Floral volatiles: from biosynthesis to function.

Floral volatiles: from biosynthesis to function1

Accepted Article

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Joëlle K. Muhlemann, Antje Klempien, Natalia Dudareva

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Department of Biochemistry, Purdue University, 175 South University Street, West

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Lafayette, IN 47907, USA

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Author for correspondence:

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Natalia Dudareva

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Tel: +1 765 494 1325

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Email: [email protected]

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Keywords: floral scent; volatile organic compounds; terpenoids; phenylpropanoids;

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benzenoids; regulation; pollination; florivory

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This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/pce.12314 1 This article is protected by copyright. All rights reserved.

Accepted Article

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Abstract

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Floral volatiles have attracted humans’ attention since antiquity and have since

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then permeated many aspects of our lives. Indeed, they are heavily used in perfumes,

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cosmetics, flavorings and medicinal applications. However, their primary function is to

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mediate ecological interactions between flowers and a diverse array of visitors, including

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pollinators, florivores and pathogens. As such, they ultimately ensure the plants’

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reproductive and evolutionary success. To date, over 1,700 floral volatile organic

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compounds have been identified. Interestingly, they are derived from only a few

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biochemical networks, which include the terpenoid, phenylpropanoid/benzenoid and fatty

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acid biosynthetic pathways. These pathways are intricately regulated by endogenous

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and external factors to enable spatially and temporally controlled emission of floral

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volatiles, thereby fine-tuning the ecological interactions facilitated by floral volatiles. In

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this review, we will focus on describing the biosynthetic pathways leading to floral volatile

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organic compounds (VOCs), the regulation of floral volatile emission, as well as

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biological functions of emitted volatiles.

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Introduction Plants are sessile organisms that need to constantly adapt to changing

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environments for their survival and reproduction. For this environmental adaptation,

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plants have evolved a wide array of specialized metabolites, also called plant secondary

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metabolites or plant natural products. To date, over 200,000 specialized metabolites

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have been described (Dixon & Strack 2003), out of which approximately 1% corresponds

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to floral VOCs identified in 90 different angio- and gymnosperms families (Knudsen et al.

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2006). VOCs are lipophilic liquids with low molecular weight and high vapor pressure at

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ambient temperatures. Physical properties of these compounds allow them to freely

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cross cellular membranes and be released into the surrounding environment (Pichersky,

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Noel & Dudareva 2006). Biosynthesis of VOCs occurs in all plant organs: roots, stems,

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leaves, fruits, seeds, as well as flowers, which were found to release the highest

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amounts and diversity of VOCs. In contrast to VOCs released from other plant organs,

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which are exclusively involved in plant defense, floral VOCs assume functions in both

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attraction of pollinators and defense against florivores and pathogens. Based on their

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biosynthetic origin, floral VOCs can be divided into three major classes: terpenoids,

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phenylpropanoids/benzenoids, fatty acid derivatives (Fig. 1). In addition, sulfur- and

2 This article is protected by copyright. All rights reserved.

nitrogen-containing compounds contribute to the attraction of pollinators to flowers by

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mimicking food or brood sources such as carrion or dung (Wiens, 1978; Faegri & Van

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der Pijl, 1979; Juergens et al., 2006). However, to date little is known about the

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biosynthetic pathways leading to the formation of these compounds.

Accepted Article

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Biosynthetic Pathways and Genes Involved in the Formation of Floral Volatiles

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Biosynthesis of Terpenoid Compounds Terpenoids are the largest class of floral volatiles and encompass 556 scent

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compounds, which are derived from two common interconvertible five-carbon (C5)

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precursors, isopentenyl diphosphate (IPP) and its allylic isomer dimethylallyl diphosphate

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(DMAPP) (McGarvey & Croteau 1995). In plants, these C5-precursors are synthesized

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from two independent and compartmentally separated pathways, the mevalonic acid

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(MVA) and the methylerythritol-phosphate (MEP) pathways, which contribute to

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terpenoid biosynthesis in a species- and/or organ-specific manner (Vranova, Coman &

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Gruissem 2013). The MEP pathway operates in plastids (Hsieh et al. 2008) and is mainly

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responsible for the formation of volatile mono- (C10) and diterpenes (C20) (~53% and

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~1% of total floral terpenoids, respectively) (Knudsen & Gershenzon 2006), whereas the

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MVA pathway is distributed between the cytosol, endoplasmatic reticulum and

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peroxisomes (Simkin et al. 2011; Pulido, Perello & Rodriguez-Concepcion 2012) and

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gives rise to precursors for volatile sesquiterpenes (C15) (~28% of total floral terpenoids).

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While being compartmentally separated, these isoprenoid biosynthetic pathways are

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connected via a metabolic “crosstalk” mediated by yet unidentified transporter(s) (Bick &

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Lange 2003; Flügge & Gao 2005). Such connectivity of the pathways allows the MEP

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pathway, often with a higher carbon flux than the MVA route, to support biosynthesis of

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cytosolically formed terpenoids as was demonstrated in vegetative tissue (Laule et al.

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2003; Ward et al. 2011), fruits (Gutensohn, Nagegowda & Dudareva 2013) and flowers

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(Laule et al. 2003; Dudareva et al. 2005; Ward et al. 2011). Indeed, the MEP pathway

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alone supports sesquiterpene biosynthesis in snapdragon flowers (Dudareva et al. 2005).

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Terpenoid research in flowers has predominantly focused on the isolation and

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characterization of terpene synthase (TPS) genes responsible for the final steps in

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terpenoid biosynthesis, while genes and cognate enzymes of the MVA and MEP

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pathways were mainly characterized from vegetative tissues (Cane 1999; Wise &

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Croteau 1999; Lange et al. 2000; Rohdich et al. 2003; Guirimand et al. 2012) with 3 This article is protected by copyright. All rights reserved.

several excellent reviews were devoted to this subject (McGarvey & Croteau 1995;

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Chappell 2002; Vranova et al. 2013). In brief, the MVA pathway starts from a stepwise

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condensation of three molecules of acetyl-CoA and consists of six enzymatic reactions

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while the MEP pathway begins with the condensation of D-glyceraldehyde 3-phosphate

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and pyruvate and involves seven enzymatic reactions.

