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Circadian Rhythms in Floral Scent Emission.

Fenske MP, Imaizumi T - Front Plant Sci (2016)

Bottom Line: To successfully recruit pollinators, plants often release attractive floral scents at specific times of day to coincide with pollinator foraging.In addition, in P. hybrida, PhLHY directly represses ODO1 and several enzyme genes in the FVBP pathway during the morning as an important negative regulator of scent emission.These findings facilitate our understanding of the relationship between a molecular timekeeper and the timing of scent emission, which may influence reproductive success.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle WA, USA.

ABSTRACT
To successfully recruit pollinators, plants often release attractive floral scents at specific times of day to coincide with pollinator foraging. This timing of scent emission is thought to be evolutionarily beneficial to maximize resource efficiency while attracting only useful pollinators. Temporal regulation of scent emission is tied to the activity of the specific metabolic pathways responsible for scent production. Although floral volatile profiling in various plants indicated a contribution by the circadian clock, the mechanisms by which the circadian clock regulates timing of floral scent emission remained elusive. Recent studies using two species in the Solanaceae family provided initial insight into molecular clock regulation of scent emission timing. In Petunia hybrida, the floral volatile benzenoid/phenylpropanoid (FVBP) pathway is the major metabolic pathway that produces floral volatiles. Three MYB-type transcription factors, ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), and EOBII, all of which show diurnal rhythms in mRNA expression, act as positive regulators for several enzyme genes in the FVBP pathway. Recently, in P. hybrida and Nicotiana attenuata, homologs of the Arabidopsis clock gene LATE ELONGATED HYPOCOTYL (LHY) have been shown to have a similar role in the circadian clock in these plants, and to also determine the timing of scent emission. In addition, in P. hybrida, PhLHY directly represses ODO1 and several enzyme genes in the FVBP pathway during the morning as an important negative regulator of scent emission. These findings facilitate our understanding of the relationship between a molecular timekeeper and the timing of scent emission, which may influence reproductive success.

No MeSH data available.


Temporal regulation of the floral volatile benzenoid/phenylpropanoid (FVBP) pathway in petunia. The FVBP pathway is the primary metabolic pathway of petunia for scent production. The FVBP pathway is composed of a series of enzymes (shown in blue ovals), which includes 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), chorismate mutase 1 (CM1), arogenate dehydratase (ADT), phenylalanine ammonia-lyase (PAL), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), S-adenosyl-L-methionine:benzoic acid/salicylic acid carboxyl methyltransferase (BSMT), and cinnamate 4-hydroxylase (C4H). These enzymes modify products of the Calvin cycle into volatile scents that are emitted by the flowers (volatile products shown in pink). Solid lines in the FVBP pathway represent single enzymatic steps, while dotted lines represent multiple steps. Representative daily mRNA expression patterns are drawn for selected genes. The relationship between LATE ELONGATED HYPOCOTYL (LHY) and GIGANTEA (GI) in the circadian oscillator was conceptualized based on knowledge obtained from Arabidopsis research and their expression patterns in petunia. Transcriptional regulators in the FVBP pathway are highlighted by yellow backgrounds, including ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), EOBII, and MYB4. Solid arrows connecting transcription factors to FVBP genes denote confirmation of direct molecular binding demonstrated by electrophoretic mobility shift assay (EMSA), yeast one-hybrid, and/or transient reporter assay; dashed lines lack this confirmation. EOBI may regulate the FVBP gene expression more directly (not through the regulation of ODO1). The general emission pattern of benzenoid compounds is shown in the bottom left-hand corner; this profile is synthesized based on daily scent emission profiles of four major benzenoids in Fenske et al. (2015).
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Figure 1: Temporal regulation of the floral volatile benzenoid/phenylpropanoid (FVBP) pathway in petunia. The FVBP pathway is the primary metabolic pathway of petunia for scent production. The FVBP pathway is composed of a series of enzymes (shown in blue ovals), which includes 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), chorismate mutase 1 (CM1), arogenate dehydratase (ADT), phenylalanine ammonia-lyase (PAL), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), S-adenosyl-L-methionine:benzoic acid/salicylic acid carboxyl methyltransferase (BSMT), and cinnamate 4-hydroxylase (C4H). These enzymes modify products of the Calvin cycle into volatile scents that are emitted by the flowers (volatile products shown in pink). Solid lines in the FVBP pathway represent single enzymatic steps, while dotted lines represent multiple steps. Representative daily mRNA expression patterns are drawn for selected genes. The relationship between LATE ELONGATED HYPOCOTYL (LHY) and GIGANTEA (GI) in the circadian oscillator was conceptualized based on knowledge obtained from Arabidopsis research and their expression patterns in petunia. Transcriptional regulators in the FVBP pathway are highlighted by yellow backgrounds, including ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), EOBII, and MYB4. Solid arrows connecting transcription factors to FVBP genes denote confirmation of direct molecular binding demonstrated by electrophoretic mobility shift assay (EMSA), yeast one-hybrid, and/or transient reporter assay; dashed lines lack this confirmation. EOBI may regulate the FVBP gene expression more directly (not through the regulation of ODO1). The general emission pattern of benzenoid compounds is shown in the bottom left-hand corner; this profile is synthesized based on daily scent emission profiles of four major benzenoids in Fenske et al. (2015).

