On the Natural Diversity of Phenylacylated-Flavonoid and Their
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Phytochem Rev DOI 10.1007/s11101-017-9531-3 On the natural diversity of phenylacylated-flavonoid and their in planta function under conditions of stress Takayuki Tohge . Leonardo Perez de Souza . Alisdair R. Fernie Received: 23 November 2016 / Accepted: 26 August 2017 © The Author(s) 2017. This article is an open access publication Abstract Plants contain light signaling systems and Keywords Flavonoid · Natural diversity · undergo metabolic perturbation and reprogramming Phenelyacylation · Species conservation · under light stress in order to adapt to environmental UV-B changes. Flavonoids are one of the largest classes of natural phytochemical compounds having several Abbreviations biological functions conferring stress defense to ANS Anthocyanidin synthase plants and health benefits in animal diets. A recent BAHD BEAT/AHCT/HCBT/DAT study of phenylacylated-flavonoids (also called BGLU Beta glucosidase hydroxycinnamoylated-flavonoids) of natural acces- CHI Chalcone isomerase sions of Arabidopsis suggested that phenylacylation CHS Naringenin-chalcone synthase of flavonoids relates to selection under different COP1 CONSTITUTIVE natural light conditions. Phenylacylated-flavonoids PHOTOMORPHOGENIC 1 which are decorated with hydroxycinnamoyl units, CPD Cyclobutane pyrimidine dimers namely cinnamoyl, 4-coumaroyl, caffeoyl, feruloyl CRY CRYPTOCHROME and sinapoyl moieties, are widely distributed in the CUL4 CULLIN 4 plant kingdom. Currently, more than 400 phenylacy- DDB UV-damaged DNA binding protein lated flavonoids have been reported. Phenylacylation DFR Dihydroflavonol 4-reductase renders enhanced phytochemical functions such as EBG Early biosynthetic genes ultraviolet-absorbance and antioxidant activity, F3′5′H Flavonoid 3′,5′-hydroxylase although, the physiological role of phenylacylation F3H Flavanone 3-hydroxylase of flavonoids in plants is largely unknown. In this FLS Flavonol synthase review, we provide an overview of the occurrence FPT Flavonol phenylacyltransferase and natural diversity of phenylacylated-flavonoids as HY5 ELONGATED HYPOCOTYL 5 well as postulating their biological functions both in HYH HY5-HOMOLOG planta and with respect to biological activity follow- IFR Isoflavone reductase ing their consumption. IFS Isoflavone synthase LBG Late biosynthetic genes LDL Low-density lipoprotein & T. Tohge · L. Perez de Souza · A. R. Fernie ( ) NIL Near isogenic lines Max-Planck Institute of Molecular Plant Physiology, Am Mu¨hlenberg 1, 14476 Potsdam-Golm, Germany NMR Nuclear magnetic resonance e-mail: [email protected] PAL Phenylalanine ammonia lyase 123 Phytochem Rev PHY PHYTOCHROME A biosynthetic genes are missing in several plant species QTL Quantitative trait locus such as algae and moss (Tohge et al. 2013a, b). Since RUP REPRESSOR OF UV-B orthologous genes of the early steps in flavonoid PHOTOMORPHOGENESIS pathway are found even in liverworts and mosses SCPL Serine carboxypeptidase-like (Winkel-Shirley 2001), the evolution of flavonoid UGT1 UDP-sugar-dependent glycosyltransferase 1 biosynthesis appears to be as yet incompletely under- UV Ultra-violet stood. However, the appearance of subclasses of UVR8 UV REPAIR DEFECTIVE 8 flavonoids (Fig. 1), suggests that branches in the pathway have evolved in specific plant lineages over the course of evolution. The core flavonoid biosyn- thetic pathway is well documented. The main chemical backbone of flavonoids (flavonoid aglycones, Fig. 1)is Introduction synthesized from phenylalanine via a set of core biosynthetic genes including CHS, chalcone isomerase Flavonoids are by far the major sub-class of phenyl- (CHI), flavanone 3-hydroxylase (F3H), dihy- propanoids, which are themselves the third largest droflavonol 4-reductase (DFR), anthocyanidin class of plant secondary metabolites (specialized synthase (ANS) that are relatively well-conserved metabolites). Flavonoids comprise in excess of 8000 among land plants. Specific steps make specialized metabolites bearing a common diphenylpropane (C6– flavonoids such as isoflavone synthase (IFS) and C3–C6) backbone (Tohge et al. 2013a, b). Several isoflavone reductase (IFR) which make isoflavones, classes of flavonoids have been categorized on the flavonol synthase (FLS) required for flavonol biosyn- basis of their core skeleton: C6–C3–C6 (flavonoids), thesis and flavonoid 3′,5′-hydroxylase (F3′5′H) for (C6–C3–C6)2 (biflavonoids) and (C6–C3–C6)n (con- production of 3′,5′-hydroxylated flavonoids. Six major densed tannins). The major flavonoids, in which two types of flavonoid aglycones, flavonols (Fig. 1a e.g. aromatic rings are linked via a three carbon chain kaempferol and quercetin), flavones (Fig. 1b e.g. (C6–C3–C6), have been reported to have manifold apigenin and luteolin), anthocyanidins (Fig. 1c e.g. biological functions in the productive pollen fertility, cyanidin, delphinidin and petunidin), flavanols (Fig. 1d signalling with microorganisms, auxin transport reg- e.g. catechin