Abstract
Flower color and scent, crucial qualitative characteristics of ornamental plants, display extensive variation. These distinct pigments and scents play a key role in attracting specific pollinators. While previous research primarily delved into the synthetic regulatory mechanisms of individual traits and their respective attraction to insects, recent studies unveil an interconnectedness between flower color and scent through transcriptional regulatory networks. Moreover, evidence suggests that both color and scent actively contribute to insect attraction. This review summarizes the co-regulation and synthesis of pigments and scents, highlighting their pivotal roles in pollinator attraction. The insights provided will serve as valuable references for applications in metabolic engineering, novel variety breeding, and insect and pest detection and management.
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Introduction
Flower color and scent play pivotal roles, enhancing the commercial value of ornamental plants and influencing their yield and quality. Additionally, plants use these representative traits to attract pollinators, ensuring successful reproduction (Parachnowitsch and Manson 2015; Koski 2020). Research has categorized flower pigments into flavonoids, carotenoids, and betalains, whereas flower scents are grouped into terpenoids, benzenoids/phenylpropanoids, and fatty acid derivatives. Briefly, flavonoids, betalains, and benzenoids/phenylpropanoids originate from the general shikimate pathway, with carotenoid and terpenoid volatiles being common precursors (Tanaka et al. 2008; Sun et al. 2016; Duan et al. 2020). Despite the identification of numerous regulators associated with pigment and scent biosynthesis across various plants (Yang et al. 2020, 2021; Cao et al. 2022; Shen et al. 2022), a comprehensive summary and discussion on their cooperative regulation and subsequent impacts on the metabolic flux of the biosynthetic pathway are yet to be realized (Yeon and Kim 2021). Because color and scent are crucial visual and olfactory cues for attracting pollinators, understanding the biosynthetic pathways and transcriptional regulations is essential for gaining comprehensive insights into plant-animal interactions (Hirota et al. 2012). This review delves into recent advances in comprehending the associations between floral pigments, scent compounds, biosynthesis, regulation, and their role in attracting pollinators.
Diversity and composition of color and scent compounds
Flavonoids, a prevalent class of water-soluble specialized metabolites in plants, possess a fundamental C6-C3-C6 structure and encompass various subclasses, including flavones (colorless to pale yellow), isoflavones (colorless), anthocyanins (orange to blue), flavonols (colorless to pale yellow), and proanthocyanidins (colorless) (Tanaka et al. 2008; Jaakola 2013). Flavonoids were thought to be synthesized in the cytosol (endoplasmic reticulum) and mainly transported to vacuoles for storage (Zhao and Dixon 2009) (Fig. 1a).
Structures of main color and scent compounds. a Flavonoids. b Betalains. c Carotenoids. d The basic skeleton structure of terpenoids. e Benzenoid and phenylpropanoid volatiles
Betalains, exclusive to the order Caryophyllales (except for the families Caryophyllaceae and Molluginaceae) (Clement and Mabry 1996), originate from tyrosine and constitute water-soluble nitrogen-containing compounds. These compounds can be broadly categorized into betacyanins (red to violet) and betaxanthins (yellow to orange) (Polturak et al. 2017). The synthesis involves the conversion of betalamic acid, the fundamental structure for all betalains. Stored in vacuoles like anthocyanins, betalains exhibit greater stability over a broader pH range (Azeredo 2009) (Fig. 1b).
Carotenoids are derived from the widely distributed C5 (isoprene unit) and contribute to the yellow-to-red coloration in flowers and fruits (Tanaka et al. 2008). In contrast to flavonoids and betalains, carotenoids are fat-soluble pigments synthesized and accumulated in plastids. They are structurally classified into carotenes (phytoene, lycopene, α-carotene, and β-carotene), existing in either a linear structure or incorporating a cyclic hydrocarbon ring, and oxygenated xanthophylls (zeaxanthin, violaxanthin, and lutein), containing functional groups such as hydroxyl, epoxy, or keto groups (Simkin 2021). Carotenoids exhibit varied content and composition between photosynthetic and nonphotosynthetic tissues. Chloroplasts in photosynthetic tissues primarily house carotenoids, whereas chromoplasts in nonphotosynthetic tissues serve as the primary storage sites (Iijima et al. 2020) (Fig. 1c).
Terpenes, a group exceeding 40,000 compounds, play a substantial role in primary and secondary plant metabolism. All terpenoids originate from isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP), both C5 molecules (Duan et al. 2020). Terpenoid biosynthesis involves the mevalonate (MVA) and methylerythritol phosphate (MEP) pathways. The MVA pathway primarily produces sesquiterpenes (C15) and triterpenes (C30), whereas the MEP pathway predominantly produces monoterpenes (C10), diterpenes (C20), sesterterpenes (C25), and volatile carotenoid derivatives (tetraterpenes, C40) (Muhlemann et al. 2014; Sun et al. 2016) (Fig. 1d).
Benzenoids and phenylpropanoids, the second most abundant group of plant volatiles, play diverse roles in interactions with the surrounding ecosystem (Dudareva et al. 2013). Derived from L-phenylalanine, benzenoids/phenylpropanoids undergo benzene ring modifications through methylation, hydroxylation, or acetylation, resulting in over 300 phenolic scent compounds. These include phenylpropenes (C6-C3), benzenoids (C6-C1), and phenylpropanoid-related metabolites (C6-C2) (Widhalm and Dudareva 2015; Yeon and Kim 2021) (Fig. 1e).
