The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium

Vaccinium berries are regarded as “superfoods” owing to their high concentrations of anthocyanins, flavonoid metabolites that provide pigmentation and positively affect human health. Anthocyanin localization differs between the fruit of cultivated highbush blueberry (V. corymbosum) and wild bilberry...

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Main Authors: Declan J. Lafferty, Richard V. Espley, Cecilia H. Deng, Andrew P. Dare, Catrin S. Günther, Laura Jaakola, Katja Karppinen, Murray R. Boase, Lei Wang, Henry Luo, Andrew C. Allan, Nick W. Albert
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.910155/full
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author Declan J. Lafferty
Declan J. Lafferty
Richard V. Espley
Cecilia H. Deng
Andrew P. Dare
Catrin S. Günther
Laura Jaakola
Laura Jaakola
Katja Karppinen
Murray R. Boase
Lei Wang
Henry Luo
Andrew C. Allan
Andrew C. Allan
Nick W. Albert
author_facet Declan J. Lafferty
Declan J. Lafferty
Richard V. Espley
Cecilia H. Deng
Andrew P. Dare
Catrin S. Günther
Laura Jaakola
Laura Jaakola
Katja Karppinen
Murray R. Boase
Lei Wang
Henry Luo
Andrew C. Allan
Andrew C. Allan
Nick W. Albert
author_sort Declan J. Lafferty
collection DOAJ
description Vaccinium berries are regarded as “superfoods” owing to their high concentrations of anthocyanins, flavonoid metabolites that provide pigmentation and positively affect human health. Anthocyanin localization differs between the fruit of cultivated highbush blueberry (V. corymbosum) and wild bilberry (V. myrtillus), with the latter having deep red flesh coloration. Analysis of comparative transcriptomics across a developmental series of blueberry and bilberry fruit skin and flesh identified candidate anthocyanin regulators responsible for this distinction. This included multiple activator and repressor transcription factors (TFs) that correlated strongly with anthocyanin production and had minimal expression in blueberry (non-pigmented) flesh. R2R3 MYB TFs appeared key to the presence and absence of anthocyanin-based pigmentation; MYBA1 and MYBPA1.1 co-activated the pathway while MYBC2.1 repressed it. Transient overexpression of MYBA1 in Nicotiana benthamiana strongly induced anthocyanins, but this was substantially reduced when co-infiltrated with MYBC2.1. Co-infiltration of MYBC2.1 with MYBA1 also reduced activation of DFR and UFGT, key anthocyanin biosynthesis genes, in promoter activation studies. We demonstrated that these TFs operate within a regulatory hierarchy where MYBA1 activated the promoters of MYBC2.1 and bHLH2. Stable overexpression of VcMYBA1 in blueberry elevated anthocyanin content in transgenic plants, indicating that MYBA1 is sufficient to upregulate the TF module and activate the pathway. Our findings identify TF activators and repressors that are hierarchically regulated by SG6 MYBA1, and fine-tune anthocyanin production in Vaccinium. The lack of this TF module in blueberry flesh results in an absence of anthocyanins.
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spelling doaj.art-d034883f3db04a52a72dfd67a9961d002022-12-22T03:32:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.910155910155The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in VacciniumDeclan J. Lafferty0Declan J. Lafferty1Richard V. Espley2Cecilia H. Deng3Andrew P. Dare4Catrin S. Günther5Laura Jaakola6Laura Jaakola7Katja Karppinen8Murray R. Boase9Lei Wang10Henry Luo11Andrew C. Allan12Andrew C. Allan13Nick W. Albert14The New Zealand Institute for Plant and Food Research Limited, Palmerston North, New ZealandSchool of Biological Sciences, The University of Auckland, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Auckland, New ZealandDepartment of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, NorwayNorwegian Institute of Bioeconomy Research (NIBIO), Tromsø, NorwayDepartment of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, NorwayThe New Zealand Institute for Plant and Food Research Limited, Palmerston North, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North, New ZealandSchool of Biological Sciences, The University of Auckland, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Auckland, New ZealandThe New Zealand Institute for Plant and Food Research Limited, Palmerston North, New ZealandVaccinium berries are regarded as “superfoods” owing to their high concentrations of anthocyanins, flavonoid metabolites that provide pigmentation and positively affect human health. Anthocyanin localization differs between the fruit of cultivated highbush blueberry (V. corymbosum) and wild bilberry (V. myrtillus), with the latter having deep red flesh coloration. Analysis of comparative transcriptomics across a developmental series of blueberry and bilberry fruit skin and flesh identified candidate anthocyanin regulators responsible for this distinction. This included multiple activator and repressor transcription factors (TFs) that correlated strongly with anthocyanin production and had minimal expression in blueberry (non-pigmented) flesh. R2R3 MYB TFs appeared key to the presence and absence of anthocyanin-based pigmentation; MYBA1 and MYBPA1.1 co-activated the pathway while MYBC2.1 repressed it. Transient overexpression of MYBA1 in Nicotiana benthamiana strongly induced anthocyanins, but this was substantially reduced when co-infiltrated with MYBC2.1. Co-infiltration of MYBC2.1 with MYBA1 also reduced activation of DFR and UFGT, key anthocyanin biosynthesis genes, in promoter activation studies. We demonstrated that these TFs operate within a regulatory hierarchy where MYBA1 activated the promoters of MYBC2.1 and bHLH2. Stable overexpression of VcMYBA1 in blueberry elevated anthocyanin content in transgenic plants, indicating that MYBA1 is sufficient to upregulate the TF module and activate the pathway. Our findings identify TF activators and repressors that are hierarchically regulated by SG6 MYBA1, and fine-tune anthocyanin production in Vaccinium. The lack of this TF module in blueberry flesh results in an absence of anthocyanins.https://www.frontiersin.org/articles/10.3389/fpls.2022.910155/fullanthocyaninproanthocyanidinMYBtranscription factorflavonoidberry
spellingShingle Declan J. Lafferty
Declan J. Lafferty
Richard V. Espley
Cecilia H. Deng
Andrew P. Dare
Catrin S. Günther
Laura Jaakola
Laura Jaakola
Katja Karppinen
Murray R. Boase
Lei Wang
Henry Luo
Andrew C. Allan
Andrew C. Allan
Nick W. Albert
The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
Frontiers in Plant Science
anthocyanin
proanthocyanidin
MYB
transcription factor
flavonoid
berry
title The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
title_full The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
title_fullStr The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
title_full_unstemmed The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
title_short The Coordinated Action of MYB Activators and Repressors Controls Proanthocyanidin and Anthocyanin Biosynthesis in Vaccinium
title_sort coordinated action of myb activators and repressors controls proanthocyanidin and anthocyanin biosynthesis in vaccinium
topic anthocyanin
proanthocyanidin
MYB
transcription factor
flavonoid
berry
url https://www.frontiersin.org/articles/10.3389/fpls.2022.910155/full
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