How relevant are flavonoids as antioxidants in plants?

Flavonoids are a large family of plant secondary metabolites, principally recognized for their health-promoting properties in human diets. Most flavonoids outperform well-known antioxidants, such as ascorbate (vitamin C) and α-tocopherol (vitamin E), in in vitro antioxidant assays because of their strong capacity to donate electrons or hydrogen atoms. However, experimental evidence for an antioxidant function in plants is limited to a few individual flavonoids under very specific experimental and developmental conditions. As we discuss here, although flavonoids have been demonstrated to accumulate with oxidative stress during abiotic and biotic environmental assaults, a convincing spatio-temporal correlation with the flavonoid oxidation products is not yet available. Thereby, the widely accepted antioxidant function of flavonoids in plants is still a matter of debate.

Introduction

Flavonoids are a family of plant secondary metabolites of >9000 individual molecules found in all tissues and organs [1]. Together with bryophytes and pteridophytes, higher plants are the only natural source of flavonoids [2], many of which are considered to be nutraceuticals (see Glossary) [3]. In plants, flavonoids are involved in an array of processes, including plant–pathogen interactions, pollination, light screening, seed development and allellopathy [4]. Many flavonoid biosynthetic genes are induced under stress conditions and, accordingly, flavonoid levels increase during exposure to biotic and abiotic stresses, such as wounding, drought, metal toxicity and nutrient deprivation 5, 6. A common denominator in these environmental stress conditions is the production and accumulation of reactive oxygen species (ROS), such as superoxide anions (O₂^–), hydrogen peroxide (H₂O₂), hydroxyl radicals (OH) and singlet oxygen (¹O₂). ROS accumulation leads to oxidative stress that can damage cellular components, such as DNA, lipids, proteins and sugars 7, 8. To minimize oxidative stress-related traumas, ROS homeostasis in plants is tightly regulated by a complex machinery of enzymatic and non-enzymatic antioxidants [9]. Flavonoids have been suggested to act as antioxidants, protecting plants from oxidative stress.

Adapting previous definitions 10, 11 to an in planta situation, we consider an antioxidant to be a molecule that: (i) could donate electrons or hydrogen atoms (i.e. low reduction potential); (ii) yields an antioxidant-derived radical that (iii) is efficiently quenched by other electron or hydrogen sources to prevent cellular damage; and (iv) whose properties are spatially and temporally correlated with oxidative stress events.

For new antioxidant candidates, the first hint for an in planta function is given by high performance within established in vitro antioxidant tests (Box 1). In these assays, the antioxidant capacities of flavonoids are several-fold higher than those of ascorbate (vitamin C) or α-tocopherol (vitamin E), two well known in planta antioxidants [12]. Here, we evaluate experimental data that suggest that flavonoids have an in planta antioxidant function; however, many aspects of this putative function remain unclear, thereby suggesting that the putative antioxidant function of flavonoids is still a matter of debate.