One of the most notable and studied class of phytochemicals are phenolic compounds (PC), which from a chemical perspective are characterised by one or more hydroxyl groups (-OH) attached to an aromatic hydrocarbon group. Phenol (C₆H₆O) stands as the fundamental chemical structure on which this group (ranging from simple phenolics to complex and highly polymerized compounds) is based (Vermerris and Nicholson, 2006). Through LC-MS and GC-MS identification, PC were by far the most frequently described phytochemicals in legume varieties with phenolic acids, flavonoids and condensed tannins the primary sub-classes found in seeds (Tor-Roca et al., 2020).

Phenolic acids are relatively small molecules when compared to other PC such as flavonoids or tannins, and they are characterised by a phenol with a carboxylic acid functional group (Vermerris and Nicholson, 2006). They include hydroxybenzoic acid derivatives, gallic, vanillic and syringic acids and hydroxycinnamic acid derivatives such as caffeic, ferulic, p-coumaric and sinapic acids (Singh et al., 2017). Flavonoids, in turn, stand out as one of the most prevalent group of PC which is particularly abundant in various types of legumes (Tor-Roca et al., 2020). With two benzene rings linked together by a group of three carbons they are divided into anthocyanin- (coloured), and anthoxanthin- (colourless) compounds. Anthoxanthins are divided further into flavones, flavans, flavonols, and isoflavones, the latter almost exclusively found in leguminous plants (Mutha et al., 2021). Daidzein and genistein, major isoflavones present in soybean (Glycine max), have been linked to reduced risk of certain types of cancer, namely prostate (Adjakly et al., 2013), and breast cancer (Sohel et al., 2022).

Tannins are a class of compounds that have a wide structural diversity and share the ability to conjugate with polysaccharides and proteins. They are usually divided into two groups: hydrolysable- or condensed-tannins, with the former being able to undergo hydrolysis, and produce carbohydrates and phenolic acids. In contrast, condensed tannins are more stable and obtained through the condensation of flavan-3-ols (Hill, 2003). Like almost all PC, tannins have shown antioxidant properties and bioactive potential. Nevertheless, the complexes formed between tannin-protein can reduce protein digestibility and inactivate digestive enzymes, thus the perception of these compounds as (solely) ‘anti-nutritional’ factors (Samtiya et al., 2020). Regardless, it is important to assess their health benefits alongside possible undesired effects (Geraldo et al., 2022).

Lignans are part of a group of diphenolic compounds and have been extensively studied for their health benefits due to their steroid-analogous chemical structure (Senizza et al., 2020). They share some chemical and structural characteristics with lignin which is a phenolic polymer found in the cell walls of legumes and other plants, and it is the third most abundant biopolymer on Earth (Pérez et al., 2002; Vermerris and Nicholson, 2006). As a complex polymer possessing a cross-linked structure, lignin is relatively resistant to mineralisation or decomposition, and can be found in high concentrations in woody tissues, contributing to both plant- and soil-health (Frei, 2013).

The biological activities of PC are frequently centred on extractable phenolic compounds, meaning compounds that can be easily extracted from the matrix using water or organic solvents, or a mixture of these. Yet, it is now recognized that this approach overlooks the non-extractable PCs or bound phenolics - a considerable proportion of dietary polyphenolics, which are not extracted using traditional methods (Silva et al., 2018). Several legume crop species have been shown to possess high amounts of both PC and dietary fibre (polysaccharides) in the food and in-field residue components, which in turn leads to bound phenolics in their matrices. Legume PCs interact with each other and other compounds, such as carbohydrates, proteins, or lipids, through reversible noncovalent and mostly irreversible covalent interactions, impairing the bioavailability of these bound phenolics (Rocchetti et al., 2022).

Alkaloids are a diverse group of chemicals that possess alkali-like properties and consist of at least one N atom within a heterocyclic ring structure. While not all legumes contain alkaloids, some species are known to produce these compounds, with significant contribution to plant growth and defence. For instance, faba beans and peas have residual alkaloids concentrations but, quinolizidine alkaloids are common and well-documented among commercially important lupin genotypes. They have garnered significant attention from farmers and breeders due to their potent bitter taste and potential toxicity at high doses (Pereira et al., 2022), which is why it is recommend they remain below the industry threshold of 0.02% (Boschin et al., 2008). Nevertheless, recent studies show that lupanine, one of the prevalent alkaloids of the genus Lupinus in both their foliage and their seed (Hill, 2003), has been shown to have anti-inflammatory and anti-cancer properties (Guerra-Ávila et al., 2023). Sparteine, another lupin alkaloid, has been associated with antiarrhythmic and anticonvulsant properties (Frick et al., 2017), showcasing the dual nature of alkaloids in legumes as both anti-nutritional factors and potential pharmaceutical agents.

