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Metabolic engineering of terpene metabolism in lavender

Abstract

Background

Several members of the Lamiaceae family of plants produce large amounts of essential oil [EO] that find extensive applications in the food, cosmetics, personal hygiene, and alternative medicine industries. There is interest in enhancing EO metabolism in these plants.

Main body

Lavender produces a valuable EO that is highly enriched in monoterpenes, the C10 class of the isoprenoids or terpenoids. In recent years, substantial effort has been made by researchers to study terpene metabolism and enhance lavender EO through plant biotechnology. This paper reviews recent advances related to the cloning of lavender monoterpene biosynthetic genes and metabolic engineering attempts aimed at improving the production of lavender monoterpenes in plants and microbes.

Conclusion

Metabolic engineering has led to the improvement of EO quality and yield in several plants, including lavender. Furthermore, several biologically active EO constituents have been produced in microorganisms.

1 Background

Lavender (genus Lavandula) belongs to the family Lamiaceae and is known for producing large amounts of essential oil [EO]. The genus Lavandula encompasses over 30 known species, each characterized by a unique EO profile [1, 2]. The presence of specific monoterpenes in lavender EO contributes to its value, making it a significant resource in the production of perfumes, medicinal products, food flavorings, and antiseptics [3, 4]. The most abundant monoterpenes in lavender EO are linalool, linalyl acetate, borneol, camphor, and 1,8-cineole [5, 6]. Other notable monoterpenes include limonene, lavandulol, lavandulyl acetate, and α-terpineol [4, 7, 8]. In addition, lavender produces certain monoterpenes in response to environmental conditions [8, 9].

Among all lavender species, Lavandula angustifolia, Lavandula latifolia, and their natural hybrid, Lavandula x intermedia, hold significant commercial importance [10]. L. angustifolia is highly valued in the perfumery industry due to its high levels of linalool and linalyl acetate. EO obtained from L. latifolia is important in the medical sector because of its high concentrations of linalool, camphor, and 1,8-cineole. L. x intermedia EO contains constituents found in both parents, and is widely used in personal care and hygiene products, [3].

This review highlights recent efforts aimed at biotechnological improvement of lavender EO in engineered plants. It also provides information on the production of lavender EO constituents in microorganisms.

2 Main text

2.1 Methodology

Published articles were sourced from various search engines and databases, including Web of Science, Google Scholar, ScienceDirect, Scopus, and SciFinder. Keywords used in the search included lavender, along with essential oil, glandular trichomes, gene cloning, transformation, metabolism, engineering, terpene synthases, terpene biosynthesis, and genome editing. Additionally, separate searches were conducted for yeast, bacteria, and cyanobacteria in conjunction with key monoterpenes from lavender EO such as linalool, 1,8-cineole, and borneol.

2.2 Terpenes

The terpenoids (terpenes), also known as isoprenoids, represent the most abundant class of plant secondary metabolites. They serve crucial roles in plant growth, development, overall metabolism, and defense against predators, diseases, and competition [11]. Many terpenes have applications in cosmetics, pharmaceuticals, insecticides, and potential biofuels. In plants, the biosynthesis of terpenes is divided into three stages. The first stage involves the production of the common precursors, isopentenyl diphosphate [IPP] and its isomer dimethylallyl diphosphate [DMAPP] via the 2-C-methyl-D-erythritol 4-phosphate [MEP] pathway, also known as the 1-deoxy-D-xylulose-5-phosphate [DXP] pathway, and/or mevalonate [MVA] pathway. During the second stage, intermediates such as geranyl diphosphate [GPP], farnesyl diphosphate [FPP], and geranylgeranyl diphosphate [GGPP] are synthesized from IPP/DMAPP by isoprenyl diphosphate synthases [IDSs], also known as prenyltransferases. The final stage involves the production of various terpenes, catalyzed by terpene synthases [TPSs] such as linalool synthase [LINS] and 1,8-cineole synthase [CINS], along with terpene-modifying enzymes. It has been shown that the enzymes involved in terpene production have distinct subcellular localizations: all MEP pathway enzymes are located in plastids, while MVA pathway enzymes are found in the cytosol or peroxisomes [13, 14]. IDSs and TPSs exhibit more diverse localizations and are frequently associated with the subcellular site of terpene biosynthesis [12].

2.3 Glandular trichomes [GTs]

GTs are specialized plant structures dedicated to the synthesis and accumulation of EO. Lavender possesses two types of GTs: peltate GTs and capitate GTs. Peltate GTs produce and store a significant amount of monoterpene-rich EO in lavender [6, 15]. Each peltate GT comprises a basal cell, anchoring it to the epidermis, a stalk cell, up to eight secretory cells, and a storage cavity.[16]. A plasma membrane separates the storage cavity from the secretory cells [17, 18]. Within the secretory cells, EO synthesis occurs in two compartments: the cytosol and the leucoplast, where the MVA and MEP pathways operate, respectively [17, 19, 20]. EO constituents synthesized in the plastids via the MEP pathway are transported to the cytosol and subsequently secreted into the storage cavity, either directly or after processing [18].

Trichome formation, which is widely studied in Arabidopsis, is regulated in part by transcription factors [TFs] that can have either positive or negative effects. Additionally, other TFs function upstream or downstream of these regulators [21]. Recently, Zhang et al. [22] studied GT formation in lavender using a genomics approach, identifying several TFs belonging to R2R3-MYB subfamily associated with GT development.