Volatile alcohols/aldehydes, originating from polyunsaturated fatty acids (PUFAs) (Dudareva et al. 2013), undergo diverse pathways for conversion. Some PUFAs transform into α-hydro (pero) xy PUFAs through the lipoxygenase (LOX) pathway mediated by α-dioxygenase, while others become self-oxidative products (Feussner and Wasternack 2002). Lipid peroxide derivatives undergo additional processing through the hydroperoxide lyase (HPL) branch of the LOX pathway, converting both types of hydroperoxide fatty acid derivatives into C6 and C9 aldehydes. These volatile aldehydes, whether saturated or unsaturated, are substrates for alcohol dehydrogenases, producing volatile alcohols that can be further transformed into esters (Feussner and Wasternack 2002; Mostafa et al. 2022). C6 and C9 aldehydes and alcohols are synthesized in vegetative tissues and are commonly known as green leaf volatiles (Ma et al. 2022). Research highlights that the appealing fragrance of certain ornamental plants, such as Dianthus caryophyllus (Kishimoto et al. 2011), the orchid genus Ophrys (Schlüter et al. 2011), and Antirrhinum majus (Suchet et al. 2011), is mainly attributed to volatile alcohols/aldehydes. However, compared to terpenoid and phenylpropanoid/phenylpropanoid volatiles, limited data are available regarding the biosynthesis of fatty acid derivatives in flowers. Consequently, this review provides a comprehensive discussion on the synthesis and analysis of terpenoid and phenylpropanoid regulation in floral systems.
The biosynthetic pathways of color and scent compounds
Flavonoids, betalain pigments, and benzenoid/phenylpropanoid volatiles all originate from the shikimate pathway. Among them, flavonoids and benzenoids/phenylpropanoids derive from L-phenylalanine, whereas betalains originate from tyrosine. After the synthesis of L-phenylalanine and tyrosine from shikimic acid, they enter the secondary metabolic pathway (phenylpropanoid pathway and tyrosine pathway) to synthesize various compounds (Rippert et al. 2009). In terms of synthesis location, flavonoids and phenylpropanoid-related volatiles are synthesized in the cytosol, whereas benzenoid products are generated either in peroxisomes (via the β-oxidative pathway) or in the cytosol (via the non-β-oxidative pathway) (Widhalm and Dudareva 2015; Sun et al. 2016). Carotenoids are predominantly C40 terpenoid pigments with conjugated double bonds (Giuliano et al. 2002). Carotenoids and terpenoid volatiles are synthesized through the MEP pathway (in plastids) or MVA pathway (in the cytosol), both sharing common precursors, IPP and DMAPP (Nisar et al. 2015) (Fig. 2). These pigments and volatiles, while having common precursors, follow distinct synthetic pathways. The detailed relationships between them are described below.
Correlation between flavonoid and benzenoid/phenylpropanoid synthesis
Flavonoids and benzenoids/phenylpropanoids originate from the phenylpropanoid pathway, commencing with the aromatic amino acid phenylalanine (Fig. 3). Phenylpropanoid-related volatiles (C8) play crucial roles as scent compounds in various flowers, including roses and petunias, with identified and characterized genes and enzymes responsible for their biosynthesis. In roses, phenylalanine undergoes conversion to 2-phenylacetaldehyde by phenylacetaldehyde synthase (PAAS), followed by its transformation to 2-phenylethanol catalyzed by phenylacetaldehyde reductase (PAR) (Chen et al. 2011). The biosynthesis of volatile benzenoids (C7) initiates with L-phenylalanine ammonia lyase (PAL), catalyzing the conversion of phenylalanine to cinnamic acid. Subsequently, cinnamic acid transforms into benzenoid-related products through the β-oxidative pathway, the non-β-oxidative pathway, or a combination of the two (Sun et al. 2016). Sequentially, cinnamic acid undergoes conversion to p-coumaric acid and then to p-coumaroyl-CoA through the catalysis of cinnamate 4-hydroxylase (C4H) and 4-coumarate:CoA ligase (4CL). Following the generation of the intermediate p-coumaroyl-CoA, this shared precursor undergoes catalysis by chalcone synthase (CHS) and p-coumarate 3-hydroxylase (C3H). Carbon flow is directed into branches, producing flavonoid (C15) and phenylpropene volatiles (C9) through several reactions involving side chain and benzene ring modifications (Yahyaa et al. 2019; Zhang et al. 2021a) (Fig. 1a and 1e, Fig. 3). Given their lower molecular weights compared to flavonoid pigments, benzenoid/phenylpropanoid volatiles are synthesized upstream of anthocyanin production. These secondary metabolites compete for the utilization of phenylalanine (Sinopoli et al. 2019; Joh et al. 2020; Yeon and Kim 2021).
