Flavonoid mediated selective cross-talk between plants and beneficial soil microbiome

Abstract

Plants generate a wide variety of organic components during their different growth phases. The majority of those compounds have been classified as primary and secondary metabolites. Secondary metabolites are essential in plants' adaptation to new changing environments and in managing several biotic and abiotic stress. It also invests some of its photosynthesized carbon as secondary metabolites to establish a mutual relationship with soil microorganisms in that specific niche. As soil harbors both pathogenic and beneficial microorganisms, it is essential to identify some specific metabolites that can discriminate beneficial and pathogenic ones. Thus, a detailed understanding of metabolite's architectures that interact with beneficial microorganisms could open a new horizon of ecology and agricultural research. Flavonoids are used as classic examples of secondary metabolites in this study to demonstrate recent developments in understanding and realizing how these valuable metabolites can be controlled at different levels. Most of the research was focused on plant flavonoids, which shield the host plant against competitors or predators, as well as having other ecological implications. Thus, in the present review, our goal is to cover a wide range of functional and signalling activities of secondary metabolites especially, flavonoids mediated selective cross-talk between plant and its beneficial soil microbiome. Here, we have summarized recent advances in understanding the interactions between plant species and their rhizosphere microbiomes through root exudates (flavonoids), with a focus on how these exudates facilitate rhizospheric associations.

Supplementary information: The online version contains supplementary material available at 10.1007/s11101-022-09806-3.

Keywords: Flavonoids; NodD–flavonoid complex; Plant–microbe interactions; Quorum sensing; Secondary metabolites.

Fig. 1

Diversity and roles of plant metabolites. Plants undergo a range of stresses and biotic disruptions in their natural environments, resulting in the activation of stress and defensive responses induced by signalling mechanisms and different pathways to fulfil cellular functions necessary for physiological processes. The physiological mechanisms have an effect on primary metabolites, which provides different biosynthetic intermediates for secondary metabolites, with concomitant impact on biosynthesis of bioactive compounds. This is usually determined by the plant’s genotype, species and cultivar, as well as its developmental stage and physiological condition

Fig. 2

Vesicle mediated flavonoid transport. After anthocyanin biosynthesis (biosynthetic site-endoplasmic reticulum), they are transported to the vacuolar membrane and sequestered. Anthocyanins are transported by macrophagocytosis or microphagocytosis via ER-derived vesicles. On the other site, the transporter-mediated pathway is facilitated by vacuole-associated proteins such as ABC, BTL and MATE-like transporters. GSTs function as ligandins, via the formation of glutathione conjugated anthocyanins, to accommodate the efficient and dynamic transport of anthocyanins from endoplasmic reticulum to vacuoles

Fig. 3

Signalling interactions between Rhizobium and legume root. Flavonoids are secreted by legume roots to Rhizobium. That plant secreted flavonoids enter the cytoplasm of Rhizobium through cell membrane and activate rhizobial NodD by conformational modifications. Activated NodD binds to the nod box in the promoter region of nod genes to induce the enzymatic expressions needed for nod factors synthesis. Nod factors attach to it’s receptors on plant root hairs to induce nodule formation by deformation of root hair and cortex cell division

Fig. 4

In silico binding studies of NodD protein of Rhizobium leguminosarum bv. trifolii (UniProtKB - P04680 ) and each flavonoids (Table 1). Here NodD–flavonoid complex were arranged based on their binding affinities (more negative values represent stronger interaction). EachNodD–flavonoid complexformhydrogen (green dotted line between amino acid and flavonoid) andhydrophobic bond (red half circles) during NodD–flavonoid interaction. The central picture (present inside the oval circle) predicted binding sites of 19 flavonoids in NodD protein of Rhizobium leguminosarum bv. trifolii (UniProtKB-P04680 ). Individual higher regulation figures have been supplied in supplementary data (Figs. S2, S3)

Fig. 5

Mechanisms and impacts of QS communication system used in different kinds of interactions between plants and microorganisms. Plant and microbial associations are accelerated by several chemical signals exchanged between them. Plant species exude a variety of chemical substances in the rhizosphere, in order to easily interact with their nearby soil microorganisms and these chemical compounds are also involved in attracting beneficial microbes, activation of several microbial traits and the formation of mutualistic relationships in the rhizosphere. QS molecules are used by several rhizobacteria to colonies plant surfaces or plant-associated environments through quorum sensing-mediated expression of genes. Bacteria also produce phytohormones, anti-microbial compounds, volatiles to induce defense proteins, metabolites and promote the growth and development of plant species by reducing oxidative stress and allelopathic effects