A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning

Maor Battat, Asa Eitan, Ilana Rogachev, Kati Hanhineva, Alisdair Fernie, Takayuki Tohge, Jules Beekwilder, Asaph Aharoni

Research output: Contribution to journalArticleAcademicpeer-review

3 Citations (Scopus)

Abstract

The pollen wall is a complex, durable structure essential for plant reproduction. A substantial portion of phenylpropanoids (e.g. flavonols) produced by pollen grain tapetal cells are deposited in the pollen wall. Transcriptional regulation of pollen wall formation has been studied extensively, and a specific regulatory mechanism for Arabidopsis (Arabidopsis thaliana) pollen flavonol biosynthesis has been postulated. Here, metabolome and transcriptome analyses of anthers from mutant and overexpression genotypes revealed that Arabidopsis MYB99, a putative ortholog of the petunia (Petunia hybrida) floral scent regulator ODORANT1 (ODO1), controls the exclusive production of tapetum diglycosylated flavonols and hydroxycinnamic acid amides. We discovered that MYB99 acts in a regulatory triad with MYB21 and MYB24, orthologs of emission of benzenoids I and II, which together with ODO1 coregulate petunia scent biosynthesis genes. Furthermore, promoter-activation assays showed that MYB99 directs precursor supply from the Calvin cycle and oxidative pentose-phosphate pathway in primary metabolism to phenylpropanoid biosynthesis by controlling TRANSKETOLASE2 expression. We provide a model depicting the relationship between the Arabidopsis MYB triad and structural genes from primary and phenylpropanoid metabolism and compare this mechanism with petunia scent control. The discovery of orthologous protein triads producing related secondary metabolites suggests that analogous regulatory modules exist in other plants and act to regulate various branches of the intricate phenylpropanoid pathway.

LanguageEnglish
Pages87-108
Number of pages22
JournalPlant Physiology
Volume180
Issue number1
DOIs
Publication statusPublished - 1 May 2019

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Petunia
phenylpropanoids
Pollen
Arabidopsis
pollen
metabolites
flavonols
Flavonols
odors
biosynthesis
Plant Structures
Coumaric Acids
metabolome
Pentose Phosphate Pathway
plant reproduction
Petunia hybrida
metabolism
Metabolome
pentoses
Calvin cycle

Cite this

Battat, M., Eitan, A., Rogachev, I., Hanhineva, K., Fernie, A., Tohge, T., ... Aharoni, A. (2019). A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning. Plant Physiology, 180(1), 87-108. https://doi.org/10.1104/pp.19.00009
Battat, Maor ; Eitan, Asa ; Rogachev, Ilana ; Hanhineva, Kati ; Fernie, Alisdair ; Tohge, Takayuki ; Beekwilder, Jules ; Aharoni, Asaph. / A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning. In: Plant Physiology. 2019 ; Vol. 180, No. 1. pp. 87-108.
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abstract = "The pollen wall is a complex, durable structure essential for plant reproduction. A substantial portion of phenylpropanoids (e.g. flavonols) produced by pollen grain tapetal cells are deposited in the pollen wall. Transcriptional regulation of pollen wall formation has been studied extensively, and a specific regulatory mechanism for Arabidopsis (Arabidopsis thaliana) pollen flavonol biosynthesis has been postulated. Here, metabolome and transcriptome analyses of anthers from mutant and overexpression genotypes revealed that Arabidopsis MYB99, a putative ortholog of the petunia (Petunia hybrida) floral scent regulator ODORANT1 (ODO1), controls the exclusive production of tapetum diglycosylated flavonols and hydroxycinnamic acid amides. We discovered that MYB99 acts in a regulatory triad with MYB21 and MYB24, orthologs of emission of benzenoids I and II, which together with ODO1 coregulate petunia scent biosynthesis genes. Furthermore, promoter-activation assays showed that MYB99 directs precursor supply from the Calvin cycle and oxidative pentose-phosphate pathway in primary metabolism to phenylpropanoid biosynthesis by controlling TRANSKETOLASE2 expression. We provide a model depicting the relationship between the Arabidopsis MYB triad and structural genes from primary and phenylpropanoid metabolism and compare this mechanism with petunia scent control. The discovery of orthologous protein triads producing related secondary metabolites suggests that analogous regulatory modules exist in other plants and act to regulate various branches of the intricate phenylpropanoid pathway.",
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Battat, M, Eitan, A, Rogachev, I, Hanhineva, K, Fernie, A, Tohge, T, Beekwilder, J & Aharoni, A 2019, 'A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning', Plant Physiology, vol. 180, no. 1, pp. 87-108. https://doi.org/10.1104/pp.19.00009

A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning. / Battat, Maor; Eitan, Asa; Rogachev, Ilana; Hanhineva, Kati; Fernie, Alisdair; Tohge, Takayuki; Beekwilder, Jules; Aharoni, Asaph.

In: Plant Physiology, Vol. 180, No. 1, 01.05.2019, p. 87-108.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Battat, Maor

AU - Eitan, Asa

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AU - Fernie, Alisdair

AU - Tohge, Takayuki

AU - Beekwilder, Jules

AU - Aharoni, Asaph

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AB - The pollen wall is a complex, durable structure essential for plant reproduction. A substantial portion of phenylpropanoids (e.g. flavonols) produced by pollen grain tapetal cells are deposited in the pollen wall. Transcriptional regulation of pollen wall formation has been studied extensively, and a specific regulatory mechanism for Arabidopsis (Arabidopsis thaliana) pollen flavonol biosynthesis has been postulated. Here, metabolome and transcriptome analyses of anthers from mutant and overexpression genotypes revealed that Arabidopsis MYB99, a putative ortholog of the petunia (Petunia hybrida) floral scent regulator ODORANT1 (ODO1), controls the exclusive production of tapetum diglycosylated flavonols and hydroxycinnamic acid amides. We discovered that MYB99 acts in a regulatory triad with MYB21 and MYB24, orthologs of emission of benzenoids I and II, which together with ODO1 coregulate petunia scent biosynthesis genes. Furthermore, promoter-activation assays showed that MYB99 directs precursor supply from the Calvin cycle and oxidative pentose-phosphate pathway in primary metabolism to phenylpropanoid biosynthesis by controlling TRANSKETOLASE2 expression. We provide a model depicting the relationship between the Arabidopsis MYB triad and structural genes from primary and phenylpropanoid metabolism and compare this mechanism with petunia scent control. The discovery of orthologous protein triads producing related secondary metabolites suggests that analogous regulatory modules exist in other plants and act to regulate various branches of the intricate phenylpropanoid pathway.

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Battat M, Eitan A, Rogachev I, Hanhineva K, Fernie A, Tohge T et al. A MYB Triad Controls Primary and Phenylpropanoid Metabolites for Pollen Coat Patterning. Plant Physiology. 2019 May 1;180(1):87-108. https://doi.org/10.1104/pp.19.00009