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Formation of -Farnesene in Tea (Camellia Sinensis) Leaves Induced

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Formation of -Farnesene in Tea (Camellia Sinensis) Leaves Induced International Journal of Molecular Sciences Article Formation of α-Farnesene in Tea (Camellia sinensis) Leaves Induced by Herbivore-Derived Wounding and Its Effect on Neighboring Tea Plants 1,2, 1,3, 1,2 4 4 Xuewen Wang y, Lanting Zeng y, Yinyin Liao , Jianlong Li , Jinchi Tang and Ziyin Yang 1,2,3,* 1 Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement & Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Xingke Road 723, Tianhe District, Guangzhou 510650, China 2 University of Chinese Academy of Sciences, Yuquan Road 19A, Beijing 100049, China 3 Center of Economic Botany, Core Botanical Gardens, Chinese Academy of Sciences, Xingke Road 723, Tianhe District, Guangzhou 510650, China 4 Tea Research Institute, Guangdong Academy of Agricultural Sciences & Guangdong Provincial Key Laboratory of Tea Plant Resources Innovation and Utilization, Dafeng Road 6, Tianhe District, Guangzhou 510640, China * Correspondence: [email protected]; Tel.: +86-20-3807-2989 These authors contributed equally to this work. y Received: 17 July 2019; Accepted: 22 August 2019; Published: 25 August 2019 Abstract: Herbivore-induced plant volatiles (HIPVs) play important ecological roles in defense against stresses. In contrast to model plants, reports on HIPV formation and function in crops are limited. Tea (Camellia sinensis) is an important crop in China. α-Farnesene is a common HIPV produced in tea plants in response to different herbivore attacks. In this study, a C. sinensis α-farnesene synthase (CsAFS) was isolated, cloned, sequenced, and functionally characterized. The CsAFS recombinant protein produced in Escherichia coli was able to transform farnesyl diphosphate (FPP) into α-farnesene and also convert geranyl diphosphate (GPP) to β-ocimene in vitro. Furthermore, transient expression analysis in Nicotiana benthamiana plants indicated that CsAFS was located in the cytoplasm and could convert FPP to α-farnesene in plants. Wounding, to simulate herbivore damage, activated jasmonic acid (JA) formation, which significantly enhanced the CsAFS expression level and α-farnesene content. This suggested that herbivore-derived wounding induced α-farnesene formation in tea leaves. Furthermore, the emitted α-farnesene might act as a signal to activate antibacterial-related factors in neighboring undamaged tea leaves. This research advances our understanding of the formation and signaling roles of common HIPVs in crops such as tea plants. Keywords: aroma; Camellis sinensis; α-farnesene synthetase; herbivore; jasmonic acid; signaling; tea; volatile 1. Introduction Tea (Camellia sinensis) plants are important woody economic crops with shoots and leaves that can be used to make the popular beverage [1]. Tea is usually grown in temperate and subtropical regions, such that insect attack is a normal annual phenomenon. In response to herbivore invasion, plants can release chemical compounds, known as herbivore-induced plant volatiles (HIPVs) [2,3]. HIPVs from economic crops, including tea plants, have been researched. Studies have indicated that (Z)-3-hexenol, nerolidol, (E)-β-ocimene, (E)-β-caryophyllene, (E,E)-α-farnesene and other terpenoids can be released when herbivores attack tea trees [4,5]. Furthermore, α-farnesene is a common volatile released by Int. J. Mol. Sci. 2019, 20, 4151; doi:10.3390/ijms20174151 www.mdpi.com/journal/ijms Int.Int. J. Mol.J. Mol. Sci. Sci.2019 2019, 20, 18, 4151, x FOR PEER ARTICLE 2 of 215 of 15 volatile released by tea plants when suffering attack [6]. α-Farnesene has been reported to have an teaimportant plants when effect su onffering insect attack resistance, [6]. α -Farnesenesuch as defense has been against reported of Lobesia to have botrana an importantthrough locating effect on insectspawning resistance, herbivores such as [7]. defense Compared against with of Lobesiaother economic botrana through plants, locatingα-farnesene spawning in tea herbivoresplants has [7]. Comparedreceived little with study. other economic plants, α-farnesene in tea plants has received little study. TheThe response response to to stress stress conditions, conditions, includingincluding insect resistance, resistance, of of αα-farnesene-farnesene has has been been reported reported inin several several studies studies [ 8[8–10–10].]