and epicatechin), isoflavones (Fig. 1e e.g. ulation and pigmentation, as well as in the protection daidzein) and flavanones (Fig. 1f e.g. naringenin and of plants from various environment stresses, for sakuranetin) are the major sub-classes of the flavonoid example high light, UV-B irradiation and pathogens/ family. In addition, additional steps (Zhang et al. 2014) pests (Taylor and Grotewold 2005; Tohge et al. are involved in further decoration such as glycosyla- 2013a, b; Nakabayashi et al. 2014). Additionally they tion and acylation of flavonoids and these exhibit a exhibit a range of diverse functions including roles in large natural diversity and are commonly species- developmental processes in plants (Taylor and Grote- specific (Tohge et al. 2013a, b). Several gene families wold 2005; Silva-Navas et al. 2016; Tohge and have been characterized functionally as being involved Fernie 2016). On the other hand, flavonoids have in flavonoid decoration. Flavonoid glycosyltransferase several health beneficial effects including anti-retro- genes were found in the UDP-sugar-dependent glyco- viral, anti-hypertensive, anti-inflammatory, anti- syltransferase 1 (UGT1) (Yonekura-Sakakibara and aging and insulin-sensitizing activities, the reduction Hanada 2011) and glycoside hydrolase family 1-type of the risk of a range of chronic diseases including (beta glucosidase, BGLU) (Matsuba et al. 2010; cardiovascular disease, cancer and osteoporosis as Ishihara et al. 2016) gene families. Similarly, flavone well as inhibition of low-density lipoprotein (LDL) synthases (FNS-I and FNS-II) have been found from oxidation (Butelli et al. 2008; Crozier et al. 2009; both P450 and 2-oxoglutarate/Fe(II)-dependent dioxy- Zhang et al. 2014; Tohge and Fernie 2016). genase (2-ODD) gene families (Tohge et al. 2013a, b). Some sub-classes of phenylpropanoids, such as Furthermore, flavonoid acyltransferases have been syringyl-lignin and hydroxycinnamate biosynthesis characterized from both the BEAT/AHCT/HCBT/ are consequently widespread in plant lineages even DAT (BAHD) (D’Auria 2006; Tohge et al. 2015; in Angiosperms. On the other hand, some flavonoid Petersen 2016) and the serine carboxypeptidase-like 123 Phytochem Rev A B C R2 R3 R1 R3 R4 OH R1 R2 + HO O HO O HO O R4 R2 OH OH R1 OH O OH O OH chrysin: R =H, R =H, R =H, R =H 1 2 3 4 pelargonidin: R =H, R =H kaempferol: R1=H, R2=H, R3=OH, R4=H apigenin: R =H, R =H, R =H, R =OH 1 2 1 2 3 4 cyanidin: R =OH, R =H quercetin: R1=H, R2=OH, R3=OH, R4=H luteolin: R =H, R =H, R =OH, R =OH 1 2 1 2 3 4 peonidin: R =OMe, R =H isorhamnetin: R1=H, R2=OMe, R3=OH, R4=H scutellarein: R =OH, R =H, R =H, R =OH 1 2 1 2 3 4 delphinidin: R =OH, R =OH myricetin: R1=H, R2=OH, R3=OH, R4=OH baicalein: R =OH, R =H, R =H, R =H 1 2 1 2 3 4 petunidin: R =OMe, R =OH kaempferide: R1=H, R2=H, R3=OMe, R4=H vitexin: R =H, R =-C-Glc, R =H, R =OH 1 2 1 2 3 4 malvidin: R =OMe, R =OMe gossypetin: R1=OH, R2=OH, R3=OH, R4=H 1 2 D E F OH R2 O OH HO R3 HO O R1 O R2 R2 O R1 R1 OH OH OH O daidzein: R =H, R =H naringenin: R =H, R =H, R =OH catechin: R1= OH, R2=H 1 2 1 2 3 genistein: R =OH, R =H sakuranetin: R =OMe, R =H, R =OH epicatechin: R1= OH, R2=H 1 2 1 2 3 glycitein: R =, R =OMe isosakuranetin: R =OH, R =H, R =OMe gallocatechin: R1= OH, R2=OH 1 2 1 2 3 eriodictyol: R =OH, R =OH, R =OH epigallocatechin: R1= OH, R2=OH 1 2 3 hesperitin: R1=OH, R2=OH, R3=OMe Fig. 1 Major flavonoid aglycones in land plants. a Flavonols, b flavones, c anthocyanidins, d flavanols, e isoflavones and f flavanones (SCPL) (Tohge et al. 2016) gene families. Interest- and reprogramming under light stress. Part of this ingly, the same or highly similar products can be metabolic reprograming induces production of phyto- formed by enzymes from different gene families using protectants such as phenylpropanoids in land plants. differently-activated substrates. Such evolutionary Enhancing our understanding of gene conservation and convergence of flavonoid decoration enzymes has the corresponding specificity of flavonoids in nature is been subject to natural selective pressures which important for future studies in which interesting natural generate mechanisms for tolerance to environmental variants are characterized at the molecular genetic, stress such as that imposed by natural UV-B (280– biochemical and physiological levels to lay the foun- 315 nm) irradiation (Jenkins 2009; Tilbrook et al. dations for the design of stress resistant crop plants. 2013) and photo-oxidative damage induced by photo- Natural chemical diversity of functional phyto- inhibition (Steyn et al. 2002;). Such effects of irradi- chemicals often corresponds to the evolution of ance in UV-B wavelength range on plants has been adaptation to specific environments, and therefore widely studied, since UV-B causes primary effects of the understanding of natural diversity using a broad non-specific damage to DNA, RNA, proteins and lipid range of accessions offers a very powerful tool to membranes as well as secondary effects such as investigate phytochemical functions in nature.