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Prunus Armeniaca) International Journal of Molecular Sciences Article Insights of Phenolic Pathway in Fruits: Transcriptional and Metabolic Profiling in Apricot (Prunus armeniaca) Helena Gómez-Martínez , Francisco Gil-Muñoz , Almudena Bermejo, Elena Zuriaga and Maria L. Badenes * Instituto Valenciano de Investigaciones Agrarias (IVIA), CV 315, Km 10,5, 46113 Moncada, Valencia, Spain; [email protected] (H.G.-M.); [email protected] (F.G.-M.); [email protected] (A.B.); [email protected] (E.Z.) * Correspondence: [email protected] Abstract: There is an increasing interest in polyphenols, plant secondary metabolites, in terms of fruit quality and diet, mainly due to their antioxidant effect. However, the identification of key gene enzymes and their roles in the phenylpropanoid pathway in temperate fruits species remains uncertain. Apricot (Prunus armeniaca) is a Mediterranean fruit with high diversity and fruit quality properties, being an excellent source of polyphenol compounds. For a better understanding of the phenolic pathway in these fruits, we selected a set of accessions with genetic-based differences in phenolic compounds accumulation. HPLC analysis of the main phenolic compounds and tran- scriptional analysis of the genes involved in key steps of the polyphenol network were carried out. Phenylalanine ammonia-lyase (PAL), dihydroflavonol-4-reductase (DFR) and flavonol synthase (FLS) were the key enzymes selected. Orthologous of the genes involved in transcription of these enzymes were identified in apricot: ParPAL1, ParPAL2, ParDFR, ParFLS1 and ParFLS2. Transcriptional data of Citation: Gómez-Martínez, H.; the genes involved in those critical points and their relationships with the polyphenol compounds Gil-Muñoz, F.; Bermejo, A.; Zuriaga, were analyzed. Higher expression of ParDFR and ParPAL2 has been associated with red-blushed E.; Badenes, M.L. Insights of Phenolic accessions. Differences in expression between paralogues could be related to the presence of a Pathway in Fruits: Transcriptional BOXCOREDCPAL cis-acting element related to the genes involved in anthocyanin synthesis ParFLS2, and Metabolic Profiling in Apricot ParDFR and ParPAL2. (Prunus armeniaca). Int. J. Mol. Sci. 2021, 22, 3411. https://doi.org/ Keywords: phenolic pathway; FLS; DFR; PAL; fruits 10.3390/ijms22073411 Academic Editor: Ana Jiménez Received: 5 March 2021 1. Introduction Accepted: 24 March 2021 Apricot (Prunus armeniaca) is an important fruit crop in Mediterranean basin countries Published: 26 March 2021 and Asia, with a wide diversity in pomological characteristics and fruit quality properties due to its different diversification centers [1]. Apricots are a good source of vitamins, Publisher’s Note: MDPI stays neutral carotenoids, and polyphenols [2], which makes this species a good choice from a nutraceu- with regard to jurisdictional claims in tical point of view [3]. published maps and institutional affil- Higher plants have several defense mechanisms against biotic and abiotic stresses. iations. Some of these mechanisms result in the synthesis of a large number of secondary metabo- lites. Flavonoids are one of these defense-related secondary metabolites, being a family of polyphenols synthesized by the phenylpropanoid biosynthetic pathway [4]. These sec- ondary metabolites remain in different plant organs and accumulate on the plant surface [5]. Copyright: © 2021 by the authors. In the case of flavonoid compounds, their accumulation is unequally distributed within Licensee MDPI, Basel, Switzerland. tissues, as its concentration is higher in the peel of several fruits such as apple [6], peach [7], This article is an open access article or apricot [8]. distributed under the terms and Polyphenols have been identified as secondary metabolites with great antioxidant conditions of the Creative Commons activity [9–11]. In recent years, there is an increasing interest in them as contributors to fruit Attribution (CC BY) license (https:// quality and dietary properties. In the case of apricot, the fruit peel is an excellent source creativecommons.org/licenses/by/ of phenolic compounds. The main phenylpropanoid-derivate secondary metabolites in 4.0/). Int. J. Mol. Sci. 2021, 22, 3411. https://doi.org/10.3390/ijms22073411 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 18 Int. J. Mol. Sci. 2021, 22, 3411 2 of 17 source of phenolic compounds. The main phenylpropanoid-derivate secondary metabo- litesapricot in apricot are chlorogenic are chlorogenic and neochlorogenic and neochlorogenic acids, two acids, caffeate two caffeate derivates derivates monolignols, monolig- while nols,the mainwhile flavonolsthe main areflavonols rutin and are quercetin-3-glucuroniderutin and quercetin-3-glucuronide [12]. [12]. PhenylpropanoidPhenylpropanoid biosynthesis biosynthesis starts starts from from the the conversion conversion of of L L-phenylalanine-phenylalanine into into cinnamiccinnamic acid acid due due to to the the action action of of phenylalanine phenylalanine ammonia ammonia-lyase-lyase (PAL) (PAL) (Figure (Figure 1)1).. FigureFigure 1. 