. ForFor instance,instance, the functions of of αα--farnesene,farnesene, linalool, linalool, and and other other inducible inducible compounds are the same as (Z)-3-hexenol, which can be used by parasitoids to forage and locate compounds are the same as (Z)-3-hexenol, which can be used by parasitoids to forage and locate hosts [11]. This indicates that many types of volatile can be considered as plant-to-plant and hosts [11]. This indicates that many types of volatile can be considered as plant-to-plant and plant-to-herbivore communication signals [10,12]. A recent study reported that (E,E)-α-farnesene plant-to-herbivore communication signals [10,12]. A recent study reported that (E,E)-α-farnesene emitted by insect-induced soybean plays a defense role against nematodes [13]. Therefore, emitted by insect-induced soybean plays a defense role against nematodes [13]. Therefore, investigating investigating the α-farnesene biosynthesis is of significance. α-Farnesene is classified as a α α thesesquiterpene-farnesene biosynthesiswith coding genes is of significance. that are part of-Farnesene or closely related is classified to the as plant a sesquiterpene terpene synthase with gene coding genes(TPS that) family are part[14,15]. ofor The closely formation related of tomonoterpene the plant terpene and sesquiterpene synthase gene have (TPS) been family investigat [14,15ed]. in The formationmany plant of monoterpene species, including and sesquiterpene apple (Malus havedomestica been) investigated[16], Arabidopsis in many [17,18] plant, soybean species, [13] including, and appletomato (Malus [19]. domestica(E,E)-α-Farnesene)[16], Arabidopsis synthase has[17 ,been18], soybeanfound in [apple13], and fruit tomato and expressed [19]. (E ,fromE)-α -Farnesenethe peel synthasetissues [16]. has beenHowever, found the in biosynthesis apple fruit of and α-farnesene expressed in from tea leaves the peel has tissuesremained [16 unknown.]. However, This the biosynthesisstudy aimed of toα-farnesene investigate in the tea formation leaves has of remained α-farnesene unknown. in tea leaves This studyexposed aimed to herbivore to investigate attack the formationand its potential of α-farnesene signaling in function tea leaves. exposed to herbivore attack and its potential signaling function. 2.2. Results Results 2.1.2.1. E ffEectffect of of Herbivore Herbivore Attack Attack on onα α-Farnesene-Farnesene Formation TeaTea greengreen leafhopper leafhopper (Empoasca (Empoasca (Matsumurasca(Matsumurasca) onukii) onukiiMatsuda)Matsuda) and tea geometrid and tea ( geometridEctropis (Ectropisgrisescens grisescens Warren)Warren) are the are two the main two maintea plant tea plant herbivores herbivores and andare areclassified classified as ashaving having piercing-suckingpiercing-sucking mouthparts mouthparts andand mandibulatemandibulate mouthparts, respectively. respectively. When When these these two two different different speciesspecies of herbivoresof herbivores separately separately attacked attacked tea leavestea leaves of C. of sinensis C. sinensiscv. Jinxuan, cv. Jinxuan,α-farnesene α-farnesene was detected was indetected all groups in over all gr time.oups Furthermore,over time. Furthermore,α-farnesene α was-farnesene produced was in produced both insect in both treatments insect (Figuretreatment1A,B).s This(Fig showedure 1A,that B). teaThis plants showed could that release tea plants HIPVs, could including releaseα HIPVs,-farnesene, including when α attacked-farnesene, by diwhenfferent herbivoreattacked mouthparts.by different herbivore Although mouthparts. secretion from Although herbivore secretion mouthparts from herbivore could influencemouthparts the could HIPVs releasedinfluence to somethe HIPVs extent, released we concluded to some thatextent, wounding we concluded was the that common wounding factor was during the common attack, andfactor that α-farneseneduring attack, produced and bythat wounding α-farnesene might produced have an insect-resistanceby wounding might function. have To an verify insect this-resistance hypothesis, wefunction. mechanically To verify damaged this hypothesis tea leaves, we tosimulate mechanically herbivore damaged attack tea and leaves discovered to simulate the formationherbivore of attack and discovered the formation of α-farnesene with a significantly increased content compared α-farnesene with a significantly increased content compared with the control (Figure1C). This result with the control (Figure 1C). This result indicated that wounding stress that imitated herbivore indicated that wounding stress that imitated herbivore attack could induce α-farnesene formation. attack could induce α-farnesene formation. Figure 1. The formation of α-farnesene induced by two main herbivores and wounding stress in Figure 1. The formation of α-farnesene induced by two main herbivores and wounding stress in C. C. sinensis cv. Jinxuan. (A) Under tea green leafhopper attack; (B) Under tea geometrid attack. CK, sinensis cv. Jinxuan. (A) Under tea green leafhopper attack; (B) Under tea geometrid attack. CK, withoutwithout herbivores herbivores attack attack collectedcollected in in differ differentent treatment treatment time time.
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