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Circadian Clock Gene LATE ELONGATED HYPOCOTYL Directly Regulates the Timing of Floral Scent Emission in Petunia

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Circadian Clock Gene LATE ELONGATED HYPOCOTYL Directly Regulates the Timing of Floral Scent Emission in Petunia Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia Myles P. Fenske1, Kristen D. Hewett Hazelton1, Andrew K. Hempton1, Jae Sung Shim, Breanne M. Yamamoto, Jeffrey A. Riffell, and Takato Imaizumi2 Department of Biology, University of Washington, Seattle, WA 98195-1800 Edited by Steve A. Kay, University of Southern California, Los Angeles, CA, and approved June 1, 2015 (received for review December 1, 2014) Flowers present a complex display of signals to attract pollinators, (9). Floral scent in Petunia is dominated by volatile benzenoid/ including the emission of floral volatiles. Volatile emission is highly phenylpropanoids (FVBP), a group of organic compounds regulated, and many species restrict emissions to specific times originally derived from phenylalanine (5). FVBP emission relies of the day. This rhythmic emission of scent is regulated by the on the availability of precursor compounds that flow from enzy- circadian clock; however, the mechanisms have remained un- matic reactions in the shikimate pathway and later throughout the known. In Petunia hybrida, volatile emissions are dominated by FVBP metabolic pathways (Fig. 1A). ODORANT1 (ODO1), a products of the floral volatile benzenoid/phenylpropanoid (FVBP) transcriptional activator gene of FVBP gene expression, exhibits a metabolic pathway. Here we demonstrate that the circadian clock daily oscillatory expression with an evening peak (10). By binding gene P. hybrida LATE ELONGATED HYPOCOTYL (LHY; PhLHY) reg- to the promoters of several key enzymes, such as 5-enolpyruvyl- ulates the daily expression patterns of the FVBP pathway genes shikimate 3-phosphate synthase (EPSPS), ODO1 facilitates the and floral volatile production. PhLHY expression peaks in the introduction of precursor molecules to the FVBP synthesis path- morning, antiphasic to the expression of P. hybrida GIGANTEA way, suggesting that ODO1 is a master regulator of FVBP emis- (PhGI), the master scent regulator ODORANT1 (ODO1), and many sions in Petunia. Two transcription factors, EMISSION OF other evening-expressed FVBP genes. Overexpression phenotypes BENZENOIDS I (EOB I) and EOBII, up-regulate the expres- of PhLHY in Arabidopsis caused an arrhythmic clock phenotype, sion of ODO1 and other FVBP-related genes (11, 12). which resembles those of LHY overexpressors. In Petunia, consti- Analysis of the ODO1 promoter (12), as well as the promoters of tutive expression of PhLHY depressed the expression levels of several other regulatory genes in the FVBP pathway, revealed the PhGI, ODO1, evening-expressed FVBP pathway genes, and FVBP presence of specific cis-elements referred to as evening elements emission in flowers. Additionally, in the Petunia lines in which (EEs). The EE is a binding site for two similar circadian-clock PhLHY expression was reduced, the timing of peak expression of transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 PhGI, ODO1, and the FVBP pathway genes advanced to the morn- (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), and a ing. Moreover, PhLHY protein binds to cis-regulatory elements related factor, REVEILLE 8, in Arabidopsis (13). CCA1 and LHY, called evening elements that exist in promoters of ODO1 and which are highly expressed during the morning, function as repressors other FVBP genes. Thus, our results imply that PhLHY directly sets for evening expressed genes (14, 15) and activators for morning the timing of floral volatile emission by restricting the expression expressed genes (16). Thus, we hypothesized that the Petunia of ODO1 and other FVBP genes to the evening in Petunia. ortholog of CCA1/LHY, through the repression of ODO1 and several circadian rhythm | floral volatile | benzenoids | Petunia hybrida | LHY Significance lant development and physiology are extensively influenced Flowering plants attract pollinators in part by emitting volatile Pby the circadian clock (1). The precise timing of a single plant scents from their petals. This emission of scent is highly regu- behavioral output often requires a suite of internal mechanisms lated, and is often restricted to a specific portion of the day. to occur in coincidence or in quick succession before the be- Although the biochemical pathways of scent production are havior taking place. Transcriptome analysis revealed that the well characterized, little is known of their transcriptional reg- circadian clock controls transcription of one third of genes in ulation. Here we describe a direct molecular link between the Arabidopsis (2). In this way, the clock can exert a holistic effect circadian clock and floral volatile emissions. We find that a on a complex mechanism at a precise moment in time. The ef- clock transcription factor regulates the timing of multiple fectiveness of the clock’s ability