Saponins (a group of terpenoids) in legumes are present in the form of triterpenoid glycosides or steroids that have a variety of biological activities (Mustafa et al., 2022). Due to their surfactant character, they have the ability to produce foam, and are often responsible for the soapy taste and bitter flavour of some legume species (Shi et al., 2004). Some of the most studied saponins in legumes include soyasaponins, which are found in soybeans and other members of the legume family, such as lentil and pea (Tor-Roca et al., 2020). These compounds have been shown to have a range of biological activities, including cholesterol-lowering effects, anti-cancer properties, and anti-inflammatory effects (Guang et al., 2014). However, in addition to their bitter taste, saponins can be toxic when present in high concentrations and may exert adverse effects on nutrient absorption. This is primarily due to their capacity to inhibit metabolic and digestive enzymes, as well as their tendency to bind to essential nutrients like zinc (Samtiya et al., 2020), emphasising the trade-off that we have with most of these phytochemicals between positive and disadvantageous traits.

Legumes are also a high dietary source of phytosterols (steroid compounds derived from plants), and these comprise the bulk of unsaponifiable substances found in plant lipids (Salehi et al., 2020). Structurally similar to cholesterol, they are thought to have cholesterol-lowering effects (Gupta et al., 2011), hence they are regarded as important dietary elements for upholding good cardiovascular health. Lentil hulls have been found to contain elevated concentrations of phytosterols, namely β-Sitosterol (Mustafa et al., 2022), which has potential as a notable drug of the future due to their action as a neuroprotective and chemopreventive agent (i.e., preventing, reversing of blocking invasive cancers) (Babu and Jayaraman, 2020).

Phytic acid, also known as phytate, myo-inositol hexakisposphate or IP6, is present in several legumes but its concentration can vary greatly among pulses, with considerable discrepancies between high-phytic acid species as common bean or pea and low-phytic acid species, like faba bean and lentils (Sinkovič et al., 2023). Phytic acid can also complex both micro- and macro-elements, potentially leading to a reduction in the bioavailability of minerals, protein function, and ion cofactors to ensure proper enzymatic function (Shi et al., 2018). When consumed within the recommended daily doses, nonetheless, phytates have important health benefits, either chelating toxic metals or through anticarcinogenic properties and antioxidant activity (Geraldo et al., 2022). The majority of the phosphorus contained within seeds exists in the form of phytic acid (Gupta et al., 2015).

Oligosaccharides from the raffinose family, also known as α-galactosides, have bonds between galactose residues ranging from one to six. In humans, the enzyme needed to break down these compounds is not found in the small intestine. As a result, consuming grains like fava beans and peas (Carbas et al., 2021), which contain these oligosaccharides, often leads to excessive quantities of intestinal gas, and stomach discomfort (Pereira et al., 2022). Despite these unwanted side effects, legume-derived raffinose family oligosaccharides are increasingly being included in pro- and pre-biotics. They also show potential in combating obesity and diabetes and preventing non-alcoholic fatty liver disease (Elango et al., 2022).

With agroecological outcomes ranging from local (impacts on soil health and fertility) to global scales (emission of greenhouse gases) (Berihu et al., 2023), the soil microbiome and its interaction with plants and their phytochemicals is of upmost importance, due to their potential to support sustainable and regenerative agriculture, and downstream food- and feed-systems.

