Regulation of Plant Tannin Synthesis in Crop Species

Abstract

Plant tannins belong to the antioxidant compound family, which includes chemicals responsible for protecting biological structures from the harmful effects of oxidative stress. A wide range of plants and crops are rich in antioxidant compounds, offering resistance to biotic, mainly against pathogens and herbivores, and abiotic stresses, such as light and wound stresses. These compounds are also related to human health benefits, offering protective effects against cardiovascular and neurodegenerative diseases in addition to providing anti-tumor, anti-inflammatory, and anti-bacterial characteristics. Most of these compounds are structurally and biosynthetically related, being synthesized through the shikimate-phenylpropanoid pathways, offering several classes of plant antioxidants: flavonoids, anthocyanins, and tannins. Tannins are divided into two major classes: condensed tannins or proanthocyanidins and hydrolysable tannins. Hydrolysable tannin synthesis branches directly from the shikimate pathway, while condensed tannins are derived from the flavonoid pathway, one of the branches of the phenylpropanoid pathway. Both types of tannins have been proposed as important molecules for taste perception of many fruits and beverages, especially wine, besides their well-known roles in plant defense and human health. Regulation at the gene level, biosynthesis and degradation have been extensively studied in condensed tannins in crops like grapevine (Vitis vinifera), persimmon (Diospyros kaki) and several berry species due to their high tannin content and their importance in the food and beverage industry. On the other hand, much less information is available regarding hydrolysable tannins, although some key aspects of their biosynthesis and regulation have been recently discovered. Here, we review recent findings about tannin metabolism, information that could be of high importance for crop breeding programs to obtain varieties with enhanced nutritional characteristics.

Keywords: antioxidants; biosynthesis; ellagitannins (ETs); flavonoids; fruits; proanthocyanidins.

FIGURE 1

Schematic of shikimate pathway reactions. 3-dehydroshikimate and chorismate are highlighted in red as the precursors of hydrolysable tannins and proanthocyanidins, respectively. Abbreviations: phosphoenolpyruvate (PEP), erythrose 4-phosphate (E4P), inorganic phosphate (P_i), 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS), 3-deoxy-D-arabino-heptulosonate-7-phosphate (DAHP), dehydroquinate synthase (DHQS), 3-dehydroquinate (3-DHQ), 3-dehydroquinate dehydratase (DHQD), 3-dehydroshikimate (3-DHS), shikimate dehydrogenase (SDH), shikimate kinase (SK), shikimate-3-phosphate (S3P), 5-enolpyruvylshikimate 3-phosphate synthase (EPSPS), 5-enolpyruvylshikimate-3-phosphate (EPSP), and chorismate synthase (CS). Adapted from Vogt, 2010; Akagi et al., 2011; Mir et al., 2015; Stefanachi et al., 2018.

FIGURE 2

Schematic of the structure of catechins and proanthocyanidins. (A) General structure of a catechin, where (A–C) indicate the distinct rings of the carbon backbone C6-C3-C6, numbers 2 and 3 indicate the chiral carbons (stereochemistry not shown), and R₁, R₂ and R₃ are the possible substituent groups. (B) An example of a catechin (+)-catechin. (C) General structure of a proanthocyanidin, where n indicates the number of repetitions of the monomer in brackets. The bond between the monomers is called an interflavan linkage.

FIGURE 3

Simplified flavonoid pathway. One branch of this pathway yields flavanols that can be transported to the vacuole by several proposed mechanisms. Abbreviations: flavonoid 3-hydroxylase (F3H), flavonoid 3′-hydroxylase (F3′H), flavonoid 3′5′-hydroxylase (F3′5′H), dihydroflavonol 4-reductase (DFR), anthocyanidin synthase (ANS), UDP-glucose flavonoid 3-O-glucosyltransferase (UFGT), anthocyanidin reductase (ANR), and leucoanthocyanidin reductase (LAR). Modified from Akagi et al., 2011; Yu et al., 2020; Wei et al., 2021.

FIGURE 4

General regulation scheme of proanthocyanidin synthesis. The scheme shows regulation via MBW-complex formation and cold-, light- and wounding-induced regulation. The degradation of MdMYB9/11 through BT2 and the proteasome is also shown with the red arrows, resulting in the impossibility of these two transcription factors to form the MBW-complex. Arrows indicate positive regulation, while flat-ended lines mean negative regulation (repression). Dotted lines indicate a process not fully elucidated. At: Arabidopsis thaliana, Dk: Diospyros kaki, Fa: Fragaria x ananassa, Md: Malus domestica, Pp: Prunus persica, Vv: Vitis vinifera.

FIGURE 5

Biosynthetic pathway of hydrolysable tannins. The hydrolysis of gallotannins and ellagitannins yields gallic acid and sugar (glucose represented) and gallic acid, ellagic acid, and sugar, respectively. Dotted lines represent multistep reactions. Abbreviations: 3-dehydroshikimate (3-DHS), gallic acid (GA), sugar unit (S), ellagic acid (EA), β-glucogallin (β-GG), pentagalloylglucose (PGG), shikimate dehydrogenase (SDH), and β-glucogallin-dependent galloyltransferases (GGT).