Ionone: Its Occurrence and Biological Function and Metabolic Engineering
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plants Review β-Ionone: Its Occurrence and Biological Function and Metabolic Engineering Antonello Paparella 1 , Liora Shaltiel-Harpaza 2,3 and Mwafaq Ibdah 4,* 1 Faculty of Bioscience and Technology for Food, Agriculture, and Environment, University of Teramo, Via Balzarini 1, 64100 Teramo, Italy; [email protected] 2 Migal Galilee Research Institute, P.O. Box 831, Kiryat Shmona 11016, Israel; [email protected] 3 Tel Hai College, P.O. Box 831, Kiryat Shmona, Upper Galilee 12210, Israel 4 Newe Yaar Research Center, Agricultural Research Organization, P.O. Box 1021, Ramat Yishay 30095, Israel * Correspondence: [email protected]; Tel.: +972-4-953-9537; Fax: +972-4-983-6936 Abstract: β-Ionone is a natural plant volatile compound, and it is the 9,10 and 90,100 cleavage product of β-carotene by the carotenoid cleavage dioxygenase. β-Ionone is widely distributed in flowers, fruits, and vegetables. β-Ionone and other apocarotenoids comprise flavors, aromas, pigments, growth regulators, and defense compounds; serve as ecological cues; have roles as insect attractants or repellants, and have antibacterial and fungicidal properties. In recent years, β-ionone has also re- ceived increased attention from the biomedical community for its potential as an anticancer treatment and for other human health benefits. However, β-ionone is typically produced at relatively low levels in plants. Thus, expressing plant biosynthetic pathway genes in microbial hosts and engineering the metabolic pathway/host to increase metabolite production is an appealing alternative. In the β β present review, we discuss -ionone occurrence, the biological activities of -ionone, emphasizing insect attractant/repellant activities, and the current strategies and achievements used to reconstruct enzyme pathways in microorganisms in an effort to to attain higher amounts of the desired β-ionone. Citation: Paparella, A.; Shaltiel-Harpaza, L.; Ibdah, M. β β-Ionone: Its Occurrence and Keywords: biological activity; biosynthesis; -ionone; insect attractant/repellant; metabolic engineering Biological Function and Metabolic Engineering. Plants 2021, 10, 754. https://doi.org/10.3390/ plants10040754 1. Introduction Plant volatile organic compounds (VOCs) are specialized metabolites, which have Academic Editor: Laura Cornara been described from more than 90 plant families [1,2]. A wide diversity of compounds are emitted from leaves, flowers, fruits, bark, and roots, as well as from specialized storage Received: 16 March 2021 structures, e.g., glands [1,2]. VOCs are lipophilic liquids and have low molecular mass Accepted: 11 April 2021 (<300 Da) with high vapor pressures. Plant VOCs are derived from various biosynthesis Published: 12 April 2021 pathways and are often classified into significant groups, including phenylpropanoids, fatty acids, amino acids, and terpenoids [3]. Publisher’s Note: MDPI stays neutral VOCs are primarily intended to protect plants against pathogens and herbivores with regard to jurisdictional claims in or to provide a reproductive benefit in attracting pollinators and seed dispersers [3–7]. published maps and institutional affil- Plant VOCs have attracted considerable scientific interest for commercial applications, e.g., iations. decorative cosmetics, shampoos, and fine fragrances, as well as for their potential benefits for human health [8–10]. Ionone is a ketone with a monocyclic terpenoid backbone made up of 13 carbon atoms. The name “ionone” is derived from “iona” (Greek for violet), which refers to the violet Copyright: © 2021 by the authors. odor, and “ketone,” which refers to the structure of the ionone [11,12]. β-Ionone is the 9,10 Licensee MDPI, Basel, Switzerland. and 90,100 cleavage product of β-carotene (Figure1)[13–16]. This article is an open access article It is a common aromatic volatile found in various tissues in many plant species, e.g., distributed under the terms and in the essential oil (EO) of Osmanthus fragrans, Petunia hybrid, and Rosa bourboniana, and in conditions of the Creative Commons fruits and vegetables, including carrot, tomato, melon, raspberry, apricot, plum, apple, and Attribution (CC BY) license (https:// β creativecommons.org/licenses/by/ fig [14,17–21]. -Ionone has become quite attractive for commercial applications and in 4.0/). medical and pharmaceutical industries [22–28]. Plants 2021, 10, 754. https://doi.org/10.3390/plants10040754 https://www.mdpi.com/journal/plants Plants 2021, 10, 754 Plants 2021, 10, 754 2 of 12 2 of 12 Figure 1. Production of β-ionone from β-carotene by carotenoid cleavage dioxygenase 1 (CCD1). Figure 1. Production of β-ionone from β-carotene by carotenoid cleavage dioxygenase 1 (CCD1). This review aims to highlight