1.PhenolicPhenolic biosynthesis biosynthesis pathway pathway.. Red Red arrows arrows represent represent the the key key genes genes studied: studied: PAL PAL (phe- (pheny- nylalaninelalanine ammonia-lyase), ammonia-lyase), FLS FLS (flavonol (flavonol synthase), synthase), and and DFRDFR (dihydroflavonol-4-reductase).(dihydroflavonol-4-reductase). YellowYel- lowsquares squares represent represent the the main main metabolites metabolites contributing contributing to apricotto apricot antioxidant antioxidant capacity. capacity. PhenylalaninePhenylalanine ammonia ammonia-lyase-lyase (PAL) (PAL) has has been been described described as as the the first first enzyme enzyme in in the the phenylpropanoidphenylpropanoid pathway, pathway, considered considered a akey key regulatory regulatory point point between between primary primary and and sec- sec- ondaryondary metabolism metabolism through through conversion conversion of of L L-phenylalanine-phenylalanine into cinnamiccinnamic acidacid [[13].13]. PALPAL is isencoded encoded by by a a multi-gene multi-gene family, family, in in which which the the number number of of genes genes involved involved depends depends on on the thespecies. species. In ArabidopsisIn Arabidopsisand andNicotiana Nicotiana, four, four PAL-encoding PAL-encoding genes genes have beenhave describedbeen described [14–16 ], [14five–16], in poplarfive in poplar [17], and [17], two and in differenttwo in differentPrunus speciesPrunus [species18]. In the[18]. following In the following step, cinnamic step, cinnamicacid 4-hydroxylase acid 4-hydroxylase converts converts cinnamic cinnamic acid into 4-coumaricacid into 4-coumaric acid, to which acid, a to coenzyme-A which a co- is enzymeadded- dueA is toadded the actiondue to ofthe 4-coumarate-CoA action of 4-coumarate ligase,-CoA giving ligase, 4-coumaroyl-CoA giving 4-coumaroyl as a- result.CoA asAt a result. this point, At this the point, pathway the canpathway branch can off branch to the caffeateoff to the derivates caffeate derivates biosynthesis, biosynthesis, producing producingchlorogenic chlorogenic and neochlorogenic and neochlorogenic acids. Alternatively, acids. Alternatively, 4-coumaroyl-CoA 4-coumaroyl is- alsoCoA usedis also by usedchalcone by chalcone synthase synthase to catalyze to catalyze the synthesis the synthesis of chalcone, of chalcone, which is which isomerized is isomerized to colorless to colorlessflavanones. flavanones. These compounds These compounds can be hydroxylatedcan be hydroxylat at threeed at different three different positions, positions, by three bydifferent three different flavonoid flavonoid hydroxylases, hydroxylases, producing producing a group a ofgroup dihydroflavonols. of dihydroflavonols. Then, the Then, phe- thenolic phenolic pathway pathway can branch can branch off to theoff flavonolsto the flavonols biosynthesis biosynthesis due to thedue actionto the ofaction flavonol of flavonolsynthase synthase (FLS). This (FLS). enzyme This uses enzyme dihydroflavonols uses dihydr (dihydroquercetin,oflavonols (dihydroquercetin, dihydrokaempferol, dihy- drokaempferolor dihydromyricetin), or dihydromyricetin) as a substrate as to producea substrate kaempferol, to produce quercetin, kaempferol, or myricetin,quercetin, or the myricetinmain precursors, the main of precursors some flavonols of some such flavonols as rutin such or as quercetin-3-glucuronide. rutin or quercetin-3-glucuronide. Previous Previousworks have works identified have identified FLS-encoding FLS-encoding genes in genes Arabidopsis in Arabidopsis [19,20]. [19,20]. In addition, In addition, FLS has FLSbeen has related been related with dihydroflavonols with dihydroflavonols catalysis catalysis to flavonol to flavonol but also but it also has it been has relatedbeen re- to anthocyanin accumulation [20,21]. On the other hand, dihydroflavonol-4-reductase (DFR) lated to anthocyanin accumulation [20,21]. On the other hand, dihydroflavonol-4-reduc- enzyme controls one of the limiting steps of the anthocyanin pathway, reducing dihy- tase (DFR) enzyme controls one of the limiting steps of the anthocyanin pathway, reduc- droflavonols to leucoanthocyanidins [22–24], therefore using the same substrate as FLS. ing dihydroflavonols to leucoanthocyanidins [22–24], therefore using the same substrate Several DFR-encoding genes have been identified in different species [23,25–27]. Although as FLS. Several DFR-encoding genes have been identified in different species
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