A schematic diagram of shared biosynthetic pathways for pigments and scent compounds. PAAS, phenylacetaldehyde synthase; PAR, phenylacetaldehyde reductase; BPBT, benzoyl-CoA:benzylalcohol/2-phenylethanol benzoyltransferase; AOs, aldehyde oxidases; BSMT, benzoic acid/salicylic acid carboxyl methyltransferase; CNL, cinnamoyl-CoA ligase; CHD, cinnamoyl-CoA hydratase/dehydrogenase; KAT, 3-ketoacyl-CoA thiolase; CCoAOMT, caffeoyl-CoA O-methyltransferase; CCR, cinnamoyl-CoA reductase; CAD, cinnamyl-alcohol dehydrogenase; CFAT, coniferyl alcohol acetyltransferase; IGS, isoeugenol synthase; EGS, eugenol synthase; PAL, phenylalanine ammonia lyase; C4H, cinnamic acid 4-hydroxylase; 4CL, 4-coumarate: CoA-ligase; CHS, chalcone synthase; CHI, chalcone isomerase; FNS1/2, flavone synthase 1/2; IFS, isoflavone synthase; F3H, flavanone 3-hydroxylase; F3’H, flavonoid 3’-hydroxylase; F3′5’H, flavonoid 3’,5’-hydroxylase; FLS, flavonol synthase; DFR, dihydroflavonol 4-reductase; LAR, leucoanthocyanidin reductase; ANS, anthocyanidin synthase; ANR, anthocyanidin reductase; 3GT and 5GT, anthocyanidin 3 and 5 glucosyltransferase; ART, anthocyanidin 3-glucoside rhamnosyltransferase; AAT, anthocyanidin 3-rutinoside acyltransferase; 3’AMT, anthocyanidin 3’ O-methyltransferase; 3′5’AMT, anthocyanidin 3′5’ O-methyltransferase; MVA, mevalonic acid; MEP, methylerythritol phosphate; DMAPP, dimethylallyl diphosphate; IPP, isopentenyl diphosphate; FPP, farnesyl diphosphate; GPP, geranyl diphosphate; GGPP, geranylgeranyl diphosphate; HMG-CoA, 3-hydroxy-3-methylglutaryl coenzyme A; DXS, 1-deoxy-D-xylulose 5-phosphat synthase; DXR, 1-deoxy-D-xylulose 5-phosphate reductoisomerase; MCT, 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase; CMK, 4-diphosphocytidyl-2-C-methyl-D-erythritol kinase; MDS, 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase; HDS, (E)-4-hydroxy-3-methylbut-2-enyl-diphosphate synthase; HDR, 4-hydroxy-3-methylbut-2-enyl diphosphate reductase; GPPS, geranyl pyrophosphate synthase; GGPPS, geranyl diphosphate synthase; TPS, terpene synthase; GFDPS, geranylfarnesyl diphosphate synthase; zFPS, Z,Z-farnesyl diphosphate synthase; SBS, santalene and bergamotene synthase; ZIS, α-zingiberene synthase; AACT, acetoacetyl-CoA transferase; HMGS, hydroxymethylglutaryl-CoA synthase; HMGR, hydroxymethylglutaryl-CoA reductase; MVK, mevalonate kinase; PMK, phosphomevalonate kinase; MVD, diphosphomevalonate decarboxylase; IPK, isopentenyl phosphate kinase; IDI, isopentenyl-diphosphate delta-isomerase; Phos, phosphorylate; FPPS, Farnesyl pyrophosphate synthase; SQS, squalene synthase; SQE, squalene epoxidase; OSC, oxidosqualene cyclase; PSY, phytoene synthase; PDS, phytoene desaturase; ZDS, zeta-carotene desaturase; ZISO, zeta-carotene isomerase; CRTISO, carotene isomerase; LCY-ε, lycopene epsilon-cyclase; LCY-β, lycopene beta-cyclase; BCH1/2, β-carotene hydroxylase 1/2; ZEP, zeaxanthin epoxidase; VDE, violaxanthin de-epoxidase; NSY, neoxanthin synthase; CYP97A, cytochrome P450 carotene β-hydroxylase; CYP97C, cytochrome P450 carotene ε-hydroxylase; CCD, carotenoid cleavage dioxygenases
Correlation between flavonoid and betalain synthesis
Significant differences exist in the biosynthesis of flavonoids and betalains. While there is a well-established understanding of flavonoid synthesis, the production and regulation of betalains have only been partially characterized (Fig. 3). Flavonoids are synthesized in nearly all plant species. In contrast, betalains are exclusively found in eight families of the order Caryophyllales, including Aizoaceae, Amaranthaceae, Basellaceae, Cactaceae, Didiereaceae, Nyctaginaceae, Phytolaccaceae, and Portulacaceae (Iwashina 2015). Betalain-containing species include several flavonoid compounds, including flavones, flavonols, flavanones, dihydroflavonols, chalcones, aurones, flavanans, and proanthocyanidins. Notably, anthocyanins and biflavonoids are absent. Among these classes, the major flavonoids found in betalain-containing families are flavonols (Iwashina 2015).
Betalains and anthocyanins exhibit a mutually exclusive distribution, with no plant species producing both types of pigments (Grotewold 2006). The accumulation of flavonols in Caryophyllales plants suggests a potential inhibition of the late step in anthocyanin biosynthesis, particularly impeding the conversion of dihydroflavonols to anthocyanins. However, the specific molecular mechanisms underlying the mutual exclusion of betalains from anthocyanins remain incompletely understood. In recent years, advances in molecular techniques such as transcriptomics and metabolic profiling have partially elucidated the molecular mechanism behind the absence of anthocyanin production in betalain-producing plants (Polturak et al. 2018; Liu et al. 2019; Zhou et al. 2020; Sakuta et al. 2021). In Mirabilis jalapa, the anthocyanidin synthase (ANS) gene exhibits a significant sequence deletion, potentially accounting for the absence of anthocyanins. This hypothesis is further supported by the presence of flavonol glycosides and an active dihydroflavonol 4-reductase (DFR) enzyme in M. jalapa petals (Polturak et al. 2018). Sakuta et al. (2021) revealed that the functional loss of the R2R3-type v-myb avian myeloblastosis viral (R2R3-MYB) transcription factor (TF) and the production of anthocyanin pigment (PAP) homologs led to a deficiency in anthocyanin production within betalain-producing Caryophyllales plants. In conclusion, the absence of anthocyanins in betalain-producing Caryophyllales plants may result from the loss of functions of enzymes or TFs associated with anthocyanin synthesis.
