Natural selection on floral volatile production in<i><i>Penstemon digitalis</i></i>: Highlighting the role of linalool

Parachnowitsch, Amy L.; Burdon, Rosalie C. F.; Raguso, Robert A.; Kessler, André

doi:10.4161/psb.22704

Cited by 26 publications

(36 citation statements)

References 32 publications

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“…The genus Penstemon is becoming a model system for floral biology research, in part because of its diversity and multiple evolutionary transitions from bee to hummingbird pollination (Castellanos et al 2004;Wessinger et al 2014;Wilson et al 2007). Until recently, studies of scent in the genus Penstemon have been absent (Parachnowitsch et al 2012(Parachnowitsch et al , 2013. For beepollinated P. digitalis, Parachnowitsch et al (2012) found natural selection to increase floral scent emission rates in a common garden population, suggesting that scent plays an important role in Penstemon reproductive ecology.…”

Section: Introductionmentioning

confidence: 97%

Spatiotemporal Floral Scent Variation of Penstemon digitalis

et al. 2015

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Variability in floral volatile emissions can occur temporally through floral development, during diel cycles, as well as spatially within a flower. These spatiotemporal patterns are hypothesized to provide additional information to floral visitors, but they are rarely measured, and their attendant hypotheses are even more rarely tested. In Penstemon digitalis, a plant whose floral scent has been shown to be under strong phenotypic selection for seed fitness, we investigated spatiotemporal variation in floral scent by using dynamic headspace collection, respectively solid-phase microextraction, and analyzed the volatile samples by combined gas chromatography-mass spectrometry. Total volatile emission was greatest during flowering and peak pollinator activity hours, suggesting its importance in mediating ecological interactions. We also detected tissue and reward-specific compounds, consistent with the hypothesis that complexity in floral scent composition reflects several ecological functions. In particular, we found tissue-specific scents for the stigma, stamens, and staminode (a modified sterile stamen common to all Penstemons). Our findings emphasize the dynamic nature of floral scents and highlight a need for greater understanding of ecological and physiological mechanisms driving spatiotemporal patterns in scent production.

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Section: Introductionmentioning

confidence: 97%

Spatiotemporal Floral Scent Variation of Penstemon digitalis

et al. 2015

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“…Its two enantiomeric forms, due to the chirality of its hydroxylated carbon, occur in different proportions in floral extracts from distinct plant species (Dötterl et al, 2006a;Parachnowitsch et al, 2013). Various cyclic pyranoid or furanoid oxygenated derivatives are most often present along with linalool, such as the furanoid lilac compounds (Figure 1).…”

Section: Introductionmentioning

confidence: 99%

CYP76C1 (Cytochrome P450)-Mediated Linalool Metabolism and the Formation of Volatile and Soluble Linalool Oxides in Arabidopsis Flowers: A Strategy for Defense against Floral Antagonists

Boachon¹,

Junker²,

Miesch³

et al. 2015

Plant Cell

144

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The acyclic monoterpene alcohol linalool is one of the most frequently encountered volatile compounds in floral scents. Various linalool oxides are usually emitted along with linalool, some of which are cyclic, such as the furanoid lilac compounds. Recent work has revealed the coexistence of two flower-expressed linalool synthases that produce the (S)-or (R)-linalool enantiomers and the involvement of two P450 enzymes in the linalool oxidation in the flowers of Arabidopsis thaliana. Partially redundant enzymes may also contribute to floral linalool metabolism. Here, we provide evidence that CYP76C1 is a multifunctional enzyme that catalyzes a cascade of oxidation reactions and is the major linalool metabolizing oxygenase in Arabidopsis flowers. Based on the activity of the recombinant enzyme and mutant analyses, we demonstrate its prominent role in the formation of most of the linalool oxides identified in vivo, both as volatiles and soluble conjugated compounds, including 8-hydroxy, 8-oxo, and 8-COOH-linalool, as well as lilac aldehydes and alcohols. Analysis of insect behavior on CYP76C1 mutants and in response to linalool and its oxygenated derivatives demonstrates that CYP76C1-dependent modulation of linalool emission and production of linalool oxides contribute to reduced floral attraction and favor protection against visitors and pests.