2.4 Monoterpene biosynthesis

Monoterpenes are synthesized within the plastids of photosynthetic organisms, utilizing primary metabolites [12, 23]. In plants, chloroplasts serve as the major sites for monoterpene biosynthesis via the MEP pathway (Fig. 1) [24]. The pathway initiates with the condensation and decarboxylation of pyruvate [PYR] and glyceraldehyde 3-phosphate [G3P] by DXP synthase [DXS], yielding DXP. Subsequently, DXP reductoisomerase [DXR] catalyzes the reduction of DXP to MEP via NADPH-dependent isomerization [25]. MEP undergoes a series of enzymatic reactions involving MEP cytidyltransferase [MCT], 4-(cytidine 5ˈ-diphospho)- 2-C-methyl-D-erythritol-kinase [CMK], and 2-C-methyl-D-erythritol-2,4-cyclodiphosphate [MEcPP] synthase [MDS], leading to the formation of MEcPP [26, 27]. MEcPP is further reduced to 4-hydroxy-3-methylbut-2-enyl diphosphate [HMBPP] by HMBPP synthase [HDS]. IPP and DMAPP, the final products of MEP pathway, are generated in a ratio of approximately 5:1through the reduction of HMBPP by HMBPP reductase [HDR] [28,29,30]. Prenyltransferases, including geranyl diphosphate synthase [GPPS] and neryl diphosphate synthase [NPPS], catalyze the condensation of IPP and DMAPP to synthesize GPP and neryl diphosphate [NPP], which are precursors of monoterpenes [31]. In addition to monoterpenes, IPP/DMAPP derived from the MEP pathway is used to produce numerous other terpenes including photosynthetic pigments such as phytol and carotenoid precursors [32, 33].

Fig. 1
figure 1

Biosynthesis of isopentenyl diphosphate [IPP] and dimethylallyl diphosphate [DMAPP] through 2-C-methyl-D-erythritol 4-phosphate [MEP] pathway. PYR [pyruvate], G3P [glyceraldehyde 3–phosphate], DXP [1-deoxy-D-xylulose-5-phosphate], CPP-ME [cytidyl diphosphate-methyl-D-erythritol], CPP-MEP [cytidyl diphosphate-methyl-D-erythritol 4-phosphate], MEcPP [2-C-methyl-D-erythritol -2,4-cyclodiphosphate], HMBPP [1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate], GPP [geranyl diphosphate], NPP [neryl diphosphate], and GGPP [geranylgeranyl diphosphate]

2.5 Monoterpene metabolism in lavender

In line with other plant species, TPSs are responsible for catalyzing the conversion of the GPP substrate into cyclic and acyclic monoterpenes within the secretory cells of lavender GTs [34, 35]. Numerous researchers have undertaken efforts to clone TPS genes and characterize their functionality in vitro, aiming to elucidate their roles in EO production (Table 1). For instance, Landmann et al. [1] employed a homology-based PCR approach to clone two monoterpene synthases [monoTPSs]: limonene synthase [LaLIMS] and LINS [LaLINS], and one sesquiterpene synthase [sesquiTPSs]: bergamotene synthase [LaBERS] from L. angustifolia leaves and flowers. Subsequently, the cloned cDNAs were expressed in Escherichia coli. LaLIMS produced limonene, terpinolene, camphene, α-pinene, β-myrcene, and traces of β-phellandrene, while LaLINS solely produced (R)-(−)-linalool, and LaBERS converted FPP into bergamotene. In addition, Demissie et al. [36] reported the cloning and functional characterization of β-phellandrene synthase [LaβPHLS] in E. coli. Their results showed that the recombinant LabPHLS converted GPP and NPP into β-phellandrene. In 2012, Demissie et al. [4] identified the CINS [LiCINS] gene from L. x intermedia and cloned it into E. coli. The resulting bacterially generated recombinant protein, approximately 63 kDa in size, converted GPP mainly into 1,8-cineole. As reported again by Demissie et al. [37], L. x intermedia lavandulyl diphosphate synthase [LiLPPS] was cloned using a homology-based cloning method and expressed in E. coli. The resulting protein, with a molecular weight of about 34.5 kDa, catalyzed the fusion of two DMAPP units to form lavandulyl diphosphate [LPP] in vitro. The works of Demissie et al. [4, 36, 37] were continued by the research of Sarker et al. [2, 7, 38], who cloned and expressed borneol dehydrogenase [LiBDH], caryophyllene synthase [LiCPS], and two alcohol acetyltransferases [LiAAT-3 and LiAAT-4] genes in E. coli. The recombinant LiBDH protein converted borneol into camphor, the recombinant LiCPS protein converted FPP into 9-epicaryophyllene, and both recombinant LiAAT-3 and LiAAT-4 proteins converted lavandulol to lavandulyl acetate. In 2015, Benabdelkader et al. [9] cloned two monoTPSs and one sesquiTPS from L. pedunculata and functionally identified them as fenchol synthase [LpFENS], α-pinene synthase [LpPINS], and germacrene A synthase [LpGEAS]. Interestingly, while the expression patterns of FENS and PINS genes aligned with the enzyme product accumulation profile, this correlation was not observed for GEAS. Next, Adal et al. [8] identified and characterized a monoTPS gene, 3-carene synthase [Li3CARS], from L. x intermedia. The results showed that the recombinant Li3CARS transformed GPP into 3-carene as the major product (Fig. 2). In 2019, the same researcher reported the cloning of S-LINS [LiS-LINS] gene from L. x intermedia in bacteria. The cloned LiS-LINS catalyzed the conversion of GPP into S-linalool as the sole product [39]. In 2023, Adal et al. [40] cloned lavender (+)- bornyl diphosphate synthase [LiBPPS] in bacteria, and the recombinant LiBPPS promoted the conversion of GPP to (+)- bornyl diphosphate [BPP] as the main product, accompanied by the formation of several minor monoterpene compounds. In a recent study, Ling et al. [41] identified terpene synthase 7 [LaTPS7] and terpene synthase 8 [LaTPS8] genes from L. angustifolia during the budding phases. Subsequently, they cloned these TPSs into E. coli and Nicotiana benthamiana. The recombinant LaTPS7 generated nine different products in vitro, including camphene, myrcene, and limonene, while LaTPS8 produced eight volatiles using GPP and NPP as substrate. Moreover, the overexpression of LaTPS7 in N. benthamiana resulted in the synthesis of limonene, whereas LaTPS8 yielded α-pinene and sylvestrene.