Correlation between carotenoid pigments and terpenoid volatiles
In plants, volatile terpenoids are typically synthesized using geranyl diphosphate (GPP, C10) or trans-farnesyl diphosphate (FPP, C15), resulting in the production of monoterpenes (C10) and sesquiterpenes (C15), respectively (Kang et al. 2014). Carotenoids and monoterpenes are synthesized through the MEP pathway, whereas sesquiterpenes are produced via the MVA pathway (Fig. 3). Most genes encoding enzymes in carotenoid and terpenoid biosynthesis have been identified with characterized enzymatic activities. However, the biosynthetic relationship between carotenoids and terpenoid volatiles remains understudied (Tanaka et al. 2008; Zheng et al. 2019; Nagegowda and Gupta 2020). Studies indicate that certain carotenoids can produce apocarotenoid volatiles through the action of carotenoid cleavage dioxygenases (CCDs) (Huang et al. 2009; Ma et al. 2013). For instance, CmCCD4a from Chrysanthemum morifolium enzymatically cleaves β-carotene at the 9, 10 (9′, 10′) positions in vivo, producing β-ionone (Huang et al. 2009). HaCCD1 from Helianthus annuus, displaying a broad substrate specificity for carotenoids, prefers β-carotene to generate β-ionone in vivo (Qi et al. 2021). Current research on carotenoid pigments and terpenoid volatiles has mainly concentrated on vegetables and fruits. The impact of carotenoid synthesis pathway gene expression on terpenoid volatiles remains unknown and requires further investigation.
Transcriptional regulation of key genes involved in color and scent biosynthesis
MYBs, basic helix-loop-helix (bHLH) TFs, and WRKYs represent the predominant TF families in plants. Numerous studies have confirmed their involvement in specialized plant metabolism, including pathways such as the biosynthesis of benzenoids, phenylpropanoids, terpenoids, and flavonoids (Table 1). However, the collective regulatory mechanisms of these TFs in synthesizing flower color and scent compounds remain inadequately understood. Here, we present a comprehensive overview discussing recent advancements in the functions and mechanisms of these TFs, highlighting their roles in coordinating flower color and scent biosynthesis.
Regulators of flower color compound biosynthesis
Several TF families that regulate flower coloration in ornamental plants have been identified as transrepressors, transactivators, or coregulators involved in color compound synthesis (Table 1). The transcriptional regulation of flavonoids primarily involves the MYB or MYB-bHLH-WDR (MBW) complex (Tanaka et al. 2008). Within the MBW complex, MYB TFs act as activators or repressors, directly or indirectly governing the expression of flavonoid structural genes. bHLH proteins typically act as bridges between MYB and WD40 proteins. They can also directly bind to the promoters of downstream genes involved in flavonoid biosynthesis, inducing flavonoid biosynthesis. In contrast, WD40 repeat proteins can interact with either bHLH or MYB proteins to indirectly regulate flavonoid accumulation (Hichri et al. 2010; Li et al. 2016). Additionally, microRNAs (miRNAs), such as miR156, miR828, miR165/166, and miR778, degrade or inhibit the translation of flavonoid synthesis-related mRNAs through complementary pairing of target mRNAs, thereby inhibiting gene transcription and affecting flavonoid accumulation (Gou et al. 2011; Yan et al. 2012; Wang et al. 2015; Bonar et al. 2018).
In the last five years, numerous TFs that regulate carotenoid synthesis have been identified in fruits and vegetables. Examples include Malus domestica apetala2 (AP2)/ethylene response factor (ERF) TF MdAP2-34, MdMADS6 (Dang et al. 2021; Li et al. 2022a), Musa acuminata squamosa promoter binding protein-like 16 (MaSPL16) (Zhu et al. 2020), Citrus sinensis CsERF061, CsMADS5 (Lu et al. 2021; Zhu et al. 2021), and Capsicum annuum B-box (BBX) zinc-finger TF CaBBX20 (Ma et al. 2023). However, research on carotenoids in ornamental plants has been less extensive compared to fruits and vegetables. In Mimulus lewisii, reduced carotenoid pigmentation 1 (RCP1), an R2R3-MYB, was identified as the first TF activating floral carotenoid accumulation (Sagawa et al. 2016). The Chrysanthemum morifolium apetala3, pistillata, and ultrapetala1 interacting factor 1 (CmAP3-CmPI-CmUIF1) complex directly activates the expression of CmCCD4a-2, regulating carotenoid metabolism in flowers (Lu et al. 2022). In Osmanthus fragrans, 2-(4-chlorophenylthio)-triethylamine hydrochloride (CPTA) induces OfMYB43 expression. Transient overexpression of OfMYB43 significantly promotes the expression of phytoene desaturase (PDS), zeta-carotene isomerase (ZISO), lycopene epsilon-cyclase (LCYE), and CCD4, leading to increased accumulation of beta-branch carotenoids (Xi et al. 2021).
While TFs play a crucial role in regulating betalain metabolism, our current understanding of the regulation of betalain pigmentation in plants is limited. However, some MYB and WRKY TFs have been identified to participate in the biosynthetic regulation of betalains (Hatlestad et al. 2015; Cheng et al. 2017; Zhang et al. 2021b; Xie et al. 2021). Beta vulgaris BvMYB1 activates the expression of Cytochrome P450 76AD1 (CYP76AD1) and 4,5-dioxygenase 1 (DODA1) expression, leading to betalain accumulation in beets, establishing it as the first MYB TF involved in regulating betalain biosynthesis (Hatlestad et al. 2015). The discovery of HpWRKY44 as the first WRKY TF involved in betalain biosynthesis in pitaya highlights its role in transcriptionally activating the CYP76AD1 promoter (Cheng et al. 2017). Subsequently, HuMYB1 and HmoWRKY40 were identified as players in regulating betalain biosynthesis in plants (Xie et al. 2021; Zhang et al. 2021b). These findings suggest the significant roles of MYB and WRKY TFs in betalain biosynthesis; however, the complete regulatory network remains to be fully elucidated.
