Plant Flavonoids in Mediterranean Species: A Focus on Flavonols as Protective Metabolites under Climate Stress

Abstract

Flavonoids are specialized metabolites largely widespread in plants where they play numerous roles including defense and signaling under stress conditions. These compounds encompass several chemical subgroups such as flavonols which are one the most represented classes. The most studied flavonols are kaempferol, quercetin and myricetin to which research attributes antioxidative properties and a potential role in UV-defense through UV-screening mechanisms making them critical for plant adaptation to climate change. Despite the great interest in flavonol functions in the last decades, some functional aspects remain under debate. This review summarizes the importance of flavonoids in plant defense against climate stressors and as signal molecules with a focus on flavonols in Mediterranean plant species. The review emphasizes the relationship between flavonol location (at the organ, tissue and cellular scales) and their function as defense metabolites against climate-related stresses. It also provides evidence that biosynthesis of flavonols, or flavonoids as a whole, could be a crucial process allowing plants to adapt to climate change, especially in the Mediterranean area which is considered as one of the most sensitive regions to climate change over the globe.

Keywords: antioxidant; biological function; biosynthesis; defense mechanism; leaves; localization; reactive oxygen species; secondary metabolism; stress response.

Figure 1

Structure and classification of flavonoids. The main subclasses of major flavonols are circled in blue. The difference between flavonoid groups depends on the chemical structure, the degree of oxidation, and the unsaturation of the linking chain (C3). Flavonols differ from each other in the number and position of the hydroxyl groups (-OH). The ortho-dihydroxy structure of quercetin is circled in orange.

Figure 2

Biosynthesis and subcellular localization of flavonols in leave tissues. Flavonols are synthesized in the cytoplasm, on the cytosolic face of the endoplasmic reticulum (ER) (right picture). The different enzymes involved in their biosynthesis (left box) are shown in blue and flavonols are indicated and framed by different colors. The pathway shown represents the general pathway found in model plants such as Arabidopsis thaliana. The first step begins with the synthesis of phenylalanine in the chloroplasts which is then transported to the cytosol via the phenylalanine plasticial cationic amino acid transporter (PhpCAT), identified in petunia. Abbreviations are as follows: C4H, cinnamate 4-hydroxylase; CHI, chalcone isomerase; CHS, naringenin-chalcone synthase; DFR, bifunctional dihydroflavonol 4-reductase/flavanone 4-reductase; F3H, flavanone 3-hydroxylase; F3′H, flavonoid 3′-hydroxylase; F3′5′H, flavonoid 3′5′-hydroxylase; FLS, flavonol synthase; LDOX, leucoanthocyanidin dioxygenase; PAL, phenylalanine ammonia-lyase; Phe, phenylalanine; UGT, UDP-dependent glucosyl transferase. Once synthetized, flavonols can be subjected to various modifications (glycosylation, methylation, etc.) and be stocked into vacuoles. They are transported into different compartments and through cells by MATE (multidrug and toxic compound extrusion) and ABC (ATP binding cassette) transporters families. In nucleus, vacuole, and chloroplast, flavonols will inhibit ROS accumulation.

Figure 3

Plant responses to abiotic stress. The colored boxes summarize the four abiotic stresses referred to in this review and their main consequences for plant physiology. Flavonols’ role as ROS scavengers and their interaction with the phytohormones ABA in leaves and auxin in roots is shown in black boxes. In leaves, the opening of stomata is allowed by the binding of ABA to membrane receptors resulting in an efflux of ions and therefore an efflux of water leading to stomata closure. ABA act on the R2R3-MYB gene by enhancing its expression thus stimulating flavonol biosynthesis. It also triggers a signaling cascade leading to ROS production. In roots, flavonols inhibit auxin transport leading to auxin accumulation and root elongation.