Table 1 Cloning and metabolic engineering of lavender genes
Fig. 2
figure 2

Metabolism of acyclic a and cyclic b monoterpenes in lavender. LIMS [limonene synthase], (−)-α-TS [(−)-α-terpineol synthase], 1,8 CS [1,8-cineole synthase], BPPS [bornyl diphosphate synthase], BDH [borneol dehydrogenase], LINS [linalool synthase], AT [acetyltransferase], and LPPS [lavandulyl diphosphate synthase]

2.6 Cloning other lavender genes

As shown in Table 1, other aspects of lavender have also been studied. For instance, Guitton et al. [42] conducted a study on the concentration of volatile organic compound [VOC] in L. angustifolia throughout inflorescence growth. They found that calyces were the primary sources of VOC accumulation, with three major VOC groups dominating the global fragrance bouquet of inflorescences. The transition of VOCs occurred between the opening of the inflorescence's first flower and the beginning of seed set. There is a need to develop more knowledge on the molecular features of bloom initiation and development in lavender. Wells et al. [43] studied the short vegetative phase [LaSVP] gene of L. angustifolia and transformed it into A. thaliana. Their results showed that expression of LaSVP in A. thaliana delayed flowering, resulted in the production of sepals instead of petals, and prevented the formation of seed pods. Additionally, Adal et al. [44] used RNA-Seq and transcript profiling to identify several TFs potentially regulating floral development in lavender. Their study focused on the roles of two TFs, LaAGAMOUS-like [LaAG-like] and LaSEPALLATA3-like [LaSEP3-like], in flower development. LaAG-like and LaSEP3-like cDNAs were overexpressed in Arabidopsis plants. The results revealed that all transgenic plants exhibited earlier flowering compared to wild-type controls. Furthermore, mildly overexpressed plants grew normally, but those that excessively expressed the transgene had curling leaves. Another researcher, Dong et al. [45] focused on a bHLH TF, LaMYC4, an important regulator for plant terpenoid biosynthesis. This gene was isolated from L. angustifolia following methyl jasmonate [MeJA] treatment and overexpressed in Arabidopsis and tobacco. Results showed that overexpression of LaMYC4 enhanced sesquiterpenoids, including caryophyllene.

2.7 Metabolic engineering to produce lavender monoterpenes

2.7.1 Engineering lavender plants

The initial lavender metabolic engineering endeavor to improve the plastidial MEP pathway for the synthesis of the precursors IPP and DMAPP, was conducted by Munoz-Bertomeu et al. [46]. In their study, Munoz-Bertomeu et al. up-regulated DXS, an enzyme catalyzing the initial step in the MEP pathway. They expressed a cDNA encoding the A. thaliana DXS into spike lavender. Gas chromatography/mass spectrometry [GC–MS] analyses indicated that transgenic plants produced significantly higher EOs compared to control plants, with the accumulated EOs maintained in the T1 generation. In another effort, Tsuro and Ikedo [47] infected calli derived from lavandin (L. × intermedia) leaves with Agrobacterium rhizogenes, and regenerated plants. However, the regenerated plantlets displayed dwarfism due to short internodes, and low EO content. Moreover, Adal et al. [40] expressed the (+)-LiBPPS gene in both sense and antisense orientation. They observed that when (+)-LiBPPS was orientated in the antisense orientation, there was a reduction in the synthesis of (+)-borneol and camphor, while plant growth and development remained unaffected. Conversely, plants with the sense-orientated (+)-LiBPPS produced higher levels of borneol and camphor, but their growth and development were adversely affected.

2.7.2 Engineering microbes to produce lavender EO constituents

Researchers are also considering engineering microorganisms (Table 2) for the (eventual) large-scale production of lavender EO monoterpene constituents. The following are prominent examples of such studies:

Table 2 Microbial production of major monoterpenes present in lavender
2.7.2.1 Production of lavender monoterpenes in yeast

Deng et al. [48] produced linalool in Saccharomyces cerevisiae by introducing a fusion protein composed of LINS from Actinidia arguta and farnesyl diphosphate synthase [ERG20] from S. cerevisiae. The fusion protein, connected by a proper polypeptide linker between enzymes, exhibited a 69.7% increase in efficiency in linalool production compared to the application of individual free enzymes. Furthermore, Zhang et al. [49] demonstrated an enhancement in linalool production in S. cerevisiae through a series of experiments: They initially integrated the Isopentenol Utilization Pathway [IUP] into S. cerevisiae by incorporating choline kinase and isopentenyl phosphate kinase. Subsequently, LINS from Actinidia arguta was truncated from the N-terminal and introduced into S. cerevisiae. A double mutation was applied to ERG20 to enhance its efficiency, followed by its introduction into S. cerevisiae. linalool production was further enhanced by optimizing isoprenol, prenol, carbon source, and including Mg2+ in the medium. Moreover, Zhou et al. [50] applied a combinatorial strategy to enhance linalool content in S. cerevisiae. This strategy involved the overexpression of the entire MVA pathway, as well as a LINS from Mentha citrata, resulting in a significant increase in linalool concentration. Later, they further enhanced linalool production by employing a double mutation in LINS and ERG20. Zhang et al. [51] conducted dual metabolic engineering of the MVA pathway to upgrade linalool content in both the mitochondria and cytoplasm of S. cerevisiae. This was achieved by introducing MVA genes into both cellular compartments, with mitochondrial localization signal [MLS] fused to the genes for transfer into mitochondria. Thus, they constructed a strain of S. cerevisiae in which the expression of LINS from Cinnamomum osmophloeum and ERG20F96W−N127W occurred in the cytoplasm and mitochondria. This recombinant S. cerevisiae exhibited increased linalool production (7.61 mg L−1). Moreover, they cultured the recombinant S. cerevisiae in media containing varying amounts of PYR and mevalonolactone as carbon sources. Notably, the medium supplemented with 70 mg L−1 mevalonolactone yielded the highest linalool concentration. Park et al. [52] enhanced linalool production by integrating an inducible sensor array into the genomic DNA of S. cerevisiae. This sensor array was comprised of sequences encoding repressor proteins controlled by constitutive promoters and strong terminators, allowing for individual or simultaneous expression upon exposure to sensor molecules in the medium. The sensor molecules employed included xylose, anhydrotetracycline, vanillic acid, and IPTG which induced the expression of LINS from M. citrata.

