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(+)-Valencene in 'Newhall' Orange

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(+)-Valencene in 'Newhall' Orange Journal of Experimental Botany, Vol. 67, No. 14 pp. 4105–4115, 2016 doi:10.1093/jxb/erw189 Advance Access publication 18 May 2016 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) RESEARCH PAPER CitAP2.10 activation of the terpene synthase CsTPS1 is associated with the synthesis of (+)-valencene in ‘Newhall’ orange Shu-ling Shen1,2,3,†, Xue-ren Yin1,2,3,†, Bo Zhang1,2,3, Xiu-lan Xie1, Qian Jiang1, Donald Grierson1,4 and Kun-song Chen1,2,3,* 1 College of Agriculture & Biotechnology, Zhejiang University, Zijingang Campus, Hangzhou 310058, PR China 2 Zhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Zijingang Campus, Hangzhou 310058, PR China 3 The State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Zijingang Campus, Hangzhou 310058, PR China 4 School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, LE12 5RD, UK * Correspondence: [email protected] † These authors contributed equally to this manuscript. Received 2 December 2015; Accepted 19 April 2016 Editor: Qiao Zhao, Tsinghua University Abstract Aroma is a vital characteristic that determines the quality and commercial value of citrus fruits, and characteristic volatiles have been analyzed in different citrus species. In sweet orange, Citrus sinensis, the sesquiterpene (+)-valencene is a key volatile compound in the fruit peel. Valencene synthesis is catalyzed by the terpene synthase CsTPS1, but the transcrip- tional mechanisms controlling its gene expression are unknown. Here, the AP2/ERF (APETALA2/ethylene response fac- tor) transcription factor, CitAP2.10, is characterized as a regulator of (+)-valencene synthesis. The expression pattern of CitAP2.10 was positively correlated with (+)-valencene content and CsTPS1 expression. Dual-luciferase assays indicated that CitAP2.10 could trans-activate the CsTPS1 promoter. Ethylene enhanced expression of CitAP2.10 and this effect was abolished by the ethylene antagonist 1-methylcyclopropene. The role and function of CitAP2.10 in (+)-valencene biosyn- thesis were confirmed using the Arabidopsis homolog (AtWRI1), which also transiently activated the CsTPS1 promoter. Furthermore, transient over-expression of CitAP2.10 triggered (+)-valencene biosynthesis in sweet orange fruit. These results indicate that CitAP2.10 regulates (+)-valencene synthesis via induction of CsTPS1 mRNA accumulation. Key words: CitAP2/ERF, Citrus sinensis, citrus volatile, ethylene, sweet orange, terpene synthase, TPS, transcriptional regulation, valencene. Introduction Over 1000 individual volatile organic compounds have been adaptation (Kessler and Baldwin, 2001). For fruit, aroma is identified from plants (Qualley and Dudareva, 2009). These one of the most significant quality traits, potentially influenc- volatiles affect plant growth, development, and environmental ing consumer acceptance. Most fruit, such as mango (Singh © The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 4106 | Shen et al. and Saini, 2014), strawberry (Van de Poel et al., 2014), pear of ethylene production by antisense ACC (aminocyclopro- (Moya-Leon et al., 2006), melon (Gonda et al., 2013), and panecarboxylate) oxidase RNA in melon prevents volatile citrus (Shi et al., 2007) produce large amounts of volatiles. production (Pech et al., 2008, 2012). Ethylene response fac- Fruits are particularly useful for aroma research, as specific tors (ERFs) have recently been identified as targets for fruit compounds are unique to the fruit and are not found in ripening and quality research, and SlERFs have been demon- other plant tissues, e.g., esters can be detected in mango fruit strated to be ripening-related transcription factors (Liu et al., but are absent from leaves (da Silva et al., 2012; Lalel et al., 2016); MaERFs have been shown to be involved in banana 2003), and linalool and C10 lactones appear in ripe peach but fruit ripening (Xiao et al., 2013); PsERFs determine the rate are absent from leaves (Horvat and Chapman, 1990). Citrus of ripening in Japanese plum (El-Sharkawy et al., 2009); fruit are also excellent materials for terpenoid research. The apple MdCBF and kiwifruit AdERF9 participate in fruit sof- volatile terpenoids, a large and structurally diverse group of tening (Tacken et al., 2010; Yin et al., 2010); and persimmon secondary metabolites, are represented by isoprenes (C5), DkERF9/10/19/22 contributes to fruit deastringency (Min monoterpenes (C10), and sesquiterpenes (C15). Volatile ter- et al., 2012, 2014). Although