Accepted Article

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Volatile terpenoids are synthesized from prenyl diphosphate precursors, which

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are produced from condensation of IPP and DMAPP by prenyltransferases. Sequential

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head-to-tail condensation of two IPP and one DMAPP molecules by farnesyl

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diphosphate (FPP) synthase in the cytosol leads to the formation of FPP, the precursor

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for sesquiterpenes (Fig. 2). Head-to-tail condensation of one DMAPP with one IPP

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molecule in plastids results in GPP formation, the precursor of monoterpenes, and is

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catalyzed by the GPP synthase (Fig. 2). This enzyme was found to be heterodimeric

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in Antirrhinum majus (snapdragon) and Clarkia breweri, both of which have a floral scent

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bouquet rich in monoterpene compounds (Tholl et al. 2004). Analyses of tissue-specific,

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developmental, and rhythmic expression of the GPPS small subunit showed positive

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correlation between expression and monoterpene emission in snapdragon flowers (Tholl

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et al. 2004), whereas no such correlation was found for the large subunit, suggesting

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that the small subunit is responsible for the regulation of GPP and subsequently

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monoterpene formation. Interestingly, a homodimeric GPPS with dual prenyltransferase

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activity (GPP synthase and FPP synthase activities) was reported in the orchid

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Phalaenopsis bellina and demonstrated to be linked to the emission of linalool and

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geraniol (Hsiao et al. 2008).

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FPP and GPP serve as substrates for terpene synthases and cyclases (Cane

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1999; Wise & Croteau 1999), which in plants are responsible for the production of a vast

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variety of volatile terpenoid compounds (Fig. 2). TPSs are highly diversified throughout

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the plant kingdom and form a mid-size gene family (Bohlmann, Meyer-Gauen & Croteau

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1998; Chen et al. 2011a), which is comprised of more than 100 genes identified in a

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variety of plant species, with one-third being isolated from flowers or fruits. Almost half of

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the known TPSs are capable of synthesizing multiple products from a single prenyl

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diphosphate precursor (Degenhardt, Köllner & Gershenzon 2009). For instance, the

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floral volatile blend of Arabidopsis consists of 20 different sesquiterpenes, almost all of

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which are synthesized by only two sesquiterpene synthases, TPS11 and TPS21 (Tholl et

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al. 2005). The same is true for the flowers of kiwifruit (Actinidia deliciosa), where almost

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all the sesquiterpenes released from flowers are the products of either germacrene D 4 This article is protected by copyright. All rights reserved.

synthase1 (AdGDS1) or α-farnesene synthase1 (AdAFS1) (Nieuwenhuizen et al. 2009).

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In addition, some TPSs exhibit substrate promiscuity resulting in formation of different

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products. However, in the case of these TSPs their subcellular localization and the

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availability of a particular substrate determine the type of product formed (Tholl 2006;

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Nagegowda et al. 2008). In addition, the diversity of formed volatile terpenoids is not

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only dependent on TPSs, but is also increased by enzymes modifying TPS products by

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hydroxylation, dehydrogenation, and acylation, which enhance their volatility and

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olfactory properties (Dudareva, Pichersky & Gershenzon 2004).

Accepted Article

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To date, multiple flower-specific TPSs have been isolated and characterized (see

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Table 1). They were shown to be responsible for the formation of the monoterpenes

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linalool (Clarkia breweri, Antirrhinum majus, and Arabidopsis thaliana) (Dudareva et al.

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1996a; Nagegowda et al. 2008; Ginglinger et al. 2013), E-(β)-ocimene (Antirrhinum

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majus and Citrus unshiu) (Dudareva et al. 2003; Shimada et al. 2005), myrcene

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(Antirrhinum majus and Alstromeria peruviana) (Dudareva et al. 2003; Aros et al. 2012)

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and 1,8-cineole (Nicotiana suaveolens and Citrus unshiu) (Shimada et al. 2005; Roeder

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et al. 2007), as well as of the sesquiterpenes nerolidol (Antirrhinum majus and Actinidia

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chinensis) (Nagegowda et al. 2008; Green et al. 2012), α-farnesene (Actinidia deliciosa)

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(Nieuwenhuizen et al. 2009), germacrene D (Actinidia deliciosa, Rosa hybrid and Vitis

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vinifera) (Guterman et al. 2002; Lucker, Bowen & Bohlmann 2004; Nieuwenhuizen et al.

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2009) and valencene (Vitis vinifera) (Lucker et al. 2004).

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Besides mono- and sesquiterpenes, certain flowers also emit irregular terpenoids

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(C8 to C18). They constitute a minor class of floral terpenoids (~7% of all floral

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terpenoids), which are formed via a three-step modification including a dioxygenase

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cleavage, enzymatic transformation and acid-catalyzed conversion into volatile

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compounds (Winterhalter & Rouseff 2001). Interestingly, the dioxygenase cleavage step

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itself can already result in volatile products, such as α- and β-ionone, geranylacetone

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and pseudoionone, as was found to be the case in petunia flowers (Simkin et al. 2004).

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Biosynthesis of phenylpropanoid/benzenoid compounds Phenylpropanoids and benzenoids represent the second largest class of plant

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VOCs (Knudsen et al. 2006) and are exclusively derived from the aromatic amino acid

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phenylalanine (Phe) (Fig. 3), which is synthesized via two alternative pathways (Maeda

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et al. 2010; Maeda, Yoo & Dudareva 2011; Maeda & Dudareva 2012; Yoo et al. 2013).

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Depending on the structure of their carbon skeleton, this class is divided into three 5 This article is protected by copyright. All rights reserved.

subclasses: phenylpropanoids (with a C6-C3 backbone), benzenoids (C6-C1) and

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phenylpropanoid-related compounds (C6-C2).

Accepted Article

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Phenylpropanoid-related compounds originate directly from Phe and constitute

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approximately 24% of all described phenylpropanoid/benzenoid compounds (Knudsen &

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Gershenzon 2006). So far, only genes and enzymes involved in the biosynthesis of

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phenylacetaldehyde and 2-phenylethanol have been isolated and characterized

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(Kaminaga et al. 2006; Sakai et al. 2007; Farhi et al. 2010; Chen et al. 2011b;

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Gutensohn et al. 2011; Hirata et al. 2012) (Fig. 3). In petunia petals, phenylacetaldehyde

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is produced via an unusual combined decarboxylation-amine oxidation reaction

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catalyzed by phenylacetaldehyde synthase (Kaminaga et al. 2006). In roses, however, it

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is formed via two alternative routes: the first involves a phenylacetaldehyde synthase

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similar to the one described in petunia, while the second route employs Phe deamination

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by an aromatic amino acid aminotransferase followed by decarboxylation of the formed

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phenylpyruvate intermediate (Sakai et al. 2007; Farhi et al. 2010; Hirata et al. 2012).

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Further conversion of phenylacetaldehyde to 2-phenylethanol is catalyzed by a

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phenylacetaldehyde reductase as was shown in roses (Sakai et al. 2007; Chen et al.

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2011b).