Kirby et al. [53] significantly enhanced 1,8-cineole production in Rhodotorula toruloides by employing an N-terminal truncated GPPS from Abies grandis and a CINS from Hypoxilon sp. These synthases were introduced into R. toruloides under the control of promoters sourced from the R. toruloides genome. Subsequently, the titer increased further through medium optimization. Ma et al. [54] overexpressed (+)-bornyl diphosphate synthase [BPPS] from Cinnamomum burmanni along with all genes involved in the MVA pathway in S. cerevisiae to produce (+)-borneol. (+)-Borneol production was further significantly increased by N-terminal truncation of BPPS and incorporating a Kozak sequence. In another study by the same researcher, Ma et al. [55], (−)-BPPS from Blumea balsamifera was identified and functionally characterized and then introduced into S. cerevisiae. Similar to the previous experiment, N-terminal truncation of BPPS and the addition of a Kozak sequence were utilized to enhance (−)-borneol production. Finally, the fusion of (−)-BPPS with ERG20F96W−N127W resulted in a further increase in the production of (−)-borneol.

2.7.2.2 Production of lavender monoterpenes in bacteria

Wu et al. [56] employed a scaffolding strategy to produce linalool in E. coli. They constructed scaffolds consisting of three domains for IPPS, GPPS and LINS enzymes, with different domain repeats for GPPS and LINS. Ligands were attached to the enzymes via linkers. The scaffold featuring one domain for IPPS, one for GPPS, and four for LINS exhibited the highest linalool production. Additionally, they optimized the concentrations of IPTG (0.5 mM), L-arabinose (0.3%), and glycerol (4%) in the medium, with an identified optimal temperature of 20º C for linalool production. Kong et al. [57] produced linalool in E. coli by designing and introducing a heterologous MVA pathway, which included genes involved in IPP and DMAPP accumulation, GPP formation, and linalool production. They showed that GPPS2 from A. grandis had a more significant effect on linalool production compared to ERG20. The lower efficiency of ERG20 in linalool production was attributed to its bifunctional activity, resulting in the production of both GPP and FPP. The recombinant E. coli strain harboring the new MVA pathway produced 15 ± 1.4 mg L−1 linalool. The linalool concentration further increased to 63 ± 5.6 mg L−1 with the overexpression of isopentenyl diphosphate isomerases. In a study by Wang et al. [58], linalool production in E. coli was enhanced through LINS modification. Initially, the most efficient LINS (4.8 mg L−1) was obtained from Streptomyces clavuligerus [bLIS]. Then, bLIS variants with different ribosomal binding sites [RBS] and translation initiation rate [TIR] were constructed. The results demonstrated a positive correlation between bLIS expression and TIR. Additionally, a fusion tag was added to increase bLIS solubility, resulting in enhanced linalool production to 33.4 mg L−1. Further optimization strategy included the addition of GPSS from A. grandis to ensure sufficient GPP availability, leading to linalool production reaching 100.1 mg L−1. Finally, culturing the recombinant E. coli in a bioreactor with fed-batch fermentation achieved a significant increase in linalool production to 1027.3 mg L−1.

Mendez-Perez et al. [59] achieved significant 1,8-cineole production (228 mg L−1) in E. coli by constructing and introducing a plasmid harboring genes related to the MVA pathway along with the CINS gene from Streptomyces clavuligerus. To further enhance 1,8-cineole production, they inserted an additional plasmid containing another copy of CINS into E. coli. This two-plasmid system led to a 33% increase in 1,8-cineole production, reaching up to 305 mg L−1. The higher level of 1,8-cineole (505 mg L−1) was achieved when CINS and GPPS were harbored in one plasmid and other genes were placed in another plasmid. Karuppiah et al. [60] inserted LINS and CINS genes from Streptomyces clavuligerus into an engineered E. coli strain, where the MVA pathway was regulated by an IPTG-inducible promoter, and an N-terminal truncated GPPS was controlled by a tetracycline-inducible promoter. This approach resulted in the production of a remarkable amount of linalool and 1,8-cineole, with the latter exhibiting a higher purity (96%) compared to those obtained from Salvia fruticose, Arabidopsis thaliana and Citrus unshiu which had purities of 67%, 42% and 63%, respectively.

Lei et al. [61] engineered the de novo production of borneol in E. coli. They co-expressed a mutant BPPS enzyme from Lippia dulcis, where a single-point mutation enhanced enzymatic activity, along with an endogenous phosphatase from E. coli to facilitate the dephosphorylation of precursors to borneol. This strategy led to a notable enhancement in borneol content under optimized fermentation condition.

2.7.2.3 Production of lavender monoterpenes in Cyanobacteria

Matsudaira et al. [62] engineered a cyanobacterium strain capable of producing S-linalool. In this strain, the LINS coding sequence from Actinidia arguta was codon-optimized for the cyanobacterium and expressed under the control of tac promoter. This strain produced 11.4 mg L−1 of S-linalool in shake flask culture. The S-linalool concentration further increased to 11.6 mg L−1 with the expression of a mutated farnesyl diphosphate synthase derived from E. coli.

Sakamaki et al. [63] reported the photosynthetic production of 1,8-cineole in cyanobacteria. They designed and constructed a codon-optimized CINS gene from Streptomyces clavuligerus for producing 1,8-cineole in Synechococcus elongatus. They placed this CINS under the control of an IPTG-dependent promoter since it could produce 1,8-cineole directly from GPP, unlike other CINS that convert terpineol into 1,8-cineole. Although the amount of 1,8-cineole produced in their attempt was not remarkable and further attempts are needed, their study showed the feasibility of producing 1,8-cineole without the need for carbon sources like sucrose.

3 Conclusion

By now, most terpene synthase genes responsible for the production of lavender EO monoterpenes have been cloned and functionally characterized. Further, many of these genes have been used to produce the corresponding monoterpenes in bacteria, yeast, and model plants such as Arabidopsis and tobacco. Additionally, the metabolic engineering of lavender has been investigated. In the latter case, success has been limited as the constitutive overexpression of terpene synthase genes is often detrimental to the host plant, as (presumably) non-GT cells cannot tolerate large amounts of the monoterpenes they produce. This problem may be resolved if GT-specific promoters that can direct the expression of transgenes specifically in GTs are used. In this context, ongoing studies currently focus on the cloning of GT-specific promoters. Such promoters could not only help enhance EO quality and yield in lavender, but also assist researchers in using this plant as a bioreactor for the large-scale production of valuable phytochemicals.