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“…Linalool, another compound with a fragrance pleasant to the human nose, is one of the most common components of floral scents (Raguso and Pichersky 1999;Knudsen 2006;Kaiser 2010) suggesting its importance and versatility in flower/pollinator communication (Parachnowitsch et al 2013;Salzmann and Schiestl 2007). It can be present as a very minor component (and still show behavioural activity) in hawkmoth pollinated Datura wrightii Regel.…”

Section: Discussionmentioning

confidence: 99%

“…It can be present as a very minor component (and still show behavioural activity) in hawkmoth pollinated Datura wrightii Regel. (Riffell et al 2009), as a nectar odour in bee pollinated Penstemon flowers (under positive selection; see Parachnowitsch et al 2012Parachnowitsch et al , 2013, and as a dominant odour in the early spring flora (BorgKarlson et al 1994). Surprisingly, Parachnowitsch et al (2012Parachnowitsch et al ( , 2013 found that floral scent in weakly scented Penstemon digitalis Nutt.…”

Section: Discussionmentioning

confidence: 99%

“…(Riffell et al 2009), as a nectar odour in bee pollinated Penstemon flowers (under positive selection; see Parachnowitsch et al 2012Parachnowitsch et al , 2013, and as a dominant odour in the early spring flora (BorgKarlson et al 1994). Surprisingly, Parachnowitsch et al (2012Parachnowitsch et al ( , 2013 found that floral scent in weakly scented Penstemon digitalis Nutt. experienced stronger (directional) selection (promoting seed fitness) than did floral colour or size and suggested that reproductive success benefits from being strongly scented in this species.…”

Section: Discussionmentioning

confidence: 99%

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Floral fraudulence: Do blue Thelymitra species (Orchidaceae) mimic Orthrosanthus laxus (Iridaceae)?

Edens-Meier¹,

Raguso²,

Westhus³

et al. 2014

Telopea

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In Western Australia, Thelymitra crinita Lindl. and T. macrophylla Lindl. are pollinated by female, polylectic bees but offer no edible rewards. Flowers of Orthrosanthus laxus (Endl.) Benth. (Iridaceae) offer granular pollen and previous authorities suggest it is a Batesian model of T. crinita. We analyzed the floral fragrances and measured the floral dimensions of the orchid species, their putative hybrid, and O. laxus. Although the 'scentless' T. crinita emitted low levels of monoterpenoids and sesquiterpenoids, the pleasantly discernible fragrance of T. macrophylla was dominated by 2-phenylethanol. Their putative hybrid produced slightly lower levels of 2-phenylethanol compared with T. macrophylla and failed to produce any sesquiterpenoids associated with T. crinita. However, the hybrid produced higher volumes of the monoterpene linalool than either parent species. The fragrance of O. laxus contained 2-phenylethanol but lacked the sesquiterpenoids. We also measured perianth area and symmetry as well as the length and width of contrastingly pigmented floral centres for each taxon. Significant differences in floral area and symmetry were detected between the putative hybrid, the two parent species, and O. laxus. In contrast, the floral reward centre area (tuft of stamens) in O. laxus was significantly larger than the pseudo-reward centres (mitras) of both Thelymitra species and their hybrid. At the peak of their respective, but overlapping flowering periods, an inflorescence of T. macrophylla produced more than twice the number of open flowers as T. crinita and more than four times the number of open flowers on cymes of O. laxus. Based on scent production and visual displays, T. macrophylla appears more likely to be a Batesian floral mimic of O. laxus. We suggest that large-flowered Thelymitra species appear to produce a novel, visual and olfactory attractant pattern of fraudulence we call the 'New Again, More Again Effect' .

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Natural selection on floral volatile production inPenstemon digitalis: Highlighting the role of linalool

Cited by 26 publications

References 32 publications

Spatiotemporal Floral Scent Variation of Penstemon digitalis

Spatiotemporal Floral Scent Variation of Penstemon digitalis

CYP76C1 (Cytochrome P450)-Mediated Linalool Metabolism and the Formation of Volatile and Soluble Linalool Oxides in Arabidopsis Flowers: A Strategy for Defense against Floral Antagonists

Floral fraudulence: Do blue Thelymitra species (Orchidaceae) mimic Orthrosanthus laxus (Iridaceae)?

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