Mentions: Among the other FVBP enzyme genes in petunia, genes encoding 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), arogenate dehydratase (ADT), chorismate mutase 1 (CM1), eugenol synthase (EGS), isoeugenol synthase (IGS), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), and S-adenosylmethionine synthetase (SAMS) also exhibit robust diurnal oscillations in their expression (Verdonk et al., 2005; Fenske et al., 2015) (Figure 1), though most show only weak oscillations in continuous dark (none do in continuous light). At least in P. hybrida, it appears likely that robust scent emission cycles are derived from the cumulative effect of the oscillatory expression of many FVBP genes in concert.


Circadian Rhythms in Floral Scent Emission.

Fenske MP, Imaizumi T - Front Plant Sci (2016)

Temporal regulation of the floral volatile benzenoid/phenylpropanoid (FVBP) pathway in petunia. The FVBP pathway is the primary metabolic pathway of petunia for scent production. The FVBP pathway is composed of a series of enzymes (shown in blue ovals), which includes 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), chorismate mutase 1 (CM1), arogenate dehydratase (ADT), phenylalanine ammonia-lyase (PAL), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), S-adenosyl-L-methionine:benzoic acid/salicylic acid carboxyl methyltransferase (BSMT), and cinnamate 4-hydroxylase (C4H). These enzymes modify products of the Calvin cycle into volatile scents that are emitted by the flowers (volatile products shown in pink). Solid lines in the FVBP pathway represent single enzymatic steps, while dotted lines represent multiple steps. Representative daily mRNA expression patterns are drawn for selected genes. The relationship between LATE ELONGATED HYPOCOTYL (LHY) and GIGANTEA (GI) in the circadian oscillator was conceptualized based on knowledge obtained from Arabidopsis research and their expression patterns in petunia. Transcriptional regulators in the FVBP pathway are highlighted by yellow backgrounds, including ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), EOBII, and MYB4. Solid arrows connecting transcription factors to FVBP genes denote confirmation of direct molecular binding demonstrated by electrophoretic mobility shift assay (EMSA), yeast one-hybrid, and/or transient reporter assay; dashed lines lack this confirmation. EOBI may regulate the FVBP gene expression more directly (not through the regulation of ODO1). The general emission pattern of benzenoid compounds is shown in the bottom left-hand corner; this profile is synthesized based on daily scent emission profiles of four major benzenoids in Fenske et al. (2015).
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Related In: Results  -  Collection