Availability of data and materials

Not applicable.

Abbreviations

AT:

Acetyltransferase

BDH:

(+)-Borneol dehydrogenase

bHLH:

Basic helix-loop-helix

bLIS:

LINS (from Streptomyces clavuligerus)

BPP:

Bornyl diphosphate

BPPS:

Bornyl diphosphate synthase

CaMV:

Cauliflower Mosaic Virus

CINS:

1,8-Cineole synthase

CMK:

4-(Cytidine 5′-diphospho)- 2-C-methyl-D-erythritol-kinase

DMAPP:

Dimethylallyl diphosphate

DXP:

1-Deoxy-D-xylulose-5-phosphate

DXR:

DXP reductoisomerase

DXS:

DXP synthase

EOs:

Essential oils

ERG20:

Farnesyl diphosphate synthase

FPP:

Farnesyl diphosphate

G3P:

Glyceraldehyde 3-phosphate

GC–MS:

Gas chromatography/mass spectrometry

GGPP:

Geranylgeranyl diphosphate

GPP:

Geranyl diphosphate

GPPS:

Geranyl diphosphate synthase

GT:

Glandular trichome

HDS:

HMBPP synthase

HDR:

HMBPP reductase

HMBPP:

1-Hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate

IDSs:

Isoprenyl diphosphate synthases

IPP:

Isopentenyl diphosphate

IUP:

Isopentenol Utilization Pathway

LaAG-like:

LaAGAMOUS-like (from L. angustifolia)

LaBERS:

Bergamotene synthase (from L. angustifolia)

LabPHLS:

β-Phellandrene synthase (from L. angustifolia)

LaSEP3-like:

LaSEPALLATA3- like (from L. angustifolia)

LaSVP:

Short vegetative phase gene (from l. angustifolia)

LaTPS7:

Terpene synthase 7 (from L. angustifolia)

LaTPS8:

Terpene synthase 7 (from L. angustifolia)

Li3CARS:

3-Carene synthase (from L. x intermedia)

LiAAT:

Alcohol acetyltransferase (from L. x intermedia)

LiBDH:

Borneol dehydrogenase (from L. x intermedia)

LiBPPS:

Bornyl diphosphate synthase (from L. x intermedia)

LiCINS:

CINS (from L. x intermedia)

LiCPS:

Caryophyllene synthase (from L. x intermedia)

LiLPPS:

Lavandulyl diphosphate synthase (from L. x intermedia)

LIMS:

Limonene synthase

LINS:

Linalool synthase

LiS-LINS:

S-linalool synthase (from L. x intermedia)

LpFENS:

Fenchol synthase (from L. pedunculata)

LpGEAS:

Germacrene A synthase (from L. pedunculata)

LpPINS:

α-Pinene synthase (from L. pedunculata)

LPP:

Lavandulyl diphosphate

LPPS:

Lavandulyl diphosphate synthase

MCT:

MEP cytidyltransferase

MDS:

MEcPP synthase

MEcPP:

2-C-methyl-D-erythritol -2,4-cyclodiphosphate

MeJA:

Methyl jasmonate

MEP:

2-C-Methyl-D-erythritol 4-phosphate

MLS:

Mitochondrial localization signal

monoTPSs:

Monoterpene synthases

MVA:

Mevalonate

NPP:

Neryl diphosphate

NPPS:

Neryl diphosphate synthase

PYR:

Pyruvate

RBS:

Ribosomal binding site

SesquiTPSs:

Sesquiterpene synthases

TFs:

Transcription factors

TIR:

Translation initiation rates

TPS:

Terpene synthase

VOC:

Volatile organic compound

References

  1. Landmann C, Fink B, Festner M, Dregus M, Engel KH, Schwab W (2007) Cloning and functional characterization of three terpene synthases from lavender (Lavandula angustifolia). Arch Biochem Biophys 465(2):417–429. https://doi.org/10.1016/j.abb.2007.06.011

    Article  CAS  PubMed  Google Scholar 

  2. Sarker LS, Galata M, Demissie ZA, Mahmoud SS (2012) Molecular cloning and functional characterization of borneol dehydrogenase from the glandular trichomes of Lavandula x intermedia. Arch Biochem Biophys 528(2):163–170. https://doi.org/10.1016/j.abb.2012.09.013

    Article  CAS  PubMed  Google Scholar 

  3. Woronuk G, Demissie Z, Rheault M, Mahmoud SS (2011) Biosynthesis and therapeutic properties of lavandula essential oil constituents. Planta Med 77(01):7–15. https://doi.org/10.1055/s-0030-1250136

    Article  CAS  PubMed  Google Scholar 

  4. Demissie ZA, Cella MA, Sarker LS, Thompson TJ, Rheault MR, Mahmoud SS (2012) Cloning, functional characterization and genomic organization of 1,8-cineole synthases from Lavandula. Plant Mol Biol 79:393–411. https://doi.org/10.1007/s11103-012-9920-3

    Article  CAS  PubMed  Google Scholar 

  5. Aprotosoaie AC, Gille E, Trifan A, Luca VS, Miron A (2017) Essential oils of Lavandula genus: a systematic review of their chemistry. Phytochem Rev 16:761–799. https://doi.org/10.1007/s11101-017-9517-1

    Article  CAS  Google Scholar 

  6. Mahmoud SS, Maddock S, Adal AM (2021) Isoprenoid Metabolism and Engineering in Glandular Trichomes of Lamiaceae. Front Plant Sci 12:699157. https://doi.org/10.3389/fpls.2021.699157

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sarker LS, Mahmoud SS (2015) Cloning and functional characterization of two monoterpene acetyltransferases from glandular trichomes of L. x intermedia. Planta 242:709–719. https://doi.org/10.1007/s00425-015-2325-1