Regulators of flower scent compound biosynthesis
The synthesis of volatiles in flowers involves multiple independent biosynthetic pathways, with TFs playing a crucial regulatory role in the process. However, only a limited number of TFs have been associated with floral scent biosynthesis. R2R3-MYBs are common regulators of benzenoid/phenylpropanoid synthesis (Table 1), notably in petunia. In petunia, MYB TFs such as Petunia × hybrida emission of benzenoids I (PhEOBI), PhEOBII, odorant 1 (PhODO1), and PhMYB4, along with the P-type H+-ATPase proton pump PH4 (PhPH4), are involved in the regulation of phenylpropanoid synthesis (Verdonk et al. 2005; Spitzer-Rimon et al. 2010, 2012; Colquhoun et al. 2011; Cna’ani et al. 2015). PhODO1, identified as a master regulator of benzenoid/phenylpropanoid production and emission in petunia, binds and regulates an extensive set of genes involved in multiple networks contributing to floral volatile metabolism (Verdonk et al. 2005; Boersma et al. 2022). PhEOBII regulates the expression of PhODO1 and activates the promoter of isoeugenol synthase (IGS) (Spitzer-Rimon et al. 2010; Colquhoun et al. 2011). PhEOBIs act both downstream of PhEOBII and upstream of PhODO1 (Spitzer-Rimon et al. 2012). The interaction between PhERF6 and EOBI negatively regulates benzenoid biosynthesis (Liu et al. 2017). Moreover, LhODO1 isolated from Lilium hybrida has been shown to regulate the production of phenylpropanoids/benzenoids (Yoshida et al. 2018).
The regulation of terpenoid biosynthesis involves six TF families: AP2/ERF, auxin response factor (ARF), bHLH, basic leucine zipper (bZIP), MYB, and WRKY (Picazo-Aragonés et al. 2020) (Table 1). TFs such as AtMYB21, AtMYC2, CpbHLH13, and AabZIP1 have been identified as regulators of sesquiterpene synthesis (Reeves et al. 2012; Hong et al. 2012; Zhang et al. 2015; Yang et al. 2020; Aslam et al. 2020). In Phalaenopsis bellina, multiple TFs, including bHLH4, bHLH6, bZIP4, ERF1, ERF9, and NAC1 (nam, ataf1/2, cuc1/2), are implicated in potentially regulating the expression of monoterpene synthase genes (Chuang et al. 2017). Additionally, several NAC, WRKY, ARF, and ERF family TFs are involved in monoterpene synthesis (Table 1). In Hedychium coronarium, HcMYBs (HcMYB7/8/75/145/248) interact with the HcJAZ1 protein, potentially playing pivotal roles in regulating the expression of floral scent biosynthesis genes, contributing to the formation of terpenoids and benzenoids (Abbas et al. 2021a). Further research on TFs promises valuable insights into the regulatory mechanisms governing flower scent production.
Coordinated regulation of floral color and scent compound biosynthesis
The regulatory mechanisms co-modulating flower color and scent compound biosynthesis remain unclear. Raymond et al. (2018) proposed that the miR156-SPL9 regulatory hub coordinates the synthesis of anthocyanins and specific terpenes by facilitating the complexation of preexisting MYB-bHLH-WD40 proteins. This complex subsequently regulates various components within both pathways (Raymond et al. 2018) (Fig. 4a). In petunia, EOBII and ODO1 regulate scent formation without significantly impacting flower color. Conversely, PhPH4 governs the release of benzenoid and phenylpropanoid volatiles and potentially influences anthocyanin accumulation through its regulatory role in vacuolar acidification (Verdonk et al. 2005; Spitzer-Rimon et al. 2012; Cna’ani et al. 2015) (Fig. 4b). The MYB21-MYC complex synergistically regulates flavonol and linalool synthesis by regulating the expression of flavonol synthase (FLS) and terpene synthase (TPS) genes in Freesia hybrida and Arabidopsis (Shan et al. 2020; Yang et al. 2020) (Fig. 4c). Additionally, the MYB-bHLH-WD40 complex plays a role in flavonoid and carotenoid biosynthesis by regulating the expression of structural genes associated with these pathways (Meng et al. 2019; Li et al. 2022b) (Fig. 4d and 4e). Furthermore, overexpressing Arabidopsis PAP1 in petunia, tobacco, and rose plants increases both anthocyanin levels and volatile compound levels (phenylpropanoids/benzenoids) (Xie et al. 2006; Zvi et al. 2008, 2012). Despite limited studies on TFs that coordinately regulate color and scent, isolating relevant TFs through gene editing methods is essential for enhancing the horticultural quality of plants.