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The first committed step in benzenoid (C6-C1) and phenylpropanoid (C6-C3)

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biosynthesis is catalyzed by a well-characterized and widely distributed enzyme, L-

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phenylalanine ammonia-lyase (PAL), which deaminates Phe to trans-cinnamic acid (CA)

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and competes with phenylacetaldehyde synthase for Phe utilization (Fig. 3). Benzenoid

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formation from CA involves shortening of the propyl-side chain by a C2 unit and was

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shown to proceed via a β-oxidative, a non-β-oxidative pathway or a combination of both

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(Boatright et al. 2004; Orlova et al. 2006) (Fig. 3). The β-oxidative pathway has only

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recently been fully elucidated in petunia flowers and appears to be analogous to fatty

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acid catabolism and is localized in peroxisomes. The pathway begins with an activation

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of CA to cinnamoyl-CoA, followed by hydration, oxidation and cleavage of the β-keto

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thioester with subsequent formation of benzoyl-CoA (Van Moerkercke et al. 2009;

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Klempien et al. 2012; Qualley et al. 2012). Benzaldehyde acts as the key intermediate in

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the alternative non-β-oxidative pathway and is oxidized to benzoic acid by a NAD+-

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dependent benzaldehyde dehydrogenase, which has been isolated and characterized

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from snapdragon flowers (Long et al. 2009). However, the enzymatic reactions leading to

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benzaldehyde formation remain unknown.


Accepted Article

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Formation of floral phenylpropanoids (C6-C3), including (iso)eugenol and

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methyl(iso)eugenol, shares the initial biosynthetic steps with the lignin biosynthetic

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pathway up to the coniferyl alcohol stage. This monolignol precursor then undergoes two

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enzymatic reactions that eliminate the oxygen functionality at the C9 position. The first

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reaction involves acetylation by an acyltransferase from the BAHD superfamily as was

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shown for the formation of coniferyl acetate from coniferyl alcohol in petunia petals

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(Dexter et al. 2007). Coniferyl acetate is then converted to the phenylpropanoids

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eugenol and isoeugenol by eugenol and isoeugenol synthases, respectively, which both

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belong to the PIP family of NADPH-dependent reductases (Koeduka et al. 2006;

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Koeduka et al. 2008) (Fig. 3).

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In flowers the diversity of phenylpropanoid/benzenoid compounds is further

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increased by modifications such as methylation, hydroxylation and acetylation of direct

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scent precursors. These modifications enhance the volatility or olfactory properties of

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scent compounds. Methylation reactions are catalyzed by either O-methyltransferases or

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carboxyl methyltransferases. O-methyltransferases were shown to be responsible for the

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synthesis of a diverse array of benzenoids/phenylpropanoids, including veratrole in

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Silene flowers (Akhtar & Pichersky ; Gupta et al. 2012), 3,5-dimethoxytoluene and 1,3,5-

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trimethoxybenzene in roses (Lavid et al. 2002; Scalliet et al. 2002), methyleugenol and

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isomethyleugenol in Clarkia (Wang & Pichersky 1998). Carboxyl methyltransferases,

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many of which belong to the SABATH family (D'Auria et al. 2003), are involved in the

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biosynthesis of volatile esters like methylbenzoate in snapdragon and petunia flowers

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(Murfitt et al. 2000; Negre et al. 2003) and methylsalicylate in Clarkia and petunia (Ross

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et al. 1999; Negre et al. 2003). Enzymes from the BAHD superfamily of acyltransferases

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(D'Auria 2006) were shown to be responsible for the biosynthesis of acetylated scent

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compounds such as benzylacetate in Clarkia (Dudareva et al. 1998), benzoylbenzoate in

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Clarkia and petunia (D'Auria, Chen & Pichersky 2002; Boatright et al. 2004; Orlova et al.

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2006) and phenylethylbenzoate in petunia flowers (Boatright et al. 2004; Orlova et al.

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2006).

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Biosynthesis of volatile fatty acid derivatives Fatty acid derivatives constitute the third class of flower VOCs, which derive from

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the unsaturated C18 fatty acids linolenic and linoleic acid. Biosynthesis of volatile fatty

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acid derivatives is initiated by a stereo-specific oxygenation of the octadecanoid

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precursors, catalyzed by a lipoxygenase (LOX) and leads to formation of 9- and 137 This article is protected by copyright. All rights reserved.

hydroperoxy intermediates (Schaller 2001; Feussner & Wasternack 2002). These

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intermediates can enter two different branches of the LOX pathway, which in turn leads

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to the formation of volatile compounds. Allene oxide synthase (AOS) exclusively utilizes

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the 13-hydroperoxy intermediate as substrate, converting it to an unstable epoxide,

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which is then subjected to a cyclization followed by a reduction and a series of

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cyclization reactions to yield jasmonic acid (JA). In contrast to the allene oxide synthase

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branch, hydroperoxide lyase can convert both types of hydroperoxide fatty acid

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derivatives into volatile C6 and C9 aldehydes. These saturated or unsaturated C6 and C9

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aldehydes are often substrates for alcohol dehydrogenases giving rise to volatile

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alcohols, which can be further converted to their esters. These C6 and C9 aldehydes and

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alcohols are commonly referred to as green leaf volatiles, as they are usually

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synthesized in vegetative tissues. However they are also important constituents in the

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floral volatile bouquet of several plant species such as carnation and wild snapdragon

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(Schade, Legge & Thompson 2001; Suchet et al. 2011).

Accepted Article

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The orchids of the genus Ophrys produce an array of fatty acid derived volatiles as

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well. Within their bouquet, alkenes are particularly important mediators in the interaction

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between orchids and their pollinators. Production of alkenes requires desaturation of

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fatty acids, a step that is likely mediated by acyl-acyl carrier protein (ACP) desaturases.

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Two isoforms of a stearoyl-acyl carrier protein (ACP) desaturase (SAD), namely SAD1

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and SAD2, were identified in Ophrys sphegodes and O. exaltata. However, only

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expression of SAD2 was positively correlated with the formation of alkenes in flowers

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(Schlüter et al. 2011). OsSAD2 is a functional desaturase capable of producing 18:1Δ9

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(ω-9) and 16:1Δ4 (ω-12) fatty acid intermediates from which 9-alkenes and 12-alkenes

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could be derived.

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Regulation of floral volatile emission

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Spatial, rhythmic and developmental regulation of floral scent emission Flowers have evolved many complex olfactory and visual guides for pollinator

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attraction. In order to maximize pollinator attraction, floral scent emission is often

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restricted to particular flower tissues and is developmentally and rhythmically regulated.

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Tissue-specific emission of floral VOCs is a characteristic feature of many

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species. In general, petals are the primary source of floral volatiles, although other

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tissues (stamens, pistils, sepals and nectaries) also contribute to the floral bouquet in 8 This article is protected by copyright. All rights reserved.

certain plant species (Dobson, Bergström & Groth 1990; Bergström, Dobson & Groth

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1995; Dobson, Groth & Bergström 1996; Flamini, Cioni & Morelli 2003; Dötterl & Jürgens

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2005; Farré-Armengol et al., 2013). Emitted from petals, VOCs often enable long-

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distance attraction of pollinators, while VOCs produced in nectaries or pollen signal

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availability of food sources. Tissue-specificity of scent emission is regulated at the level

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of scent biosynthetic gene expression and enzyme activity. Indeed, many of the scent

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biosynthetic genes isolated so far show a very specific expression profile, with the

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highest level found in the scent producing parts of the flower (see e.g. Dudareva et al.