the latest advances concerning the occurrence and the It is a common biologicalaromatic activities volatile of foundβ-ionone, in various and the currenttissues state in many of knowledge plant species, about its applicatione.g., in different industrial environments. in the essential oil (EO) of Osmanthus fragrans, Petunia hybrid, and Rosa bourboniana, and in fruits and vegetables,2. Occurrenceincluding ofcarrot,β-Ionone tomato, melon, raspberry, apricot, plum, apple, and fig [14,17–21]. β-IononeHeadspace has become solid-phase quite microextraction attractive for (HS-SPME) commercial was applications used to obtain and the EO of in medical and pharmaceuticalOsmanthus fragrans industries, which [22–28]. was then analyzed by gas chromatography–mass spectrometry (GC–MS) at four different stages of flowering. The primary chemical components of the This review aims to highlight the latest advances concerning the occurrence and the EO obtained from O. fragrans were β-ionone, a-ionone, and other VOCs, e.g., linalool biological activities ofand β-ionone, nerol [29]. and Capillary the current GC–MS withstate olfactometry of knowledge analysis about was its used application to determine the in different industrialvolatile environments. profile of samples of Thymus vulgaris EO. The compounds with the highest aroma impact for T. vulgaris were β-ionone, borneol, terpinyl acetate, and β-damascenone [30]. 2. Occurrence of β-IononeThe EO of the leaves of Lawsonia inermis L. (henna) was found to contain β-ionone as one of its major components [31]. The EO of the genus Rosa (Rosaceae) is commercially Headspace solid-phasecrucial in microextraction the fragrance and food(HS-SPME) industries was [32– used34]. Honarvar to obtain et the al. [EO35] reportedof Os- that manthus fragrans, whichEOs ofwas fresh then and analyzed dried flowers by of gas Musk chromatography–mass Rose contain approximately spectrometry 2% of β-ionone of (GC–MS) at four differentthe total stages chemical of constitutes.flowering. In The the EOprimary obtained chemical from fresh components aerial parts of ofViola the tricolor (Violaceae), Anca et al. [36] identified 35 VOCs, and β-ionone constituted around 2% of the EO obtained from O. fragrans were β-ionone, α-ionone, and other VOCs, e.g., linalool and total. The chemical composition of the EO from different stages of Medicago marina was nerol [29]. Capillary analyzed,GC–MS andwithβ -iononeolfactometry was one analys of the mainis was constituents used to ofdetermine the flowering the samples volatile (6%) but profile of samples ofincreased Thymus during vulgaris the EO. vegetative The compounds stage (14%) [37 ].withβ-Ionone the highest was also aroma determined impact at different for T. vulgaris were βpercentages-ionone, borneol, in the EOs terpinyl of Moroccan acetate, herbs, and namely β-damascenoneMyrtus communis [30]., Cistus The ladanifer EO , and β of the leaves of LawsoniaMontpellier inermis cistus L.[ 38(henna)]. In contrast, was found in the EOto ofcontain maca ( Lepidiumβ-ionone meyenii as one), -iononeof its was found to be a minor component [39] (Figure2). major components [31]. TheThe aroma EO of of fruitsthe genus and vegetables Rosa (Rosaceae) is determined is commercially by unique combinations crucial ofinVOCs, the fragrance and foodincluding industriesβ-ionone [32–34]. (Figure Hona3), althoughrvar et different al. [35] fruits, reported roots, andthat vegetables EOs of fresh often share and dried flowers ofmany Musk aroma Rose characteristics. contain approximately Yahyaa et al. [ 152%] analyzed of β-ionone the VOC of compositionthe total chem- in the roots ical constitutes. In theof EO various obtained carrot genotypesfrom fresh with aerial different parts colors of Viola (orange, tricolor purple, (Violaceae), white, and yellow). Anca They found that only orange and purple carrot roots accumulate β-ionone; white and yellow et al. [36] identified 35carrot VOCs, roots and do notβ-ionone [15]. β-Ionone constituted was also around identified 2% of in thethe chemicaltotal. The compositions chem- of ical composition of theEOs EO of Daucusfrom different carota subsp. stagessativus of Medicago[40]. Guillot marina et al. [was41] characterized analyzed, and the aromaticβ- ionone was one of theprofile main of co severalnstituents apricot of cultivars the flowering (Iranien, sa Orangered,mples (6%) Goldrich, but increased Hargrand, dur- Rouge du ing the vegetative stageRoussillon, (14%) [37]. and A4025) β-Ionone by using was HS-SPME.also determined In the apricot, at different several percentages VOCs, including β- in the EOs of Moroccan herbs, namely Myrtus communis, Cistus ladanifer, and Montpellier cistus [38]. In contrast, in the EO of maca (Lepidium meyenii), β-ionone was found to be a minor component [39] (Figure 2). Plants 2021, 10, 754 3 of 12 ionone,