Cooperative metabolic regulation of color and scent compounds. a Key regulatory factors associated with co-metabolism in the biosynthesis of color and scent compounds have been confirmed in various plants, including Rosa hybrida and Arabidopsis thaliana (Raymond et al. 2018), (b) Petunia hybrida (Verdonk et al. 2005; Spitzer-Rimon et al. 2012; Cna’ani et al. 2015), (c) Freesia hybrida (Shan et al. 2020; Yang et al. 2020), (d) Medicago truncatula (Meng et al. 2019), and (e) Camellia sinensis (Li et al. 2022b). The red arrow indicates activation, the black arrow indicates no effect, the blue short line indicates inhibition, and the red dashed arrow indicates putative gene regulation. SPL, squamosa promoter-binding protein-like; bHLH, basic helix-loop-helix; MYB, v-myb avian myeloblastosis virus; EPSPS, 5-enolpyruvate-shikimate-3-phosphate synthase; EOBI, emission of benzenoids I; ODO1, odorant 1; PhPH4, Petunia × hybrida P-type H+-ATPase proton pump PH4; MtTT8, Medicago truncatula transparent testa 8; MtWP1, Medicago truncatula white petal 1; CsTT8a, Camellia sinensis transparent testa 8a; CsSCPL1A1, Camellia sinensis serine carboxypeptidase-like clade 1A; miR156, microRNA156; WD40, WD40 repeat protein; NES, linalool/nerolidol synthase; DFR, dihydroflavonol-4-reductase; ANS, anthocyanidin synthase; GDS, germacrene D synthase; PAL, phenylalanine ammonia lyase; CFAT, coniferyl alcohol acetyltransferase; IGS, isoeugenol synthase; MYC2, jasmonate insensitive 1; FLS, flavonol synthase; TPS, terpene synthase; CHS, chalcone synthase; MtPDS, Medicago truncatula phytoene desaturase; MtZDS, Medicago truncatula zeta-carotene desaturase; MtCRTISO, Medicago truncatula carotene isomerase; MtLYCe, Medicago truncatula lycopene ε-cyclase; MtLYCb, Medicago truncatula lycopene β-cyclase; MtBCH, Medicago truncatula β-carotene hydroxylase; MtCYP97C, Medicago truncatula cytochrome P450 ε-ring carotenoid hydroxylase; CsANR, Camellia sinensis anthocyanidin reductase; CsPSY, Camellia sinensis phytoene synthase; CsCRTIRO, Camellia sinensis carotene isomerase; CsLCYBa, Camellia sinensis lycopene β-cyclase a; CsLCYBb, Camellia sinensis lycopene β-cyclase b; CsLYCe, Camellia sinensis lycopene ε-cyclase; CsCYP97C, Camellia sinensis cytochrome P450 ε-ring carotenoid hydroxylase; CsBCH, Camellia sinensis β-carotene hydroxylase
Pollinator attraction via flower color and scent
Insect pollination (entomophily) is a primary method for flowering plants. Pollinators effectively identify these plants by integrating visible cues, such as flower color, with invisible cues, such as floral scent. Flower color acts as a signal, enhancing visibility against the plant background and attracting pollinators. In particular, the presence of nectar guides indicates that color significantly influences visitation frequency. Thus, flower color strongly impacts the advertising of flowers to pollinators (Sheehan et al. 2012; Phillips et al. 2020; Narbona et al. 2021). Floral scents, recognized as crucial long-range attractants, predominantly allure pollinators during the night. Moreover, floral scents function over shorter distances, such as within-flower nectar guides, or serve as a defense mechanism against antagonists (Sheehan et al. 2012; García et al. 2021). Research indicates that different pollinators exhibit preferences for both color and scent (Koethe et al. 2020; Yeon and Kim 2021). Despite the critical roles of color and scent in the reproductive process facilitated by pollinators, the correlation between color/scent and pollinator attraction remains largely unexplored for most plant species.
Role of pigments and scents in attracting diverse pollinators
In the process of evolution, flowering plants seamlessly integrate flower color with pollinator attraction, endowing them with a significant competitive advantage. This organic fusion has propelled flowering plants to become the largest group of angiosperm species, contributing substantially to the diversity observed in angiosperms today (Nadot and Carrive 2021). Flower color indicates the reproductive state of plants, providing insights into the quantity and quality of stored pollen or nectar. Simultaneously, it acts as a visual signal to attract insects and facilitates their recognition of flowers. The different flower colors also ensure the accuracy and efficiency of insect recognition (Reverté et al. 2016). Notably, red flowers enriched with anthocyanins establish strong associations with moths and butterflies (Hirota et al. 2012). Flowers displaying blue and reddish-purple hues due to delphinidin enrichment exhibit pronounced attraction toward bees and butterflies (Almut et al. 2006; Dyer et al. 2021). White flowers, enriched with flavones and/or flavonols, prove enticing to moths, bees, and flies (Klaus et al. 2018; Hannah et al. 2019). Similarly, yellow flowers, enriched with carotenoids, flavonols, and/or chalcones, capture the attention of butterflies, bees, and flies (Klaus et al. 2018; Sinha et al. 2023) (Fig. 5a). Additionally, colored patterns on flowers and the coloration of nectar guides serve as visual cues for pollinators, enhancing the success of plant pollination (Richter et al. 2023).
Relationships between flower color, scent, and pollinators. a Relationships between flower color and pollinators. b Relationships between flower scents and pollinators
The scent of flowers typically comprises multiple compounds, with one or several dominant compounds constituting a significant proportion of the scent. Pollinators can discern specific scent components accurately. Additionally, the role of scent in attracting pollinators varies among closely related flower species. For example, bee-pollinated flowers frequently release terpenoid floral volatiles. Three monoterpenes (d-limonene, β-myrcene, and E-β-ocimene) modulated bumblebee flower preference and were individually sufficient to drive distinct bumblebee visits to Mimulus lewisii and M. cardinalis (Byers et al. 2014). The presence of eugenol from anthers increased bumblebee landings on Rosa rugosa flowers. Conversely, bumblebees developed a preference for phenylacetaldehyde after foraging on Brassica rapa flowers, as phenylacetaldehyde release positively correlated with pollen and nectar availability (Knauer and Schiestl 2015). Unlike unscented Petunia exserta, moths prefer scented P. axillaris, which emits benzenoid volatiles, guiding their choice at a short distance (Klahre et al. 2011). Additionally, floral scent emission follows a circadian rhythm and is closely related to pollinator behavior. The timing of scent release likely optimizes resource utilization while minimizing plant visibility to herbivores (Fenske and Imaizumi 2016) (Fig. 5b).