The symbiotic relationship between legumes and soil bacteria is a well-established and vital component of sustainable agroecosystems. To study the rhizosphere, the soil zone influenced by plant roots, researchers use techniques such as DNA-based assays or transcriptomics to identify changes in microbial communities and gene expression. In addition, rhizobia are one of the most studied soil microbe types considering their role in initiating nodule formation in the roots (or stems) of legumes, where the aforementioned BNF occurs. This process involves a series of biochemically directed steps, which includes colonization and nodule organogenesis, where various phytochemicals come into play, with flavonoids being one example. When released by legume roots as component of their exudate, flavonoids can act as chemo-attractants, facilitating the movement of compatible rhizobia ( Figure 2 ) towards the roots and enhancing the colonization and infection process, root nodule formation and so the efficiency of BNF (Cooper, 2004; Abdel-Lateif et al., 2012). Conversely, legume flavonoids may exhibit antimicrobial activities that influence the overall recruitment and functioning of the root microbiome. This negative effect on specific taxa recruitment, for example on parasitic nematodes, fungus, and pathogenic bacterial species (e.g. Pseudomonas mars-prunorum and P. phaseolicola) (Shah and Smith, 2020) highlights the complex interplay of these different mechanisms of action, underscoring the intricate relationship between legume phytochemicals and microbial populations in the soil. Additionally, flavonoids can even act as regulators of nodulation (nod genes) in rhizobia, which are essential for producing species-specific Nod factors. These factors, in turn, trigger specific changes in plant tissue, such as root cortical cell division and root hair curling, which are critical modifications for nodule organogenesis (Hassan and Mathesius, 2012). The ability to modulate certain microbial communities through flavonoid metabolism is an area of increasing interest. This research has potential applications, including extending nodulation to plants beyond legumes (Abdel-Lateif et al., 2012) or engineering plant phytochemicals to influence beneficial microbiomes (Wang et al., 2022).

Phenolic acids are also commonly presented by legume roots as exudate, and may accumulate in soil, to be used as a source of carbon by several rhizobia species, influencing legume-microbe symbiosis (Seneviratne and Jayasinghearachchi, 2003). In some instances, specific taxa as Rhizobia and Pseudomonas, have been identified as capable of breaking down flavonoids compounds into simpler structures, namely phenolic acids (Wang et al., 2022). For example, protocatechuic acid was found to be responsible for the indirect allelopathic effects of catechin, a flavonoid (Wang et al., 2014). Research suggests that the accumulation of phenolic acids led to an increased relative abundance of Bacteroidetes and Firmicutes, which utilize these compounds as growth substrates (Bai et al., 2019), and have been correlated with detrimental impacts on soil micro-ecological environment. An increase in Pseudomonas population, on the other hand, was shown to promote plant growth while degrading phenolic acids present in the rhizosphere (Wang Y. et al., 2021). These findings collectively highlight that the accumulation of phenolic acids alters microbial community structure, even as the specific mechanism of influence and their consequential effects on soil ecology and plant growth remains unclear.

Although most research has focused on the regulation by flavonoid signalling rather than by phenolic acids, there is growing evince for phenolics as determinants of nodulation. A recent study based on ultra-high-performance liquid chromatography-tandem-quadrupole mass spectrometry has reported an increased plant growth and number of nodules in L. japonicus, due to the action of three phenolic acids (p-coumaric, caffeic, and ferulic) enhancing nod genes expression, thus being considered a novel type of nod inducers (Shimamura et al., 2022). The wide range of phenolic compound classes reflects their multifaceted impact on the soil microbial community, which is important to prevent or mitigate dysbiosis in soil microbiomes that would then affect plant yield and overall nutritional quality (Giovannetti et al., 2023). Given the close link between plant nutrition and human health (Hoffmann et al., 2022), this foreshadows the importance of legume phytochemicals with microbe-modulating properties to support the One Health approach ( Figure 2 ).

Besides phenolics, organic acids are key determinants on soil microbiome structure and function. It was reported in a metagenomic approach that organic acid exudation by legume roots, when compared to wheat, explained 15% of the observed variance in rhizobacterial abundance in a microcosm (Schaedel et al., 2021). Small molecules like malic or oxalic acid, impact not only microbial activity, and are also capable of improving soil fertility too such as via mobilizing less-labile forms of P (Yu et al., 2021), promoting nutrient cycling, soil structure, and overall ecosystem resilience. Legume symbiosis with other soil microbes, such as arbuscular mycorrhizal fungi (AMF), is also highly influenced by specific molecules in root exudates. AMF are natural root symbionts, forming symbiotic relationships with a vast number of plants and helping to increase inorganic phosphorus acquisition (Wang et al., 2022). Such enhancement of root performance is in-turn helpful to nodules as they have high demand for energy (ATP-consuming), and so inorganic phosphate too. Some types of flavonoids are capable to stimulate AMF colonization, such is the case of quercetin (Tian et al., 2021) and isoflavones (daidzein and genistein) (Sugiyama, 2019), both present in root exudates, leading to an overall increase of plant biomass. Phenolic acids (Mandal et al., 2010) and strigolactones (group of sesquiterpenes) can also stimulate germination of spores and hyphal growth (Steinkellner et al., 2007), being another example of chemical-induced shifts in plant-microbial interactions leading to functional changes in the ecosystems.

