The hidden power of secondary metabolites in plant-fungi interactions and sustainable phytoremediation

Abstract

The global environment is dominated by various small exotic substances, known as secondary metabolites, produced by plants and microorganisms. Plants and fungi are particularly plentiful sources of these molecules, whose physiological functions, in many cases, remain a mystery. Fungal secondary metabolites (SM) are a diverse group of substances that exhibit a wide range of chemical properties and generally fall into one of four main family groups: Terpenoids, polyketides, non-ribosomal peptides, or a combination of the latter two. They are incredibly varied in their functions and are often related to the increased fitness of the respective fungus in its environment, often competing with other microbes or interacting with plant species. Several of these metabolites have essential roles in the biological control of plant diseases by various beneficial microorganisms used for crop protection and biofertilization worldwide. Besides direct toxic effects against phytopathogens, natural metabolites can promote root and shoot development and/or disease resistance by activating host systemic defenses. The ability of these microorganisms to synthesize and store biologically active metabolites that are a potent source of novel natural compounds beneficial for agriculture is becoming a top priority for SM fungi research. In this review, we will discuss fungal-plant secondary metabolites with antifungal properties and the role of signaling molecules in induced and acquired systemic resistance activities. Additionally, fungal secondary metabolites mimic plant promotion molecules such as auxins, gibberellins, and abscisic acid, which modulate plant growth under biotic stress. Moreover, we will present a new trend regarding phytoremediation applications using fungal secondary metabolites to achieve sustainable food production and microbial diversity in an eco-friendly environment.

Keywords: Arbuscular mycorrhizal fungi (AMF); biotrophic fungi; phytopathogenic fungi; phytoremediation; plant metabolic response; secondary metabolites; siderophore; soil mycobiota.

Figure 1

A schematic diagram to show the different plant responses against pathogenic fungi in the absence and presence of Arbuscular mycorrhizal fungi (AMF) colonization. (A) Absence of root colonization by AMF causes more damage when compared to mycorrhizal plants due to the development of symptoms in response to necrotrophic and biotrophic pathogens. In addition, host plants with undeveloped root systems have a low ability to uptake nutrients from the soil, leading to plant death by the end. (B) A symbiotic relationship between plant roots and Arbuscular mycorrhizal fungi (AMF) significantly alters ecosystems and impacts plant production via plant growth promotion due to improved acquisition of mineral nutrients through the extensive AM fungal hyphal network (mycorrhizosphere) with a massive mycorrhizal network around the root system. Furthermore, host plants can thrive under various abiotic/biotic stresses (including drought, salt, herbivory, temperature, metals, and pathogens) due to the symbiotic localization of Arbuscular mycorrhizal fungi (AMF) via complex signal communications that increase the photosynthetic plant rate. Hence, the release of strigolactones (SLs) as part of the root exudates induces the branching of AMF hyphae to promote mycorrhization. Changes in the root exudate patterns induce changes in the soil microbial community, possibly by attracting antagonists of pathogens. In addition, there are various ways of AMF-induced biotic stress tolerance in plants via competition with soil pathogens and nutrients uptake, altered root exudates which support beneficial microbes and suppress phytopathogens in the rhizosphere, AMF colonized roots have little or no space for pathogen entry. Interestingly, a general reduction in the damage and incidence of disease caused by soilborne pathogens was noticed due to defense power from the priming of the plant. The role of the phytohormones (e.g., JA and ET) in the relationship between the host plant and its symbiotic fungi are well known. Phytohormones participate as signaling molecules and improve host plant ISR (Induced Systemic Resistance). In contrast, the development of necrotrophic pathogens in plant–fungal pathogen interaction signals is restricted due to the primed jasmonate-regulated plant defense mechanisms.

Figure 2

Schematic shows the fungal bioinoculants) applications in response to diverse stress conditions.

Figure 3

Conceptual representation of the phytoremediation of metal ions by fungal siderophores. The chemical structures of selected fungal siderophores (fusarinine C, ferrichrome A, coprogen, and rhodothorulic acid) and an example of a siderophore-metal complex (Fusarinine C-ferric complex).