In addition to attracting pollinators, plant volatiles serve direct or indirect defensive functions against herbivorous insects (Lin et al. 2021) (Fig. 5b). After herbivory, plants release abundant terpenoids, fatty acid derivatives, and other substances such as indoles and methyl salicylate. Herbivore-induced volatiles are typically employed as indirect defenses to attract insects that prey on herbivores, thereby reducing further plant damage. Additionally, green leaf volatiles released by leaves also play a defensive role to a certain extent through direct toxicity to insects (Kessler and Baldwin 2001; Schuman et al. 2012; Lin et al. 2021).
Color and scent synergistically increase reproductive success
Pollinators' foraging behavior is influenced by color and scent, either independently or in combination. Pollinators determine whether a flower has been pollinated by detecting its color and scent, which work synergistically (Dormont et al. 2010). Research indicates that the combination of floral scent and color provides more reliable rewards for foraging bees, ultimately increasing flower reproductive success. In Papaver nudicaule, the combination of scent and color cues significantly enhances the discrimination of honeybees, suggesting the positive influence of color–scent associations on pollinator constancy (Martínez-Harms et al. 2018). Moreover, bumblebees demonstrate improved discrimination abilities when the scent pattern corresponds to a matching visual color pattern. Once they have acquired knowledge of the spatial arrangement of a scent pattern, they utilize the same visual cues to visit scentless flowers (Kantsa et al. 2017; Lawson et al. 2018). According to the efficacy backup hypothesis, plants provide multiple flower signals; when one signal changes, the others can serve as backups for flowers to communicate with pollinators, ensuring reproductive success (Lawson et al. 2017; Aguiar et al. 2021). Bees that have learned color–scent associations use color as a backup for selecting flowers when their olfactory signals are disturbed (Lawson et al. 2017).
Changes in post-pollination color and scent affect pollinator behavior
Floral color and scent changes in flowering plants often occur during post-pollination and senescence processes, linked to the quantity of generated flowers (such as pollen and nectar), ultimately influencing pollinator behavior and reproductive success. As pollen matures, plant petals unfold to attract pollinators through pigmentation and scent emission. However, plants stop attracting pollinators after pollination by changing their color and scent (Lucas-Barbosa 2016; Yan et al. 2016). A shift in floral color serves as a visual signal for pollinators to avoid aging flowers, enhancing pollination efficiency (Yan et al. 2016; Ruxton and Schaefer 2016). Some plants distinguish pollinated from unpollinated flowers through differences in flower color, improving overall attractiveness at a distance and allowing pollinators to easily differentiate between unpollinated and pollinated flowers (Ohashi et al. 2015).
Changes in the color of nectar guides are considered an honest signal to pollinators. For instance, in Arnebia szechenyi, the gradual disappearance of the nectar guide signifies a decline in nectar and pollen rewards. Flowers become unattractive to pollinators when lacking a nectar guide (Zhang et al. 2017). Generally, emission levels increase as flower buds approach the flowering stage and decrease when most flowers are senescent (Zheng et al. 2015; Yue et al. 2019). Volatile compound emission increases when flowers are ready for pollination; however, post-pollination, flowers reduce volatile synthesis to deter further visits and oviposition by pollinators (Martignier et al. 2019; Okamoto et al. 2022). In Quisqualis indica, nectar and scent secretion correlate with floral color changes to attract different pollinators and promote reproductive fitness. The color of Q. indica flowers shifts from white to pink to red to attract different pollinators, accompanied by alterations in scent components and decreased scent emission rates (Yan et al. 2016).
Coevolution of flower pigments, scents, and pollinators
Approximately 87.5% of flowering plants rely on animals for pollination (Skaliter et al. 2022). The distinctive characteristics of flowers, known as pollination syndromes, including color, scent, morphology, nectar, and pollen, allow plants to attract specific pollinators. Consequently, flower nectar and pollen serve as rewards for pollinators (Roy et al. 2022). In return, pollinators drive the evolution of plant diversity in pollination syndromes, leading to reproductive isolation and eventual speciation (Amrad et al. 2016; Liang et al. 2022, 2023), contingent upon their impact on the reproductive success of the flowers. This mutual adaptation relationship between a flower and its visitor is termed coevolution.
The population of Mimulus aurantiacus exhibits highly divergent flower colors between geographic races: red morphs in coastal regions and yellow morphs in mountain regions. The parapatric distribution is elucidated by pollination selection, with hummingbirds being the primary coastal pollinators selecting red morphs, whereas bees, crucial pollinators in mountain regions, specifically visit yellow morphs (Streisfeld and Kohn 2007). In addition to population diversity, pollinator preference plays a vital role in speciation. A textbook example is observed in M. cardinalis and M. lewisii, which are closely related but reproductively isolated due to pollinator preference. Hummingbird-pollinated M. cardinalis boasts a red corolla rich in carotenoids and anthocyanins, whereas bumblebee-pollinated M. lewisii has a pink corolla with vibrant yellow nectar guides abundant in carotenoids (Liang et al. 2023). A shift in the corolla color of M. lewisii leads to a change in pollinator preference. Similarly, documented cases show that an increase in the quantity and complexity of phenylpropanoid/benzenoid volatiles in petunia resulted in a shift from bee to hawkmoth pollinators; in contrast, a decrease in scent, caused by the loss of cinnamate-CoA ligase function and reduced ODO1 expression, facilitated a transition from moths to hummingbirds (Amrad et al. 2016).