Recent discoveries regarding soyasaponins, a type of saponin found in the root exudates of legume species, have highlighted their functional potential too. These compounds can disperse over greater distances in the rhizosphere, compared to isoflavones. They can influence bacterial communities by increasing the populations of bacteria that promote plant growth, such as Novosphingobium which induces the breakdown of organic matter in soil leading to the production of nutrients that plants can uptake via their roots (Fujimatsu et al., 2020). Phytochemicals, acting as antioxidants and metal chelators, also have the capacity to regulate microbial activity and soil properties, including the formation of soil organic matter and nutrient cycles (Vukicevich et al., 2016). For example, certain phytochemical-rich legume species, impact the availability of soil minerals by chelating and oxidizing/reducing metals. Isoflavonoids found in alfalfa can dissolve ferric phosphate, making both phosphate and iron accessible to the plant (Hassan and Mathesius, 2012). Tannins, on the other hand, have been shown to counteract the toxic effects of some metals through chelation, thereby positively influencing soil function and plant health (Halvorson et al., 2012). Conversely, alkaloids especially present in lupin crops can potentially have a detrimental environmental impact on plant-associated microbiota due to their mobility in soil environments. They have been recently identified as aquatic micropollutants (Günthardt et al., 2018; Hama et al., 2022).

Overall, the impact of legume phytochemicals on the soil microbiome structure and function can be complex and depend on the specific compounds produced by the legume, as well as the microbial populations present in the soil. Further research should prioritise the study of legume phytochemicals to better comprehend their influence on soil microbial relationships. Consequently, this understanding can enable the selection of select specific phytochemical-rich legumes that selectively promote the growth of beneficial microbial populations and/or soil functions of agroecosystems.

When viewed through the lens of the One Health approach ( Figure 2 ), it is clear how legumes are key drivers of human, animal, and environmental health, emphasising that the health of one component directly impacts the others (Mackenzie and Jeggo, 2019). Nevertheless, for such a complex system to thrive, it has to be resilient enough to adapt long-term human interference (Rendon et al., 2020). Considering that, ‘functional redundancy’ has often been regarded as one of the promoters of ecological resilience, either through communities with redundant species (those that perform similar functions) (Biggs et al., 2020) or even metabolic networks that have evolved to have redundant genes for key metabolic pathways (Sambamoorthy and Raman, 2018). In this context, we propose that legume phytochemicals also exhibit a degree of redundancy, as it was already discussed that various classes of compounds fulfil analogous roles. This redundancy is crucial to the capacity of legumes and their phytochemicals to serve as a pivotal bridge to enable better choices to both environmental and human dietary concerns.

Acting within the intestine, legume phytochemicals modulate gut microbiota structure and function through several cellular signalling pathways, with absorption and metabolism by the gut microbiome being a complex topic and an area of active research (Sudheer et al., 2022). Taking PC or RFOs as examples, some are absorbed in the small intestine and enter the bloodstream, but many others (due to their complex chemical structure) pass to the colon where gut bacteria metabolize them. There, a variety of enzymes can break down the parent compounds into smaller molecules and intermediates that are more easily absorbed into the blood stream ( Figure 2 ). These metabolites can have different biological activities compared to the original compounds, and some may have even stronger health-promoting effects (Santhiravel et al., 2022). In vitro models of the human gastrointestinal tract are key tools to simulate normal conditions, and study how these phytochemicals interact with gut microbes (Qi et al., 2023). Additionally, the utility of such models can be extended when allied with techniques such as high-throughput sequencing to discern the genetic basis of underpinning mechanisms of different phytochemicals. For instance, gut antioxidant function can be associated with both PC and carotenoids (Singh et al., 2017), while lignans and/or flavonoids can interact with hormonal receptors due to their hormone-like and anti-hormone effects (Liu et al., 2022). It is also important to mention that some phytochemicals, like phenolics (Manco et al., 2023), are more present in the hulls (i.e. seed coats of legume grains) compared to kernels (i.e. seeds without coats), which are isolated after dehulling (or decortication). The hulls are a coproduct which is often processed for use as a significant component of ruminant and pet-food diets (Halmemies-Beauchet-Filleau et al., 2018), but could contribute to a better health, considering the biological properties of their rich phytochemical profile.