    Article  CAS  PubMed  Google Scholar 

  8. Adal AM, Sarker LS, Lemke AD, Mahmoud SS (2017) Isolation and functional characterization of a methyl jasmonate-responsive 3-carene synthase from Lavandula x intermedia. Plant Mol Biol 93:641–657. https://doi.org/10.1007/s11103-017-0588-6

    Article  CAS  PubMed  Google Scholar 

  9. Benabdelkader T, Guitton Y, Pasquier B, Magnard JL, Jullien F, Kameli A, Legendre L (2015) Functional characterization of terpene synthases and chemotypic variation in three lavender species of section Stoechas. Physiol Plant 153(1):43–57. https://doi.org/10.1111/ppl.12241

    Article  CAS  PubMed  Google Scholar 

  10. Upson T, Andrews S, Harriott G, King C, Langhorne J (2004) The Genus Lavandula. Timber Press, Portland, OR

    Google Scholar 

  11. Booth JK, Page JE, Bohlmann J (2017) Terpene synthases from Cannabis sativa. PLoS ONE 12(3):e0173911. https://doi.org/10.1371/journal.pone.0173911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ma Y, Yuan L, Wu B, Li X, Chen S, Lu S (2012) Genome-wide identification and characterization of novel genes involved in terpenoid biosynthesis in Salvia miltiorrhiza. J Exp Bot 63(7):2809–2823. https://doi.org/10.1093/jxb/err466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sapir-Mir M, Mett A, Belausov E, Tal-Meshulam S, Frydman A, Gidoni D, Eya Y (2008) Peroxisomal localization of arabidopsis isopentenyl diphosphate isomerases suggests that part of the plant isoprenoid mevalonic acid pathway is compartmentalized to peroxisomes. Plant Physiol 148(3):1219–1228. https://doi.org/10.1104/pp.108.127951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Simkin AJ, Guirimand G, Papon N, Courdavault V, Thabet I, Ginis O, Bouzid S, Giglioli-Guivarc’h N, Clastre M, (2011) Peroxisomal localisation of the final steps of the mevalonic acid pathway in planta. Planta 234:903–914. https://doi.org/10.1007/s00425-011-1444-6

    Article  CAS  PubMed  Google Scholar 

  15. Huang S, Kirchoff BK, Liao J (2008) The capitate and peltate glandular trichomes of Lavandula pinnata L. (Lamiaceae): histochemistry, ultrastructure, and secretion1. J Torrey Bot Soc 135(2):155–167. https://doi.org/10.3159/07-RA-045.1

    Article  Google Scholar 

  16. Huchelmann A, Boutry M, Hachez C (2017) Plant glandular trichomes: Natural cell factories of high biotechnological interest. Plant Physiol 175(1):6–22. https://doi.org/10.1104/pp.17.00727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136(4):4215–4227. https://doi.org/10.1104/pp.104.050229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Boeckelmann A (2008) Monoterpene production and regulation in lavenders (Lavandula angustifolia and Lavandula x intermedia). Doctoral dissertation, University of British Columbia. https://doi.org/10.14288/1.0066802

  19. Wagner GJ (1991) Secreting glandular trichomes: more than just hairs. Plant Physiol 96(3):675–679. https://doi.org/10.1104/pp.96.3.675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Turner GW, Gershenzon J, Croteau RB (2000) Distribution of peltate glandular trichomes on developing leaves of peppermint. Plant Physiol 124(2):655–664. https://doi.org/10.1104/pp.124.2.655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Tian H, Wang X, Guo H, Cheng Y, Hou C, Chen JG, Wang S (2017) NTL8 regulates trichome formation in Arabidopsis by directly activating R3 MYB genes TRY and TCL1. Plant Physiol 174(4):2363–2375. https://doi.org/10.1104/pp.17.00510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhang Y, Wang D, Li H, Bai H, Sun M, Shi L (2023) Formation mechanism of glandular trichomes involved in the synthesis and storage of terpenoids in lavender. BMC Plant Biol 23(1):307. https://doi.org/10.1186/s12870-023-04275-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198(1):16–32. https://doi.org/10.1111/nph.12145

    Article  CAS  PubMed  Google Scholar 

  24. Huang Y, Xie FJ, Cao X, Li MY (2021) Research progress in biosynthesis and regulation of plant terpenoids. Biotechnol Biotechnol Equip 35(1):1799–1808. https://doi.org/10.1080/13102818.2021.2020162

    Article  CAS  Google Scholar 

  25. Kuzuyama T, Takahashi S, Watanabe H, Seto H (1998) Direct formation of 2-C-methyl-D-erythritol 4-phosphate from 1-deoxy-D-xylulose 5-phosphate by 1-deoxy-D-xylulose 5-phosphate reductoisomerase, a new enzyme in the non-mevalonate pathway to isopentenyl diphosphate. Tetrahedron Lett 39(25):4509–4512. https://doi.org/10.1016/S0040-4039(98)00802-8

    Article  CAS  Google Scholar 

  26. Calisto BM, Perez-Gil J, Bergua M, Querol-Audi J, Fita I, Imperial S (2007) Biosynthesis of isoprenoids in plants: structure of the 2C-methyl-d-erithrytol 2,4-cyclodiphosphate synthase from Arabidopsis thaliana. Comparison with the bacterial enzymes. Protein Sci 16(9):2082–2088. https://doi.org/10.1110/ps.072972807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Bergman ME, Davis B, Phillips MA (2019) Medically useful plant terpenoids: biosynthesis, occurrence, and mechanism of action. Molecules 24(21):3961. https://doi.org/10.3390/molecules24213961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Altincicek B, Kollas AK, Eberl M, Wiesner J, Sanderbrand S, Hintz M, Beck E, Jomaa H (2001) LytB, a novel gene of the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli. FEBS Lett 499(1–2):37–40. https://doi.org/10.1016/S0014-5793(01)02516-9

    Article  CAS  PubMed  Google Scholar 

  29. Botella-Pavía P, Besumbes Ó, Phillips MA, Carretero-Paulet L, Boronat A, Rodríguez-Concepción M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40(2):188–199. https://doi.org/10.1111/j.1365-313X.2004.02198.x