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1996a; Murfitt et al. 2000; Dudareva et al. 2003; Negre et al. 2003; Nagegowda et al.

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2008; Rodriguez-Saona et al. 2011). Within scent-emitting tissues, formation of VOCs is

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often restricted to specific cell types or layers. In snapdragon flowers for example,

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biosynthesis of the major volatile benzenoid compound methyl benzoate is restricted to

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the inner epidermal layer of the upper and lower petal lobes (Kolosova et al. 2001b).

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Similar cell-specific expression of scent biosynthetic genes was also reported for roses

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and Clarkia breweri (Dudareva et al. 1996b; Bergougnoux et al. 2007).

Accepted Article

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Rhythmicity of floral scent emission has been shown to occur in numerous

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species and often correlates with the activity of the respective pollinators (see e.g.

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(Raguso et al. 2003; Dötterl, Wolfe & Jürgens 2005; Effmert et al. 2005; Hoballah et al.

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2005; Rodriguez-Saona et al. 2011). Rhythmic emission allows plants to conserve

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valuable carbon and energy during times of the day when their primary pollinators are

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inactive. Different modes of rhythmic scent release have been described so far. Diurnal

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rhythmicity in floral VOC emission was observed in plants pollinated during the day,

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whereas nocturnally emitting plants are visited by pollinators foraging at night (Kolosova

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et al. 2001a; Waelti et al. 2008). Interestingly, the total amounts of emitted VOCs do not

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change over the day/night cycle in Dianthus inoxianus, however the levels of compounds

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contributing to pollinator attraction vary according to visitor activity (Balao et al. 2011).

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Rhythmicity of scent emission is often transcriptionally regulated, similarly to its tissue-

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specificity (see e.g. Kolosova et al. 2001a; Hendel-Rahmanim et al. 2007; Nagegowda et

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al. 2008; Nieuwenhuizen et al. 2009), although substrate availability for scent

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biosynthetic enzymes was shown to play a regulatory role in the emission of some

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compounds as well (Kolosova et al. 2001a).

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In addition to being spatially and rhythmically regulated, floral scent emission

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often changes over the lifespan of flowers. Usually, emission levels are highest when

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flowers are ready for pollination, i.e. when anthers are dehisced, and decrease during 9 This article is protected by copyright. All rights reserved.

senescence. Once pollinated, single flowers change or reduce the level of produced

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volatiles to prevent further visits potentially damaging the flower and to redirect visitors to

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the remaining unpollinated flowers (Schiestl & Ayasse, 2001; Negre et al., 2003;

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Muhlemann et al., 2006; Rodriguez-Saona et al., 2011). Developmental regulation of

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scent emission occurs at several levels, including orchestrated expression of scent

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biosynthetic genes (Colquhoun et al. 2010), enzyme activities (see e.g. Pichersky,

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Lewinsohn & Croteau 1995; Dudareva et al. 2000; Shalit et al. 2003; Boatright et al.

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2004; Nagegowda et al. 2008) and substrate availability (Dudareva et al. 2000).

Accepted Article

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Transcriptional network controlling volatile emission in flowers Orchestrated formation of volatiles from several independent pathways is not

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only a function of biochemical properties of biosynthetic enzymes, but also requires the

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involvement of transcription factors (TFs). Indeed, coordinated transcriptional regulation

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of entire scent biosynthetic networks has been recently shown (Colquhoun & Clark 2011;

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Muhlemann et al. 2012), implying that transcription factors control scent emission.

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Despite their importance, only a few TFs regulating the expression of scent

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biosynthetic genes have been identified to date. TFs controlling the flux through the

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phenylpropanoid/ benzenoid network have recently been isolated from petunia flowers.

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ODORANT1 (ODO1), a R2R3-type MYB TF, is exclusively expressed in petunia petal

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tissue and regulates the transcription of a major portion of the shikimate pathway as well

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as entry points into both the Phe (i.e., chorismate mutase) and phenylpropanoid (i.e.,

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phenylalanine ammonia-lyase) branchways (Verdonk et al. 2005). ODO1 was also found

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to activate the promoter of an ABC transporter of unknown function localized at the

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plasma membrane (Van Moerkercke et al. 2012a). In petunia flowers, ODO1 is positively

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regulated by another R2R3-type MYB TF, EMISSION OF BENZENOIDS II (EOBII),

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which also activates the promoter of the biosynthetic gene isoeugenol synthase (Spitzer-

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Rimon et al. 2010; Colquhoun et al. 2011b; Van Moerkercke, Haring & Schuurink 2011).

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The recently identified petunia EOBI was shown to be a flower-specific R2R3-type TF,

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which acts downstream of EOBII and upstream of ODO1 (Spitzer-Rimon et al. 2012; Van

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Moerkercke, Haring & Schuurink 2011). Silencing of EOBI expression lead to down-

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regulation of numerous genes in the shikimate pathway (5-enolpyruvylshikimate-3-

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phosphate synthase, 3-deoxy-D-arabinoheptulosonate 7-phosphate synthase,

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chorismate synthase, chorismate mutase, arogenate dehydratase, and prephenate

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aminotransferase), as well as downstream scent-related genes (PAL, isoeugenol 10 This article is protected by copyright. All rights reserved.

synthase, and benzoic acid/salicylic acid carboxyl methyltransferase) (Spitzer-Rimon et

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al. 2012). In contrast to ODO1, EOBI and EOBII, the MYB4 TF was found to be a

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repressor of only a single enzyme in the phenylpropanoid pathway, cinnamate-4-

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hydroxylase, thus controlling the flux toward phenylpropanoid volatile compounds in

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petunia flowers (Colquhoun et al. 2011a).

Accepted Article

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While several transcription factors regulating the phenylpropanoid/benzenoid

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network have been isolated and characterized, transcriptional regulation of the terpenoid

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pathways remains elusive. MYC2, a basic helix-loop-helix TF, was recently identified in

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Arabidopsis inflorescences and shown to activate the expression of two sesquiterpene

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synthase genes TPS11 and TPS21 via the gibberellic and jasmonic acid signaling

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pathways (Hong et al. 2012). Despite the identification of several TFs for individual

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pathways, master regulators, which orchestrate formation of diverse volatile blends and

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act upstream of multiple metabolic pathways, are yet to be discovered. Recently,

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upregulation of terpenoid and phenylpropanoid pathways was achieved by

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overexpression of the Production of Anthocyanin Pigment1 TF in roses (Zvi et al. 2012).

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However, it remains unknown whether promoters of genes involved in terpenoid

336

formation are the natural targets for this TF.

