Flavonoids Are Intra- and Inter-Kingdom Modulator Signals

Abstract

Flavonoids are a broad class of secondary metabolites with multifaceted functionalities for plant homeostasis and are involved in facing both biotic and abiotic stresses to sustain plant growth and health. Furthermore, they were discovered as mediators of plant networking with the surrounding environment, showing a surprising ability to perform as signaling compounds for a multitrophic inter-kingdom level of communication that influences the plant host at the phytobiome scale. Flavonoids orchestrate plant-neighboring plant allelopathic interactions, recruit beneficial bacteria and mycorrhizal fungi, counteract pathogen outbreak, influence soil microbiome and affect plant physiology to improve its resilience to fluctuating environmental conditions. This review focuses on the diversified spectrum of flavonoid functions in plants under a variety of stresses in the modulation of plant morphogenesis in response to environmental clues, as well as their role as inter-kingdom signaling molecules with micro- and macroorganisms. Regarding the latter, the review addresses flavonoids as key phytochemicals in the human diet, considering their abundance in fruits and edible plants. Recent evidence highlights their role as nutraceuticals, probiotics and as promising new drugs for the treatment of several pathologies.

Keywords: abiotic stress; beneficial microbes; biotic stress; microbiome; phytobiome; phytochemicals; plant secondary metabolites; plant-microbe interactions; rhizosphere; root exudates.

Figure 1

Flavonoid role in plant physiology under abiotic stress. To cope with poor nutrient availability and a variety of abiotic stresses featured by oxidative stress, plants trigger an enhanced synthesis of flavonoids that contributes to tune plant homeostasis and development. A schematic representation of the main structural components and substituent positions in the flavonoid backbone is reported in the image.

Figure 2

Plant intra- and inter-kingdom interactions mediated by flavonoids. The main aboveground and underground multitrophic interactions, that are orchestrated by flavonoids, are illustrated in the figure. The release of these phytochemicals in the soil modulates allelopathic interactions with neighbor plants and the symbiotic relationship with rhizobia and arbuscular mycorrhizal fungi (AMF). It also mediates rhizocompetence traits of plant growth promoting rhizobacteria (PGPR), exerts antimicrobial and antifungal functions against phytopatogens and stimulates the bacterial catabolism for xenobiotics degradation. Furthermore, flavonoids can tune interactions with beneficial and opportunistic insects. Recently, flavonoids have been proposed as nutraceutical and prebiotics for human health. The image was partially realized using graphic contents from Biorender (https://biorender.com/ (accessed on 2 October 2022)).

Figure 3

Flavonoid-mediated plant defense strategies against biotic stress caused by phytopathogen attacks. The attack by microbial phytopathogens induces plant defense responses (represented by the thunder symbol), including an enhanced flavonoid production and exudation. Flavonoids play numerous roles in plant defense against biotic stresses: they are quorum-sensing inhibitors, pro-oxidants and some of them are defined as phytoalexins and phytoanticipins defense compounds. These features confer flavonoids with antibacterial and antifungal activities that are mediated by a diverse array of mechanisms, some of which are reported in the figure. The down-oriented arrow (↓) represents an inhibitory effect, whereas the up-oriented arrow (↑) represents an induction effect.

Figure 4

Role of flavonoids in the plant “cry-for-help” strategy to cope with environmental stresses. Modification of root chemistry is part of the physiological responses that plants adopt to cope with environmental stresses (represented by the thunder symbol). This phenomenon is known as “cry-for-help” and it induces, among others, the exudation of flavonoids in the rhizosphere. These phytochemicals play multiple roles in the recruitment of soil microorganisms, which can establish beneficial interactions with the host plant and contribute to the holobiont fitness, mitigating the stress deleterious effects. Flavonoids can be exploited as nutrients, induce efficient colonization of the root system and act as inducers for the expression of catabolic genes for the degradation of xenobiotic compounds. In turn, beneficial microbes colonizing the rhizosphere and the endosphere can affect the root exudation pattern (dashed arrow), favoring the establishment of suitable conditions for their growth in these niches.

Figure 5

Flavonoids-mediated enhancement of the PCB degrading metabolism. The PCB-degrading strain Pseudomonas strain JAB1 was placed in close contact with flavone, which is able to induce its degradative metabolism [211] as visible by the yellow coloration assumed by the grown colonies, possibly due to the presence of a degradation intermediate [212]. The red dots represent the sites in which the solvent (control) or the flavonoid flavone were plated, according to the protocol for chemotaxis described by Reyes-Darias and colleagues [213]. Picure by Elisa Ghitti and Eleonora Rolli.