Planta (2017) 246:803–816 DOI 10.1007/s00425-017-2749-x REVIEW Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering Farhat Abbas1 · Yanguo Ke1 · Rangcai Yu2 · Yuechong Yue1 · Sikandar Amanullah3 · Muhammad Muzammil Jahangir4 · Yanping Fan1,5 Received: 20 April 2017 / Accepted: 22 July 2017 / Published online: 12 August 2017 © Springer-Verlag GmbH Germany 2017 Abstract also signifcant because of their enormous applications in Main conclusion Terpenoids play several physiological the pharmaceutical, food and cosmetics industries. Due to and ecological functions in plant life through direct and their broad distribution and functional versatility, eforts indirect plant defenses and also in human society because are being made to decode the biosynthetic pathways and of their enormous applications in the pharmaceutical, comprehend the regulatory mechanisms of terpenoids. This food and cosmetics industries. Through the aid of genetic review summarizes the recent advances in biosynthetic engineering its role can by magnifed to broad spectrum pathways, including the spatiotemporal, transcriptional and by improving genetic ability of crop plants, enhancing post-transcriptional regulatory mechanisms. Moreover, we the aroma quality of fruits and fowers and the produc‑ discuss the multiple functions of the terpene synthase genes tion of pharmaceutical terpenoids contents in medicinal (TPS), their interaction with the surrounding environment plants. and the use of genetic engineering for terpenoid production in model plants. Here, we also provide an overview of the Terpenoids are structurally diverse and the most abundant signifcance of terpenoid metabolic engineering in crop pro- plant secondary metabolites, playing an important role in tection, plant reproduction and plant metabolic engineering plant life through direct and indirect plant defenses, by approaches for pharmaceutical terpenoids production and attracting pollinators and through different interactions future scenarios in agriculture, which call for sustainable between the plants and their environment. Terpenoids are production platforms by improving diferent plant traits. Volatile terpenoids · Multifunction · * Rangcai Yu Keywords [email protected] Biosynthesis · Plant defense · Pollinator attractions · Regulation · Genetic engineering * Yanping Fan [email protected] 1 The Research Center for Ornamental Plants, College Introduction of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642, China 2 Terpenoids are structurally diverse and the most abundant College of Life Sciences, South China Agricultural group of foral volatiles, encompassing more than 40,000 University, Guangzhou 510642, China 3 individual compounds (Buckingham 2004; Muhlemann et al. College of Horticulture and Landscape Architecture, 2014). A majority of these compounds are of plant origin Northeast Agricultural University, Harbin, Heilongjiang, China and have several biological functions in higher plants. Ter- penoids are found in most plant species and are essential for 4 Institute of Horticultural Sciences, University of Agriculture, Faisalabad, Pakistan plant growth and development. They are the key components of membrane structures (sterols ­C ), function as photosyn- 5 Guangdong Key Laboratory for Innovative Development 30 and Utilization of Forest Plant Germplasm, South China thetic pigments (carotenoids ­C40); abscisic acid ­(C15) and Agricultural University, Guangzhou 510642, China gibberellins ­(C20) are phytohormones, and ubiquinones are Vol.:(0123456789)1 3 804 Planta (2017) 246:803–816 involved in mitochondrial electron transport. Many terpe- compound zerumbone from shampoo ginger is a subject of noids (including mono-, sesqui- and diterpenes) are known interest in pharmacological studies (Bertea et al. 2005; Yu to be plant secondary metabolites which play fundamental and Utsumi 2009). roles in plant–environment and plant-plant interactions (Yu Terpenoids are synthesized from two independent but and Utsumi 2009; Dudareva et al. 2013). compartmentally separated pathways: the mevalonic acid Volatile terpenoids (isoprenes, monoterpenes and sesquit- (MVA) and methylerythritol phosphate (MEP) pathways. erpenes) constitute the largest class of plant volatile com- The MEP pathway is mainly responsible for the biosynthesis pounds. They exhibit several carbon skeletons and extremely of mono- and diterpenes, producing approximately 53 and variable in chemical structure yet share a common feature 1% of the total foral terpenoids, respectively. Sesquiterpe- of biosynthesis, which occurs in almost all plant organs, nes are synthesized from the MVA pathway, contributing including the roots, stems, leaves, fruits and seeds, but their approximately 