337 338 339

Changes in floral volatile emission upon diverse biotic interactions In addition to internal regulatory mechanisms, several external factors are known

340

to influence composition, quantity and timing of volatile emission. These factors include

341

pollination and interactions with floral antagonists. Successful pollination leads to a

342

decrease or alterations in floral VOC emission in a variety of plant species (Tollsten &

343

Bergström 1989; Tollsten 1993; Schiestl & Ayasse 2001; Negre et al. 2003; Theis &

344

Raguso 2005; Muhlemann et al. 2006; Rodriguez-Saona et al. 2011). Besides reducing

345

carbon loss caused by emission, post-pollination changes in VOCs redirect pollinators to

346

yet unpollinated flowers (Schiestl & Ayasse 2001) or prevent additional visitation of

347

pollinated flowers by flower antagonists (Muhlemann et al. 2006). Post-pollination

348

decrease in emission was shown to occur within 24-96 hours of pollinator visitation

349

(depending on the plant species) and appears to be triggered once the pollen tubes

350

reach the ovary (Negre et al. 2003). Upon fertilization, different molecular mechanisms

351

were found to trigger the decrease in scent emission. In petunia flowers, reduced

352

methylbenzoate emission after pollination is the result of transcriptional downregulation

353

of the cognate gene in an ethylene-dependent manner (Negre et al. 2003). In 11 This article is protected by copyright. All rights reserved.

snapdragon flowers, however, the post-pollination decrease in methylbenzoate emission

355

largely depends on reduced S-adenosyl-L-methionine:benzoic acid carboxyl

356

methyltransferase (BAMT) activity and substrate availability (Negre et al. 2003).

Accepted Article

354

357

Altered volatile emission was also reported in the context of above- and

358

belowground plant-fungus interactions. Infection of Silene latifolia flowers by the anther

359

smut fungus Microbotryum violaceum results in decreased total scent emission and

360

discrimination against infected flowers by the pollinator (Dötterl et al. 2009). The intensity

361

and chemodiversity of floral scent emission also decrease as a function of colonization

362

by arbuscular mycorrhizal fungi in Polemonium viscosum, suggesting that plant-microbe

363

interactions occurring outside of floral tissues can also modulate flower traits providing

364

an additional layer of external regulatory mechanism (Becklin et al. 2011).

365

Herbivore-induced plant volatiles (HIPVs) have been extensively studied in

366

vegetative tissues. Signal perception and transduction mechanisms, as well as kinetics

367

of HIPV release are well characterized in these tissues (Dicke & Baldwin 2010).

368

However, only few studies have linked florivory with induction of defense VOCs in

369

flowers. One of the few known examples of florivore-induced volatile emission is

370

represented by wild parsnip flowers, which emit higher amounts of octyl esters upon

371

infestation with the parsnip webworm (Zangerl & Berenbaum 2009). Likewise,

372

Helicoverpa zea larvae feeding on cotton flower buds induce emission of terpenes and

373

fatty acid derivatives (Rose & Tumlinson 2004).

374 375 376

Floral volatiles as mediators in biotic interactions Floral VOCs possess multifaceted functions significantly contributing to attraction

377

of pollinators and serving as defense compounds against pathogens and florivores.

378

Although it was proposed that floral VOCs first served in protecting reproductive

379

structures against antagonists and only later acquired pollinator attracting capacities

380

(Pellmyr & Thien 1986), their latter function has been studied the most. Pollinator

381

attraction is mostly mediated by benzenoids, whereas defense functions are

382

predominantly assured by terpenoid and benzenoid VOCs (Schiestl 2010).

383 384 385

Floral volatiles in pollinator attraction For countless cross-pollinating plant species, mating involves the movement of

386

pollen from one individual to another. In many cases, animals such as insects, birds and

387

mammals significantly contribute to pollination by serving as vectors in pollen transfer. 12 This article is protected by copyright. All rights reserved.

Flowers employ a diverse palette of signals to mediate attraction of pollinators to flowers

389

for ensuring successful reproduction. For pollinators, this multisensory (visual, olfactory,

390

thermal, electromagnetic) input is essential to locate food and breeding sites. Over the

391

last decade, mounting evidence was accumulated for the role of floral volatiles in plant-

392

pollinator communication.

Accepted Article

388

393

It has been shown that the information conveyed by floral volatiles depends on

394

amount, composition and context of their emission, and elicits distinct behavioral

395

responses in the respective pollinators. Long-distance emission of volatiles mainly

396

contributes to guiding pollinators to flowers and is especially important for night-emitting

397

plants where production of volatiles has to be of high intensity to overcome decreased

398

conspicuousness of flowers under low illumination. In fact, the moth-pollinated Petunia

399

axillaris and Silene latifolia emit higher amounts of volatiles than day-emitting bee

400

pollinated plants within the same genus, like Petunia integrifolia and Silene dioica (Ando

401

et al. 2001; Waelti et al. 2008). In contrast, volatiles emitted over short distances trigger

402

landing, feeding and reproductive behavior. Exposure even to a single floral volatile of

403

the host plant Silene latifolia elicited landing and feeding behavior in Hadena bicruris

404

moths (Dötterl et al. 2006) while subjection of nocturnal hawkmoth Manduca sexta to an

405

olfactory stimulus induced proboscis extension (Goyret, Markwell & Raguso 2007). Not

406

only volatiles emitted from flower petals but also pollen odor can contribute to pollinator

407

foraging. Indeed, pollen odor artificially added to antherless Rosa rugosa flowers

408

increased frequency of bumblebees’ pollen-collecting behavior relative to odor- and

409

antherless flowers (Dobson, Danielson & Van Wesep 1999).

410

Volatiles emitted from flowers not only advertise food availability, but also mating

411

and oviposition opportunities. Examples include certain orchids which employ flower

412

scent to imitate pheromone blends of female pollinators, thereby triggering copulation

413

attempts of male pollinators with flowers (Schiestl et al. 1999). The dioecious species

414

Silene latifolia represents another example where floral volatiles provide oviposition cues

415

for the females of the nursery moth pollinator Hadena bicruris, which lay eggs while

416

pollinating the flowers (Brantjes 1976; Waelti et al. 2009). To mimic oviposition sites, a

417

number of species within the five plant families (Araceae, Rafflesiaceae, Annonaceae,

418

Apocynaceae and Orchidaceae) emit sulfur-containing volatile compounds to attract

419

necrophagous, saprophagous and caprophagous insects. Interestingly, these volatiles,

420

typically released by decomposing plant and animal organic matter, were found to arise

421

independently via convergent evolution (Jürgens et al. 2013). These emitted volatiles 13 This article is protected by copyright. All rights reserved.

also represent a characteristic feature of plants pollinated by necrophagous flies and

423

beetles, thus showing a clear link between certain pollinator guilds and specific floral

424

scent chemistries.