an increase in fruit aroma pro- penoids are all derived from two C5-isoprene building units, duction is usually associated with fruit ripening, the poten- isopentenyl diphosphate (IPP) and dimethylallyl diphos- tial role of AP2/ERF (APETALA2/ethylene response factor) phate (DMAPP), which are synthesized from the mevalonate transcription factors in fruit aroma has not previously been (MVA) and non-mevalonate (MEP) pathways (Mcgarvey and explored. Croteau, 1995). Most of the terpenes are synthesized from Using a citrus genome database, 126 CitAP2/ERF genes their corresponding substrates by terpene synthases (TPS). were isolated and most of them were found to be differen- In citrus species, several TPS genes have been characterized, tially expressed during citrus fruit development, which indi- including CitMTSE1 (AB110636.1) from satsuma mandarin cates their potential involvement in the ripening of citrus fruit (Citrus unshiu Marcow, Shimada et al., 2004), RlemTPS1- (Xie et al., 2014). In the present study, the transcriptional reg- 3(AB691531.1, AB266584.1, AB266585.1) from citrus jamb- ulatory roles of CitAP2.10, a CitAP2/ERF family member, hiri (Yamasaki and Akimitsu, 2007; Shishido et al., 2012), and in regulating (+)-valencene production in citrus sweet orange (+)-valencene biosynthesis-related CsTPS1 (AF514289.1) ‘Newhall’ fruit were investigated during different stages of from sweet orange (Citrus sinensis, Sharon-Asa et al., 2003). fruit development, and in response to treatment with ethylene The mechanisms and identities of transcription factors and its action inhibitor 1-methylcyclopropene. A potential regulating terpenoid biosynthesis have been characterized in role for CitAP2.10 in regulating citrus (+)-valencene produc- model plants, where members of the ARF (auxin response tion was examined by transient overexpression in citrus peels factors), MYC (myelocytomatosis related proteins), MYB and the action on the promoter of the target gene CsTPS1 (myeloblastosis related proteins), and WRKY (amino-acid was studied using a tobacco dual-luciferase assay. sequence WRKYGQK) families have been implicated. It has been reported that the Arabidopsis auxin responsive factors AtARF6 and AtARF8, as well as AtMYB21 and AtMYB24, Materials and methods can induce the production of sesquiterpenes (Mandaokar et al., 2006; Reeves et al., 2012), and AtMYC2 can regulate Plant materials and treatments synthesis of sesquiterpenes by binding to the promoter of Fruit of eleven citrus cultivars from six species were collected at the AtTPS11 and AtTPS21 (Hong et al., 2012). PtMYB14 is commercial ripened stages (Table 1; related physiological data are indicated in Supplementary Table S1 at JXB online). involved in regulating the MVA pathway, as well as jasmonate Fruits of the sweet orange (Citrus sinensis) cultivar ‘Newhall’ metabolism, resulting in the release of volatile terpenoids in were obtained from a commercial orchard in Songyang (Zhejiang, coniferous trees (Bedon et al., 2010). Similarly, NaWRKY3 China) at seven different developmental stages, namely at 120, 135, and NaWRKY6 participate in defense against herbivores in 150, 165, 180, 195 and 210 d after full bloom (DAFB) in 2011. In Nicotiana attenuata by producing terpenoids to attract pred- order to study the effect of ethylene on the biosynthesis of citrus sesquiterpenes, ‘Newhall’ sweet orange fruit were collected at 150 ators and reduce the number of herbivorous larvae (Skibbe DAFB from the same orchard in 2012, treated separately with 40 μl et al., 2008). Despite the increasing number of investigations l−1 ethylene or 1 μl l−1 1-methylcyclopropene (1-MCP) and stored at of the transcription factors regulating aroma in the plant 20 °C for 5 d after harvest. For treatments, the harvested fruit were kingdom, there have been few previous reports on the tran- randomly divided into three groups for each treatment, as three bio- scriptional regulation of fruit volatiles. logical replicates. Peel samples taken from the equatorial portion of fruits were cut into small pieces, immediately frozen in liquid nitro- The formation of plant volatiles is regulated by both gen and stored at –80 °C for subsequent study. internal (developmental, tissue-specific) and external (envi- ronmental) factors. For instance, some volatile terpenoids can be induced or inhibited by environmental stresses such Volatile compounds analysis as wounding, insect and herbivore attack, and by hormones The frozen tissues were ground in liquid nitrogen and 1 g was weighed such as gibberellins and jasmonates
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