH, down-regulation of MdGSTU22) and an increase in phenolic catabolism were concomitant with color fading process in white-flesh areas. Expression of MdGSTU22 was linked to a differentially methylated region (DMR) suggesting a potential environmental effect on the epigenetic control of gene expression involved in color fading. Altogether, these results provide the first characterization and functional identification of color fading in apple fruit flesh.https://www.frontiersin.org/articles/10.3389/fpls.2024.1462545/fullred-flesh appleMalus domesticaanthocyaninpigmentation patternapple genetics
spellingShingle Pierre Bouillon
Pierre Bouillon
Etienne Belin
Anne-Laure Fanciullino
Sandrine Balzergue
Sandrine Balzergue
Sylvain Hanteville
Yao Letekoma
Maryline Cournol
Fatima Faris
Andréa Bouanich
Dimitri Bréard
Frédéric Bernard
Jean-Marc Celton
Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
Frontiers in Plant Science
red-flesh apple
Malus domestica
anthocyanin
pigmentation pattern
apple genetics
title Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
title_full Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
title_fullStr Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
title_full_unstemmed Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
title_short Fade into you: genetic control of pigmentation patterns in red-flesh apple (Malus domestica)
title_sort fade into you genetic control of pigmentation patterns in red flesh apple malus domestica
topic red-flesh apple
Malus domestica
anthocyanin
pigmentation pattern
apple genetics
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1462545/full
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