Accepted Article

422

425

Attempts to correlate floral volatile profiles with pollination syndromes have

426

succeeded for certain plant-pollinator interactions, however, clear-cut predictions of

427

pollinator guilds based on floral scent chemistry still remain unattainable. It was

428

nevertheless established that plant species relying on moths for pollination

429

predominantly release benzenoid, terpenoid and nitrogen-containing compounds

430

(Knudsen & Tollsten 1993; Dobson 2006) and that bat-pollinated species mostly emit

431

sulfur-containing volatiles (von Helversen, Winkler & Bestmann 2000). While

432

involvement of volatiles in the attraction of hummingbirds remains debated, certain

433

ornithophilous plants were found to emit minute amounts of terpenoids and fatty acid-

434

derivatives (Knudsen et al. 2004). Furthermore, hummingbirds were shown to display

435

different behaviors (attraction or aversion) depending on the volatiles contained in the

436

nectar of artificial flowers (Kessler & Baldwin 2007; Kessler, Gase & Baldwin 2008).

437 438 439

Floral volatiles in flower defense Flowers are generally deficient in physical barriers such as a highly lignified cell

440

wall and/or an impermeable cuticle, making them highly susceptible to pathogens and

441

florivores. Moreover, they typically carry higher densities of microorganisms than other

442

aerial plant surfaces due to their high moisture and nutrient content (Johnson &

443

Stockwell 1998). Thus, flowers employ volatiles as an alternative mechanism that

444

prevents damage to their reproductive structures.

445

Many VOCs were shown to exhibit antimicrobial and antifungal activities in vitro

446

(Bakkali et al. 2008) or inferred to have these antimicrobial activities due to tissue-

447

specific expression patterns (e.g. in nectaries and/or stigmas) of their biosynthetic genes

448

(Dudareva et al. 1996a; Chen et al. 2003). However, only few VOCs have been

449

investigated for their role in defense against pathogens. (E)--caryophyllene emitted

450

from stigmas of Arabidopsis flowers was shown to limit bacterial growth. Indeed,

451

Arabidopsis plants lacking (E)--caryophyllene emission displayed denser bacterial

452

populations on their stigmas and reduced seed weight compared to wild type plants,

453

indicating that (E)--caryophyllene acts in the defense against pathogenic bacteria and is

454

important for plant fitness (Huang et al. 2012). VOCs emitted by Saponaria officinalis


petals were shown to inhibit bacterial growth and suggested to control diversity of

456

bacterial communities in petals (Junker et al. 2011b).

Accepted Article

455 457

Besides pathogens, florivores also cause substantial damage to reproductive

458

tissues. Florivores are detrimental to plant fitness as they feed on reproductive structures,

459

often displace potential pollinators and alter flower morphology (McCall 2008; Sõber,

460

Mooraa & Tederb 2010). Similarly to green tissue volatiles, floral volatiles are capable of

461

deterring insects that are detrimental to pollinator visitation and/or are feeding on flower

462

tissues. Ants are very inefficient pollinators (due to their morphology and mobility), often

463

exhibit aggressive behavior against pollinators and occasionally feed on floral structures.

464

It was shown that many common European ants are deterred by volatiles emitted from

465

temperate flowers (Willmer et al. 2009) and that inhibition of terpene biosynthesis leads

466

to loss of ant-repellent properties (Junker, Gershenzon & Unsicker 2011a). The

467

facultative florivore Metrioptera bicolor displays a strong aversion to linalool and (E)--

468

caryophyllene, both of which are widespread terpenoid constituents of scent bouquets

469

emitted by flowering species (Junker, Heidinger & Blüthgen 2010). These examples

470

strongly suggest involvement of floral volatiles in deterrence against undesirable floral

471

visitors.

472 473

Balance between defensive and attractive functions of floral volatiles

474

Pollinators and florivores navigate the same visual and olfactory landscape to

475

locate host plants. To avoid visitation by florivores while advertising their flowers to

476

pollinators, plants have to balance attracting and deterring functions of floral volatiles.

477

Unbalanced production of volatiles involved in different functions may result in negative

478

impacts on plant fitness, as was shown in the cucurbit Cucurbita pepo where

479

enhancement of floral fragrance led to higher attraction of florivores significantly affecting

480

reproductive success (Theis & Adler 2012).

481

Several strategies employed by flowers to optimize these functions and therefore

482

maximize reproductive success have been described so far. In Cirsium arvense, some

483

floral volatiles are responsible for attraction of both pollinators and florivores (Theis

484

2006). In this species, timing of emission is fine-tuned to increase likelihood of pollinator

485

rather than florivore visitation. Indeed, developmental and diel timing of Cirsium arvense

486

volatile emission was found to be positively correlated with the flowers' reproductive

487

maturity and peak activity of pollinators, respectively, while negative correlation between

488

diel emission and activity of florivores was observed (Theis, Lerdau & Raguso 2007). 15 This article is protected by copyright. All rights reserved.

Similarly to Cirsium arvense, VOCs of petunia flowers attract both pollinators and

490

florivores. Within the petunia VOC profile some compounds specifically control

491

infestation rate by florivores (i.e. isoeugenol and benzylbenzoate), whereas

492

methylbenzoate, for example, is involved in pollinator attraction. Indeed, utilization of

493

various petunia transgenic lines with downregulation of different floral scent biosynthetic

494

genes allowed elucidation of the distinct roles of individual volatile compounds in

495

attraction of mutualists and deterrence of antagonists (Kessler et al. 2013). A similarly

496

complex picture was found in the cucurbit Cucurbita moschata, where some compounds

497

are attracting both pollinators and florivores, while other compounds are only mediating

498

one type of interaction (Andrews, Theis & Adler 2007). As a consequence of interactions

499

with both mutualists and antagonists, different types of selection may act on the different

500

volatile compounds. Indeed, compounds involved in attraction of both mutualists and

501

antagonists will more likely be under balancing selection, while compounds involved in

502

interactions solely with one type of flower visitor are under directional selection pressure.

503

This diversity of selection mechanisms is predicted to lead to the evolution of very

504

complex floral volatile profiles.

Accepted Article

489

505

Nursery pollination systems represent a special case where insects simultaneously

506

pollinate the flowers and use them as breeding sites. Flowers in these systems have

507

evolved adaptive mechanisms to reduce damage caused by developing larvae that feed

508

on the plant's reproductive tissues (usually seeds) (Dufaÿ & Anstett 2003). In general,

509

damage to seeds is predicted to be proportional to the number of visiting pollinators.

510

Therefore, fast cessation of floral advertisement after successful pollination is essential

511

to avoid further damage to the plant's reproductive success. Indeed, a post-pollination

512

decrease specifically in pollinator-attracting volatiles was observed in Silene, thereby

513

providing a mechanism to prevent further loss of seeds (Muhlemann et al. 2006).