to coordinate complex behaviors genes involved in the production of floral volatiles in Petunia. has been used by many aspects of plant physiology, such as This work provides key insights into the complex yet relatively photosynthesis, stem and leaf growth, and flowering (3, 4). unexplored transcriptional regulation of scent production, and The precise timing of sexual reproductive events is critical, as also sheds light on how the circadian clock can regulate the plants are sessile and individuals are often spread over large timing of large metabolic pathways. distances. In addition to regulating the timing of flower formation, Author contributions: M.P.F., K.D.H.H., A.K.H., J.A.R., and T.I. designed research; M.P.F., when they have opened, many flowers emit floral scents to lure K.D.H.H., A.K.H., J.S.S., and B.M.Y. performed research; M.P.F., K.D.H.H., A.K.H., J.S.S., and pollinators. Attractive floral volatiles are often emitted in a rhythmic B.M.Y. analyzed data; and M.P.F., K.D.H.H., A.K.H., J.A.R., and T.I. wrote the paper. fashion, with peaks of emission coinciding with the primary polli- The authors declare no conflict of interest. ’ nator s period of activity (5). Although studies have shown that This article is a PNAS Direct Submission. rhythmic emission of scent requires the influence of a circadian Data deposition: The sequence reported in this paper has been deposited in the GenBank clock (6–8), no study of which we are aware has shown a mecha- database (accession no. KP017483). nistic link between clock function and floral volatile production. 1M.P.F., K.D.H.H., and A.K.H. contributed equally to this work. Research on floral volatile synthesis has often used the com- 2To whom correspondence should be addressed. Email: [email protected]. mon garden petunia, Petunia hybrida cv. Mitchell, which exhibits This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. PLANT BIOLOGY white flowers that peak in scent emission in the middle of night 1073/pnas.1422875112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1422875112 PNAS | August 4, 2015 | vol. 112 | no. 31 | 9775–9780 Downloaded by guest on September 23, 2021 other regulatory genes, might restrict the emission of floral volatiles A CALVIN CYCLE shikimate 5-enolpyruvate- chorismate to the evening. Increasing levels of CCA1/LHY in the morning re- EPSPS shikimate- CM1 3-phosphate presses the expression of genes necessary for volatile synthesis, and as PHENYL EOBI ODO1 SHIKIMATE ODO1/EOBI/ the levels of CCA1/LHY decrease in the evening, it facilitates the PROPANOID EOBII L -arogenate PATHWAY EOBII PATHWAY ADT induction of ODO1 and downstream FVBP enzyme gene expression. coniferyl trans- PAL cinnamic phenylalanine Here we report that the circadian clock regulates scent emission alcohol acid PAAS timing through the function of LHY ortholog in Petunia. CFAT BENZENOID phenylacetaldehyde EOBI/ coniferyl PATHWAY Results EOBII acetate 3-oxo-3-phenyl- IGS EGS *benzaldehyde propionyl-coA The Circadian Clock Regulates Volatile Emission and the Expression of KAT1 *isoeugenol *eugenol BPBT BPBT Enzyme Genes in the FVBP Pathway in the Dark. Previous work has benzyl alcohol benzoyl phenylethyl shown that daily light/dark transitions are the predominant cues *methyl benzoate benzoic acid CoA alcohol BSMT1/ *phenylethyl mediating temporal control of the major floral volatile, methyl BSMT2 *benzyl benzoate benzoate benzoate, in Petunia (17). However, emission of the terpenoid B D 10 compound β-ionone and the expression of its synthase enzyme 60 methyl benzoate 60 methyl benzoate (emitted) (emitted) showed circadian oscillations, particularly in the dark (8), indi- 40 5 40 cating that the influence of the circadian clock on scent emission 20 20 0 can be conditional. To more comprehensively assess the involve- CE0 0 ment of the circadian clock in scent emission, we measured the 5 benzyl benzoate 6 1 benzyl benzoate 4 (emitted) (emitted) emission of four major floral volatiles (methyl benzoate, benzyl 3 4 0.5 benzoate, benzaldehyde, and isoeugenol) generated through the µg/g fresh weight/hr 2 2 0 FVBP pathway (Fig. 1A) under continuous light and dark condi- 1 36 48 60 72 84 tions (Fig. 1 B–E and Fig. S1 A–D). In continuous light, volatile 0 0 0122436486072 0 12 24 36 48 60 72 84 96 emissions ceased to oscillate, and moderate levels of emission Time (hours) Time (hours) F K were maintained for all four analyzed volatiles for 3 d (Fig. 1 B 4 ODO1 3 ODO1 and C and Fig. S1 A and B). In continuous dark, volatile peak 3 2 strength diminished rapidly (Fig. 1 D and E and Fig. S1 C and D); 2 however, smaller peaks (of approximately one tenth of the size of 1 1 the peaks that occurred in the light/dark conditions) were seen for G 0 L 0 3 EPSPS 3 EPSPS all volatiles examined in the two following subjective nights, in- dicating the presence of circadian timing mechanisms in the dark. 2 2 ) Our current understanding of the transcriptional regulation of 1 1 the FVBP pathway is limited to a few transcription factors: ODO1, UBQ 0 0 EOBI, and EOBII (10–12).
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