    Article  CAS  PubMed  Google Scholar 

  30. Seemann M, Bui BTS, Wolff M, Miginiac-Maslow M, Rohmer M (2006) Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: Direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG. FEBS Lett 580(6):1547–1552. https://doi.org/10.1016/j.febslet.2006.01.082

    Article  CAS  PubMed  Google Scholar 

  31. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. The Arabidopsis Book/American Society of Plant Biologists. https://doi.org/10.1199/Ftab.0143

    Article  PubMed Central  Google Scholar 

  32. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR (2012) Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13(12):17077–17103. https://doi.org/10.3390/ijms131217077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lange BM (2015) Biosynthesis and biotechnology of high-value p-menthane monoterpenes, including menthol, carvone, and limonene. Biotechnol Isopren. https://doi.org/10.1007/10_2014_289

    Article  Google Scholar 

  34. Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70(15–16):1621–1637. https://doi.org/10.1016/j.phytochem.2009.07.030

    Article  CAS  PubMed  Google Scholar 

  35. Jia Q, Brown R, Köllner TG, Fu J, Chen X, Ka-Shu Wong GKS, Gershenzon J, Peters RJ, Chen F (2022) Origin and early evolution of the plant terpene synthase family. Proc Natl Acad Sci USA 119(15):e2100361119. https://doi.org/10.1073/pnas.2100361119

    Article  PubMed  PubMed Central  Google Scholar 

  36. Demissie ZA, Sarker LS, Mahmoud SS (2011) Cloning and functional characterization of β-phellandrene synthase from Lavandula angustifolia. Planta 233:685–696. https://doi.org/10.1007/s00425-010-1332-5

    Article  CAS  PubMed  Google Scholar 

  37. Demissie ZA, Erland LAE, Rheault MR, Mahmoud SS (2013) The biosynthetic origin of irregular monoterpenes in lavandula: Isolation and biochemical characterization of a novel cis-prenyl diphosphate synthase gene, lavandulyl diphosphate synthase. J Biol Chem 288(9):6333–6341. https://doi.org/10.1074/jbc.M112.431171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sarker LS, Demissie ZA, Mahmoud SS (2013) Cloning of a sesquiterpene synthase from Lavandula x intermedia glandular trichomes. Planta 238:983–989. https://doi.org/10.1007/s00425-013-1937-6

    Article  CAS  PubMed  Google Scholar 

  39. Adal AM, Sarker LS, Malli RPN, Liang P, Mahmoud SS (2019) RNA-Seq in the discovery of a sparsely expressed scent-determining monoterpene synthase in lavender (Lavandula). Planta 249:271–290. https://doi.org/10.1007/s00425-018-2935-5

    Article  CAS  PubMed  Google Scholar 

  40. Adal AM, Najafianashrafi E, Sarker LS, Mahmoud SS (2023) Cloning, functional characterization and evaluating potential in metabolic engineering for lavender (+)-bornyl diphosphate synthase. Plant Mol Biol 111(1):117–130. https://doi.org/10.1007/s11103-022-01315-3

    Article  CAS  PubMed  Google Scholar 

  41. Ling Z, Li J, Dong Y, Zhang W, Bai H, Li S, Wang S, Li H, Shi L (2023) Terpene produced by coexpression of the TPS and P450 genes from Lavandula angustifolia protects plants from herbivore attacks during budding stages. BMC Plant Biol 23(1):477. https://doi.org/10.1186/s12870-023-04490-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Guitton Y, Nicolè F, Moja S, Valot N, Legrand S, Jullien F, Legendre L (2010) Differential accumulation of volatile terpene and terpene synthase mRNAs during lavender (Lavandula angustifolia and L. x intermedia) inflorescence development. Physiol Plant 138(2):150–163. https://doi.org/10.1111/j.1399-3054.2009.01315.x

    Article  CAS  PubMed  Google Scholar 

  43. Wells RS, Adal AM, Bauer L, Najafianashrafi E, Mahmoud SS (2020) Cloning and functional characterization of a floral repressor gene from Lavandula angustifolia. Planta 251:1–11. https://doi.org/10.1007/s00425-019-03333-w

    Article  CAS  Google Scholar 

  44. Adal AM, Binson E, Remedios L, Mahmoud SS (2021) Expression of lavender AGAMOUS-like and SEPALLATA3-like genes promote early flowering and alter leaf morphology in Arabidopsis thaliana. Planta 254(3):54. https://doi.org/10.1007/s00425-021-03703-3

    Article  CAS  PubMed  Google Scholar 

  45. Dong Y, Zhang W, Li J, Wang D, Bai H, Li H, Shi L (2022) The transcription factor LaMYC4 from lavender regulates volatile Terpenoid biosynthesis. BMC Plant Biol 22(1):289. https://doi.org/10.1186/s12870-022-03660-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Muñoz-Bertomeu J, Arrillaga I, Ros R, Segura J (2006) Up-regulation of 1-Deoxy-D-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142(3):890–900. https://doi.org/10.1104/pp.106.086355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Tsuro M, Ikedo H (2011) Changes in morphological phenotypes and essential oil components in lavandin (Lavandula×intermedia Emeric ex Loisel) transformed with wild-type strains of Agrobacterium rhizogenes. Sci Hortic 130(3):647–652. https://doi.org/10.1016/j.scienta.2011.08.011

    Article  CAS  Google Scholar 

  48. Deng Y, Sun M, Xu S, Zhou J (2016) Enhanced (S)-linalool production by fusion expression of farnesyl diphosphate synthase and linalool synthase in Saccharomyces cerevisiae. J Appl Microbiol 121(1):187–195. https://doi.org/10.1111/jam.13105

    Article  CAS  PubMed  Google Scholar 

  49. Zhang Y, Cao X, Wang J, Tang F (2022) Enhancement of linalool production in Saccharomyces cerevisiae by utilizing isopentenol utilization pathway. Microb Cell Fact 21(1):212. https://doi.org/10.1186/s12934-022-01934-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhou P, Du Y, Xu N, Yue C, Ye L (2020) Improved linalool production in Saccharomyces cerevisiae by combining directed evolution of linalool synthase and overexpression of the complete mevalonate pathway. Biochem Eng J 161:107655. https://doi.org/10.1016/j.bej.2020.107655