514 515 516

Evolution of floral scent The evolution of angiosperms has resulted in an immense diversity of flower traits

517

such as shape, size, color and scent. To date, more than 1700 floral volatile compounds

518

have been described in over 900 flowering plant species (Knudsen et al. 2006).

519

Interestingly, the quality and quantity of emitted volatiles are species-specific and vary

520

among different populations of a given species (Raguso 2008). While much effort has so

521

far been invested in describing scent composition in various flowering species, the

522

mechanisms driving the evolution and diversification of floral scent remain underexplored. 16 This article is protected by copyright. All rights reserved.

Evolution of floral scent is potentially shaped by two factors that mutually influence each

524

other: 1) genomic changes allowing catalytic expansion and differential regulation of the

525

enzymatic machinery underlying floral scent formation and 2) ecological constraints such

526

as pollinator-mediated selection.

Accepted Article

523

527

To date, only a few studies have examined the genetic basis for odor differences

528

between closely related flowering species. Petunia axillaris and P. exserta represent a

529

good example of a closely related species with distinct pollination syndromes. While P.

530

axillaris flowers are colorless, emit benzenoid compounds and are moth-pollinated, P.

531

exserta flowers are red, devoid of scent and attract hummingbirds. Analysis of the

532

genetic basis for differences in scent profiles between these two species revealed that

533

only two quantitative trait loci are responsible for the distinct scent phenotypes (Klahre et

534

al. 2011). One of these loci maps to the MYB transcription factor ODO1, which controls

535

flux through the shikimate pathway and hence the amount of precursors available for

536

benzenoid biosynthesis (Verdonk et al. 2005), while the genetic identity of the second

537

locus is presently unknown. Clarkia breweri and C. concinna provide another example of

538

two closely related scented and non-scented species, which rely on different pollinators.

539

Although non-scented C. concinna contains genes responsible for formation of VOCs

540

(i.e., linalool, (iso)methyleugenol and benzylacetate), transcriptional and/or post-

541

transcriptional regulatory mechanisms lead to lack of their expression in flowers and

542

elimination of floral scent (Raguso & Pichersky 1995; Dudareva et al. 1996a; Cseke,

543

Dudareva & Pichersky 1998; Nam, Dudareva & Pichersky 1999). Differences in

544

transcriptional levels were also found in the flowers of the orchid genus Ophrys, which

545

emit a blend of fatty acid-derived volatiles (Schiestl et al. 1997; Schiestl et al. 1999;

546

Schiestl & Ayasse 2002). Within this blend, alkenes are the key components for the

547

attraction of pollinators to flowers and each Ophrys species emits a unique alkene profile,

548

resulting in reproductive isolation between species through attraction of distinct and

549

highly specific pollinators (Schiestl & Ayasse 2002). Ophrys sphegodes mostly emits

550

27:1Δ9 and 27:1Δ12 alkenes, while O. exaltata mainly produces a 25:1Δ7 alkene

551

(Schlüter et al. 2011). Formation of double bonds at position 9 and 12 of these alkenes

552

requires the action of a stearoyl-acyl carrier protein desaturase (SAD). Differences in

553

transcript levels, as well as changes in the tertiary structure of SAD2 between O.

554

sphegodes and O. exaltata were proposed as possible mechanisms underlying the

555

distinct alkene profiles and reproductive isolation (Schlüter et al. 2011). While large intra-

556

and interspecific variations in alkene profiles were detected within the Ophrys genus, 17 This article is protected by copyright. All rights reserved.

only limited genetic variation among species and populations was observed with

558

microsatellite markers (Mant, Peakall & Schiestl 2005). These findings suggest that

559

divergent, pollinator-mediated selection rather than genetic drift explains strong

560

differences in volatile profiles. Taken together, the above examples demonstrate that

561

small genetic variations can have large effects on floral scent chemistry and interactions

562

with pollinators.

Accepted Article

557

563

Besides genetic polymorphisms, selection by pollinators is also capable of driving

564

floral diversification and specialization. Pollinator-mediated selection is constrained by

565

the pollinator’s pre-existing preferences and sensory abilities, and can occur only when

566

the traits under selection are heritable and exhibit variation (Schiestl 2010; Schiestl &

567

Dötterl, 2012). Selection on floral scent by pollinators has been described in Penstemon

568

digitalis, which displays marked inter-population variation in its emitted floral VOCs.

569

Quantification of phenotypic selection by pollinators revealed that the monoterpene

570

linalool is a direct target of selection within this scent profile (Parachnowitsch, Raguso &

571

Kessler 2012). Several studies in other plant species have also uncovered volatile

572

compounds which are important for plant-pollinator interaction and thus serving as

573

potential targets for pollinator-mediated selection (see e.g. Dötterl et al. 2006;

574

Shuttleworth & Johnson 2010; Schiestl, Huber & Gomez 2011).

575

Interestingly, changes in floral scent through external manipulation (genetic or

576

chemical) or intrinsic processes (mutations or hybridization) were shown to drive

577

pollinator niche shifts, which are a proximate cause of floral and reproductive isolation.

578

Indeed, Shuttleworth and Johnson (Shuttleworth & Johnson 2010) have demonstrated

579

that the presence/absence of sulfur compounds within the bouquets of four Eucomis

580

species determines whether wasps or flies pollinate individual species. Also, creation of

581

more similar floral volatile profiles between Silene dioica and S. latifolia by artificial

582

manipulation of a single compound resulted in higher interspecific pollen transfer (Waelti

583

et al. 2008). Thus, the aforementioned studies show that floral scent is an important

584

factor in defining and maintaining species boundaries. They also demonstrate that loss

585

or generation of reproductive isolation can occur through relatively simple changes in

586

floral scent profiles. Evolution of reproductive isolation through changes in floral scent

587

chemistry can occur within very short time frames, as was illustrated in Ophrys

588

arachnitiformis x O. lupercalis hybrids (Vereecken, Cozzolino & Schiestl 2010). Indeed,

589

generation of novel floral volatile profiles in these hybrids led to attraction of a pollinator


species that does not pollinate any of the parent species (Vereecken et al. 2010),

591

thereby leading to rapid floral isolation.

Accepted Article

590 592 593 594

Conclusions and future perspectives Over the last two decades, the field of floral volatile research has acquired an

595

ever-increasing amount of knowledge on the functions and biosynthesis of floral scent.

596

Numerous floral volatile compounds have been identified to date from nearly 1,000 plant

597

species and their importance in mediating ecological interactions with floral mutualists

598

and antagonists has been highlighted in many plant species. Recent advances in the

599

isolation and characterization of genes and enzymes involved in different scent

600

biosynthetic pathways, as well as in the elucidation of regulatory networks controlling

601

these pathways, have also enhanced our understanding of how floral volatile

602

compounds are synthesized. Despite recent progress in floral volatile research, many

603

aspects of floral volatile function and biosynthesis remain largely unknown. In particular,

604

we still do not know how the majority of floral VOCs are synthesized, how their

605

orchestrated emission is regulated, and the specific roles of floral VOCs in large plant-

606

mutualist/antagonist interaction webs. We therefore anticipate that future research efforts

607

will focus on providing insights into these specific aspects of floral scent biology and

608

allow for development of defensive strategies as well as enhancement of yields in insect-

609

pollinated plants.