In conclusion, the interdependence of color and scent in many flowers poses challenges in discerning their individual effects. Specific floral scent compounds help pollinators distinguish between different-colored flowers (Raguso 2008). Moreover, pollinator-induced changes in flower color and scent significantly contribute to the population’s survival, reproductive abilities, and adaptability. Furthermore, pollinators may exert significant selective pressure, influencing the evolution of floral color and scent. The differentiation in flower colors and scents can lead to pollinator diversification, resulting in reproductive isolation. Therefore, the coevolution of flower color, scent, and pollinators proves advantageous for biological diversity.
Conclusions and perspectives
In this review, we systematically summarized the classification, biosynthesis, regulation, and roles of flower color and scent, providing a comprehensive understanding of their metabolic processes in plants. Although the pathways involved in color and scent compound biosynthesis are well-established, further exploration is needed to unravel the regulatory networks governing their synthesis, degradation, and transport. In particular, understanding the synergistic metabolic and cooperative regulatory mechanisms of color and scent remains a key research focus. Further research will enhance our understanding of plant pigment and aroma compound metabolic pathways, unveiling interrelationships that can serve as valuable targets for future breeding and diverse plant applications.
Through integrating phenomics, genomics, metabolomics, and advanced molecular biology techniques, including gene editing, the investigation into flower color and scent mechanisms has enhanced precision in establishing correlations between plant genotypes and these traits. Uncovering key regulatory genes governing these traits lays the foundation for molecular design breeding, facilitating targeted enhancement. Currently, noncoding RNAs, epigenetic mechanisms, and posttranslational modifications play pivotal roles in regulating pigment synthesis, particularly in flavonoid biosynthesis (Sun et al. 2023). While the study of floral scent synthesis pathways has primarily focused on model plants, there is a lag compared to floral color synthesis research. Therefore, further exploration is warranted to unravel additional regulatory factors and mechanisms of pigment synthesis in diverse ornamental plants, representing a crucial avenue for future research in ornamental plant studies.
To increase their stability and water solubility, pigments and scent substances, including flavonoids, betaine, monoterpenes, and phenylpropanoids, undergo various post-production modifications, such as glycosylation, methylation, and acylation. These modifications facilitate the transportation and storage of these compounds within subcellular compartments (Cna'ani et al. 2017). However, understanding the mechanisms governing the transport, storage, synthesis, and timely release of pigments and scent substances at specific locations requires further investigation.
Investigating the mechanisms behind plant pigment and scent synthesis contributes to a deeper understanding and application of regulatory factors. This facilitates precise trait regulation through gene editing for enhancing flower color and scent in ornamental plants. Furthermore, synthetic biology’s rapid progress enables scalable and sustainable production of pigments and scent compounds. Cells can convert inexpensive substrates into high-value products using the entire metabolic pathway. Lage-scale metabolite production becomes feasible by elucidating the biosynthesis pathway of pigments and scents in plants and transferring it to cellular organisms such as yeast (Ma et al. 2022). Yeast has been employed for synthesizing several terpenoids and flavonoids (Liu et al. 2018; Romanowski and Eustáquio 2020). Thus, with synthetic biology’s support, the heterologous synthesis of plant pigments and scent substances holds immense potential for practical applications.
Global environmental changes are causing a decline in pollinator diversity worldwide, threatening the mutualistic relationship between plants and their pollinators (Byers and Chang 2017; Glenny et al. 2018; Cordeiro and Dӧtterl 2023). To address this issue, modifying flower color and scent characteristics to enhance their appeal to pollinators is a potential approach to maintaining or improving pollination efficiency (Skaliter et al. 2022). This review explores the roles of color and scent in attracting pollinators. However, there remains a lack of understanding regarding pollinators’ perception, discrimination, and response to color and scent and their interaction with the pollination environment. The synergistic effect of color and scent on attracting pollinators remains unresolved. The interaction between pollinators, flower color, and scent signals involves multifaceted fields, including botany, zoology, evolutionary biology, behavioral ecology, sensory physiology, and neurobiology, necessitating an interdisciplinary approach. Interactions between plants and pollinators encompass reciprocity, antagonism, defense mechanisms, and other dynamics. Investigating these interactions has significant implications for biodiversity conservation and agriculture. Considering insect color and scent preferences, employing biological methods to cultivate novel plant species or create an environment through physical or chemical means can attract insects, increasing pollinator attraction. Consequently, this improves plant pollination efficiency and seed set rates and facilitates pest entrapment for effective biological control (Peng et al. 2022).
In conclusion, elucidating the metabolic regulation of flower color and scent, and understanding the underlying mechanisms, offer potential for future breeding and production improvements through metabolic engineering and molecular biotechnology. This approach facilitates the enhancement of flower color and scent characteristics, efficiently producing desired pigments and aroma substances while preserving essential plant‒plant/pollinator interactions. Moreover, these advancements will significantly contribute to both human well-being and environmental sustainability.
Availability of data and materials
Not applicable.
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This research was supported by the earmarked fund for China Agriculture Research System (CARS-23).
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G.N. and M.L. conceived of the idea; Y.S., Y.R., M.M., and Y.L. collected and analyzed the literature; Y.S wrote the first draft of the manuscript; G.N., M.L., Y.H., and Z.W. reviewed and prepared the final draft of the manuscript. All authors read and approved the final manuscript.
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Shen, Y., Rao, Y., Ma, M. et al. Coordination among flower pigments, scents and pollinators in ornamental plants. HORTIC. ADV. 2, 6 (2024). https://doi.org/10.1007/s44281-024-00029-4
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DOI: https://doi.org/10.1007/s44281-024-00029-4