28% of the total foral terpenoids (Muhle- highest amounts are released predominantly from fowers mann et al. 2014), as shown in Fig. 1. (Dudareva et al. 2013). Floral volatiles are lipophilic liquids The commercial and ecological importance of terpenoids in nature, having high vapor pressure and low molecular has inspired rapid progress in foral scent engineering for weight at ambient temperatures. These properties allow them terpenoid production in model plants. The identifcation of to freely pass through the cellular membranes for release TPS genes, decoding the biosynthetic pathways and enzymes into the adjacent environment (Pichersky et al. 2006). involved in these pathways, has made the manipulation of Among all terpenoids, mono- and sesquiterpenes are the genetic engineering in plants extremely feasible (Dudareva most commonly studied classes because of their extensive and Pichersky 2008; Yu and Utsumi 2009). Genetic engi- distribution in the plant kingdom and their essential roles neering can improve numerous input and output charac- in both human society and plants. Therefore, we will focus teristics in crops, including weed control through allelopa- more on these two terpene classes in this review article. thy, pest resistance, increases in the aroma production of Terpenoids are synthesized from two inter-convertible C5 fruits and vegetables (by altering the foral scent) and the units: isopentenyl diphosphate (IPP) and its allelic isomer production of medicinal compounds (Aharoni et al. 2005; dimethylallyl diphosphate (DMAPP). These fve-carbon Dudareva et al. 2013). Furthermore, model plants (Arabi- units serve as substrates/precursors for the biosynthesis of dopsis, Tobacco) with altered terpenoid profles can provide terpenoids. Based on their biosynthetic origin, foral volatile useful information for exploring biosynthesis, regulatory organic compounds can be divided into three major classes: compounds and their ecological importance in plant–envi- terpenoids, benzenoids/phenylpropanoids and derivatives ronment interactions. of fatty acids, wherein terpenes constitute 55% of the plant In this review, we emphasize the recent advances in secondary metabolites, alkaloids 27% and phenolics 18% understanding the molecular mechanism of the biosynthetic (Muhlemann et al. 2014). pathways and its regulation, function and manipulation of Terpenes play diverse roles in benefcial interactions genetic engineering of terpenoid production in model plants. and in mediating antagonists among organisms (Das et al. Here, we will focus on mono- and sesquiterpenoids. 2013). They protect many plant species against pathogens, predators and competitors (Hijaz et al. 2016). Furthermore, herbivore-induced monoterpenoids act as airborne signals to nearby plants in response to insect attack such as (E)- β-ocimene (Arimura et al. 2004). Although terpenes are mostly studied in the above-ground tissues, recently, their novel function in the below-ground environment, as sign- aling molecules, has been identifed (Karban et al. 2014; Delory et al. 2016). For example, β-caryophyllene, released from the roots of maize plants against beetle (Diabrotica virgifera) attack, acts as a volatile signal to attract predatory nematodes, which will defend plants indirectly from further damage (Rasmann et al. 2005). Similarly, the Hedychium coronarium farnesyl pyrophosphate synthase gene shows a quick response to herbivory and wounding and is involved Fig. 1 Pie chart showing the approximate constituents of the total in foral biosynthesis (Lan et al. 2013). Terpenoids are also foral terpenoids—mono-, sesqui-, di- and other terpenes (like isopre- benefcial for human beings. For example, limonene is exten- noids hemi, tri-, and tetraterpenes). Monoterpenes dominate over half of the pie chart, being operative in plastids and showing wide diver- sively used as a scent compound in cosmetic products (Brokl sity, while sesquiterpenes compose 1/3 of the pie chart and are dis- et al. 2013). The potential anticancer and anti-infammatory tributed in the cytosol, endoplasmic reticulum and peroxisomes 1 3 Planta (2017) 246:803–816 805 Multifunctionality of volatile terpenoids electromagnetic, visual) are necessary for locating breed- ing sites and food. Many studies showed the role of plant Terpenoid metabolites are involved in various physiological terpenoids in communication between plants and pollinators and ecological functions based on the diferential expres- (Baldwin et al. 2006). Terpenoids are a major cue for attract- sion profles of terpene synthase genes found in response ing pollinators (animals, insects, mammals, birds and bats), to biotic and abiotic environmental factors throughout plant serving as vectors