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Show All Figures
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Figure 1: Temporal regulation of the floral volatile benzenoid/phenylpropanoid (FVBP) pathway in petunia. The FVBP pathway is the primary metabolic pathway of petunia for scent production. The FVBP pathway is composed of a series of enzymes (shown in blue ovals), which includes 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), chorismate mutase 1 (CM1), arogenate dehydratase (ADT), phenylalanine ammonia-lyase (PAL), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), S-adenosyl-L-methionine:benzoic acid/salicylic acid carboxyl methyltransferase (BSMT), and cinnamate 4-hydroxylase (C4H). These enzymes modify products of the Calvin cycle into volatile scents that are emitted by the flowers (volatile products shown in pink). Solid lines in the FVBP pathway represent single enzymatic steps, while dotted lines represent multiple steps. Representative daily mRNA expression patterns are drawn for selected genes. The relationship between LATE ELONGATED HYPOCOTYL (LHY) and GIGANTEA (GI) in the circadian oscillator was conceptualized based on knowledge obtained from Arabidopsis research and their expression patterns in petunia. Transcriptional regulators in the FVBP pathway are highlighted by yellow backgrounds, including ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), EOBII, and MYB4. Solid arrows connecting transcription factors to FVBP genes denote confirmation of direct molecular binding demonstrated by electrophoretic mobility shift assay (EMSA), yeast one-hybrid, and/or transient reporter assay; dashed lines lack this confirmation. EOBI may regulate the FVBP gene expression more directly (not through the regulation of ODO1). The general emission pattern of benzenoid compounds is shown in the bottom left-hand corner; this profile is synthesized based on daily scent emission profiles of four major benzenoids in Fenske et al. (2015).
Mentions: Among the other FVBP enzyme genes in petunia, genes encoding 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), arogenate dehydratase (ADT), chorismate mutase 1 (CM1), eugenol synthase (EGS), isoeugenol synthase (IGS), 3-ketoacyl-CoA thiolase (KAT1), benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT), and S-adenosylmethionine synthetase (SAMS) also exhibit robust diurnal oscillations in their expression (Verdonk et al., 2005; Fenske et al., 2015) (Figure 1), though most show only weak oscillations in continuous dark (none do in continuous light). At least in P. hybrida, it appears likely that robust scent emission cycles are derived from the cumulative effect of the oscillatory expression of many FVBP genes in concert.

Bottom Line: To successfully recruit pollinators, plants often release attractive floral scents at specific times of day to coincide with pollinator foraging.In addition, in P. hybrida, PhLHY directly represses ODO1 and several enzyme genes in the FVBP pathway during the morning as an important negative regulator of scent emission.These findings facilitate our understanding of the relationship between a molecular timekeeper and the timing of scent emission, which may influence reproductive success.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Washington, Seattle WA, USA.

ABSTRACT
To successfully recruit pollinators, plants often release attractive floral scents at specific times of day to coincide with pollinator foraging. This timing of scent emission is thought to be evolutionarily beneficial to maximize resource efficiency while attracting only useful pollinators. Temporal regulation of scent emission is tied to the activity of the specific metabolic pathways responsible for scent production. Although floral volatile profiling in various plants indicated a contribution by the circadian clock, the mechanisms by which the circadian clock regulates timing of floral scent emission remained elusive. Recent studies using two species in the Solanaceae family provided initial insight into molecular clock regulation of scent emission timing. In Petunia hybrida, the floral volatile benzenoid/phenylpropanoid (FVBP) pathway is the major metabolic pathway that produces floral volatiles. Three MYB-type transcription factors, ODORANT 1 (ODO1), EMISSION OF BENZENOIDS I (EOBI), and EOBII, all of which show diurnal rhythms in mRNA expression, act as positive regulators for several enzyme genes in the FVBP pathway. Recently, in P. hybrida and Nicotiana attenuata, homologs of the Arabidopsis clock gene LATE ELONGATED HYPOCOTYL (LHY) have been shown to have a similar role in the circadian clock in these plants, and to also determine the timing of scent emission. In addition, in P. hybrida, PhLHY directly represses ODO1 and several enzyme genes in the FVBP pathway during the morning as an important negative regulator of scent emission. These findings facilitate our understanding of the relationship between a molecular timekeeper and the timing of scent emission, which may influence reproductive success.

No MeSH data available.