610


Figure Legends

613

Figure 1. Major volatile classes emitted by flowers. Based on their biosynthetic origin,

614

volatiles emitted by flowers can be grouped into one of the three major volatile classes:

615

terpenoids, phenylpropanoids/benzenoid and fatty acid derivatives. Each volatile class is

616

here represented by a few typical floral scent compounds.

Accepted Article

611 612

617 618

Figure 2. Schematic representation of terpenoid VOCs biosynthesis. Synthesis of

619

terpenoid VOCs occurs via the cytosolic mevalonic acid (MVA) and the plastidial

620

methylerythritol phosphate (MEP) pathways, the former giving rise to sesquiterpenes

621

and the latter to monoterpenes, diterpenes and volatile carotenoid derivatives. Cross-talk

622

between both pathways is facilitated by the export of isopentenyl pyrophosphate (IPP)

623

from the plastid to the cytosol. Stacked arrows represent multiple biosynthetic steps.

624

Volatile compounds are highlighted with a yellow background. Abbreviations: DMAPP,

625

dimethylallyl pyrophosphate; FPP, farnesyl pyrophosphate; FPPS, FPP synthase; G3P,

626

glyceraldehyde-3-phosphate; GGPP, geranylgeranyl pyrophosphate; GGPPS, GGPP

627

synthase; GPP, geranyl pyrophosphate; GPPS, GPP synthase; IPP, isopentenyl

628

pyrophosphate; TPS, terpene synthase.

629 630

Figure 3. Schematic representation of the VOC phenylpropanoid/benzenoid biosynthetic

631

pathway. Phenylpropanoid/benzenoid VOCs are derived from phenylalanine, which itself

632

is synthesized via the shikimate/phenylalanine biosynthetic pathways. Benzoic acid is

633

the central precursor of various benzenoid VOCs and is synthesized via two biosynthetic

634

routes, the beta-oxidative pathway (orange background) and non-oxidative route.

635

Stacked arrows indicate multiple enzymatic reactions. Volatile compounds are

636

highlighted with a yellow background. Abbreviations: AAAT, aromatic amino acid

637

aminotransferase; BA, benzoic acid; BA-CoA, benzoyl-CoA; BAlc, benzylalcohol; BAld,

638

benzaldehyde; BALDH, benzaldehyde dehydrogenase; BB, benzylbenzoate; BEAT,

639

acetyl-CoA:benzylalcohol acetyltransferase; BPBT, benzoyl-CoA:benzylalcohol/2-

640

phenylethanol benzoyltransferase; BSMT, benzoic acid/salicylic acid carboxyl

641

methyltransferase; CA, cinnamic acid; CA-CoA, cinnamoyl-CoA; C4H, cinnamate-4-

642

hydroxylase; CNL, cinnamoyl-CoA ligase; Eug, eugenol; IEug, isoeugenol; KAT, 3-

643

ketoacyl-CoA thiolase; MB, methylbenzoate; 3O3PP-CoA, 3-oxo-3-phenylpropionyl-CoA;

644

PAAS, phenylacetaldehyde synthase; PAL, phenylalanine ammonia lyase; pCA, p-


coumaric acid; PEB, phenylethylbenzoate; PhA, phenylacetaldehyde; Phe, L-

646

phenylalanine; PhEth, 2-phenylethanol; PhPyr, phenypyruvic acid.

Accepted Article

645 647


Table 1: List of biosynthetic genes involved in final steps of floral volatile formation. Gene Species Reference Volatile Monoterpenoids CitMTSL1 Citrus unshiu (Shimada et 1,8-Cineole al. 2005) NsCIN Nicotiana suaveolens (Roeder et al. 2007) CbLIS Clarkia breweri (Dudareva Linalool et al. 1996a) AmNES/LIS-1 Antirrhinum majus (Nagegowda et al. 2008) TPS10 Arabidopsis thaliana (Ginglinger et al. 2013) TPS14 Arabidopsis thaliana (Ginglinger et al. 2013) Am1e20 Antirrhinum majus (Dudareva Myrcene et al. 2003) AmOc15 Antirrhinum majus (Dudareva et al. 2003) AlstroTPS Alstromeria peruviana (Aros et al. 2012) Am0e23 Antirrhinum majus (Dudareva E-(β)-Ocimene et al. 2003) CitMTSL4 Citrus unshiu (Shimada et al. 2005) Sesquiterpenoids AdAFS1 Actinidia deliciosa (Nieuwenhui α-Farnesene zen et al. 2009) AdGDS1 Actinidia deliciosa (Nieuwenhui Germacrene D zen et al. 2009) VvGerD Vitis vinifera (Lucker et al. 2004) FC0592 Rosa hybrida (Guterman et al. 2002) AmNES/LIS-2 Antirrhinum majus (Nagegowda Nerolidol et al. 2008) AcNES1 Actinidia chinensis (Green et al. 2012) VvVal Vitis vinifera (Lucker et Valencene al. 2004) Benzenoids/ Phenylpropanoids AmBALDH Antirrhinum majus (Long et al. Benzaldehyde 2009) CbBEAT Clarkia breweri (Dudareva Benzylacetate et al. 1998) PhBPBT Petunia hybrida (Boatright et Benzylbenzoate al. 2004) PhEGS Petunia hybrida (Koeduka et Eugenol

Accepted Article

648


Accepted Article

Isoeugenol

PhIGS

Petunia hybrida

Isomethyleugenol

CbIEMT

Clarkia breweri

Methylbenzoate

AmBAMT

Antirrhinum majus

PhBSMT1

Petunia hybrida

PhBSMT2

Petunia hybrida

Methyleugenol

CbIEMT

Clarkia breweri

Phenylacetaldehyde

PhPAAS

Petunia hybrida

RhPAAS

Rosa hybrida

2-Phenylethanol

RdPAR

Rosa damascena

Phenylethylbenzoate

PhBPBT

Petunia hybrida

Veratrole

SlGOMT1

Silene latifolia

649 650


al. 2006) (Koeduka et al. 2006) (Wang et al. 1997) (Murfitt et al. 2000) (Negre et al. 2003) (Negre et al. 2003) (Wang et al. 1997) (Kaminaga et al. 2006) (Farhi et al. 2010) (Chen et al. 2011b) (Boatright et al. 2004) (Gupta et al. 2012)

References

Accepted Article

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Accepted Article

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Accepted Article

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Accepted Article

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Accepted Article

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Accepted Article

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New synthesis: the evolutionary ecology of floral volatiles.

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