    Article  CAS  Google Scholar 

  51. Zhang Y, Wang J, Cao X, Liu W, Yu H, Ye L (2020) High-level production of linalool by engineered Saccharomyces cerevisiae harboring dual mevalonate pathways in mitochondria and cytoplasm. Enzyme Microb Technol 134:109462. https://doi.org/10.1016/j.enzmictec.2019.109462

    Article  CAS  PubMed  Google Scholar 

  52. Park JH, Bassalo MC, Lin GM, Chen Y, Doosthosseini H, Schmitz J, Roubos JA, Voigt CA (2023) Design of four small-molecule-inducible systems in the yeast chromosome, applied to optimize terpene biosynthesis. ACS Synth Biol 12(4):1119–1132. https://doi.org/10.1021/acssynbio.2c00607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kirby J, Geiselman GM, Yaegashi J, Kim J, Zhuang X, Tran-Gyamfi MB, Prahl JP, Sundstrom ER, Gao Y, Munoz N, Burnum-Johnson KE, Benites VT, Baidoo EEK, Fuhrmann A, Seibel K, Webb-Robertson BJM, Zucker J, Nicora CD, Tanjore D, Magnuson JK, Skerker JM, Gladden JM (2021) Further engineering of R. toruloides for the production of terpenes from lignocellulosic biomass. Biotechnol Biofuels 14:1–16. https://doi.org/10.1186/s13068-021-01950-w

    Article  CAS  Google Scholar 

  54. Ma R, Su P, Guo J, Jin B, Ma Q, Zhang H, Chen L, Mao L, Tian M, Lai C, Tang J, Cui G, Huang L (2021) Bornyl diphosphate synthase from Cinnamomum burmanni and its application for (+)-borneol biosynthesis in yeast. Front Bioeng Biotechnol 9:631863. https://doi.org/10.3389/fbioe.2021.631863

    Article  PubMed  PubMed Central  Google Scholar 

  55. Ma R, Su P, Ma Q, Guo J, Chen S, Jin B, Zhang H, Tang J, Zhou T, Xiao C, Cui G, Huang L (2022) Identification of (−)-bornyl diphosphate synthase from Blumea balsamifera and its application for (−)-borneol biosynthesis in Saccharomyces cerevisiae. Synth Syst Biotechnol 7(1):490–497. https://doi.org/10.1016/j.synbio.2021.12.004

    Article  CAS  PubMed  Google Scholar 

  56. Wu J, Wang X, Xiao L, Wang F, Zhang Y, Li X (2021) Synthetic protein scaffolds for improving R-(−)-linalool production in escherichia coli. J Agric Food Chem 69(20):5663–5670. https://doi.org/10.1021/acs.jafc.1c01101

    Article  CAS  PubMed  Google Scholar 

  57. Kong S, Fu X, Li X, Pan H, Guo D (2020) De novo biosynthesis of linalool from glucose in engineered Escherichia coli. Enzyme Microb Technol 140:109614. https://doi.org/10.1016/j.enzmictec.2020.109614

    Article  CAS  PubMed  Google Scholar 

  58. Wang X, Wu J, Chen J, Xiao L, Zhang Y, Wang F, Li X (2020) Efficient biosynthesis of R-(-)-linalool through adjusting the expression strategy and increasing GPP supply in Escherichia coli. J Agric Food Chem 68(31):8381–8390. https://doi.org/10.1021/acs.jafc.0c03664

    Article  CAS  PubMed  Google Scholar 

  59. Mendez-Perez D, Alonso-Gutierrez J, Hu Q, Molinas M, Baidoo EEK, Wang G, Chan LJG, Adams PD, Petzold CJ, Keasling JD, Lee TS (2017) Production of jet fuel precursor monoterpenoids from engineered Escherichia coli. Biotechnol Bioeng 114(8):1703–1712. https://doi.org/10.1002/bit.26296

    Article  CAS  PubMed  Google Scholar 

  60. Karuppiah V, Ranaghan KE, Leferink NGH, Johannissen LO, Shanmugam M, Ní Cheallaigh A, Bennett NJ, Kearsey LJ, Takano E, Gardiner JM, Van Der Kamp MW, Hay S, Mulholland AJ, Leys D, Scrutton NS (2017) Structural basis of catalysis in the bacterial monoterpene synthases linalool synthase and 1,8-cineole synthase. ACS Catal 7(9):6268–6282. https://doi.org/10.1021/acscatal.7b01924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lei D, Qiu Z, Wu J, Qiao B, Qiao J, Zhao GR (2021) Combining metabolic and monoterpene synthase engineering for de novo production of monoterpene alcohols in Escherichia coli. ACS Synth Biol 10(6):1531–1544. https://doi.org/10.1021/acssynbio.1c00081

    Article  CAS  PubMed  Google Scholar 

  62. Matsudaira A, Hoshino Y, Uesaka K, Takatani N, Omata T, Usuda Y (2020) Production of glutamate and stereospecific flavors, (S)-linalool and (+)-valencene, by Synechocystis sp. PCC6803. J Biosci Bioeng 130(5):464–470. https://doi.org/10.1016/j.jbiosc.2020.06.013

    Article  CAS  PubMed  Google Scholar 

  63. Sakamaki Y, Ono M, Shigenari N, Chibazakura T, Shimomura K, Watanabe S (2023) Photosynthetic 1,8-cineole production using cyanobacteria. Biosci Biotechnol Biochem 87(5):563–568. https://doi.org/10.1093/bbb/zbad012

    Article  PubMed  Google Scholar 

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Oseni, O.M., Sajaditabar, R. & Mahmoud, S.S. Metabolic engineering of terpene metabolism in lavender. Beni-Suef Univ J Basic Appl Sci 13, 67 (2024). https://doi.org/10.1186/s43088-024-00524-7

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