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Review

The Role of Flavonoids in Nodulation Host-Range Specificity: An Update

by
Cheng-Wu Liu
and
Jeremy D. Murray
*
Department of Cell & Developmental Biology, John Innes Centre, Norwich, Norfolk NR4 7UH, UK
*
Author to whom correspondence should be addressed.
Plants 2016, 5(3), 33; https://doi.org/10.3390/plants5030033
Submission received: 23 June 2016 / Revised: 28 July 2016 / Accepted: 2 August 2016 / Published: 11 August 2016
(This article belongs to the Special Issue Plant Flavonoids)
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Abstract

:
Flavonoids are crucial signaling molecules in the symbiosis between legumes and their nitrogen-fixing symbionts, the rhizobia. The primary function of flavonoids in the interaction is to induce transcription of the genes for biosynthesis of the rhizobial signaling molecules called Nod factors, which are perceived by the plant to allow symbiotic infection of the root. Many legumes produce specific flavonoids that only induce Nod factor production in homologous rhizobia, and therefore act as important determinants of host range. Despite a wealth of evidence on legume flavonoids, relatively few have proven roles in rhizobial infection. Recent studies suggest that production of key “infection” flavonoids is highly localized at infection sites. Furthermore, some of the flavonoids being produced at infection sites are phytoalexins and may have a role in the selection of compatible symbionts during infection. The molecular details of how flavonoid production in plants is regulated during nodulation have not yet been clarified, but nitrogen availability has been shown to play a role.

Graphical Abstract

1. Introduction

Nodulation in legumes evolved as a highly specific interaction between the legumes and gram-negative soil bacteria called rhizobia. The symbiosis is initiated with a chemical signal exchange between host and symbiont. In low nitrogen conditions specific flavonoids are secreted by the host roots, which activate the production of specific lipo-chitooligosaccharide signaling compounds, called Nod factors, by homologous (compatible) rhizobia. Flavonoid perception in the rhizobia is mediated by NodD, a protein that promotes transcription of bacterial nod genes involved in synthesis and secretion of Nod factors [1,2]. The perception of specific Nod factors triggers a signaling cascade in the host that leads, in most legumes, to the formation of the specialized intracellular structures called infection threads. The infection thread acts as a conduit to provide access for the rhizobia to the inner root tissues where they are endocytosed into nodule cells and begin to fix nitrogen [3]. While Nod factor recognition is a key determinant of host range specificity [4,5], differences in flavonoid (NodD-mediated) induction of nod genes plays an equally important role [6]. Loss of the ability to produce or perceive either Nod factors or flavonoids prevents nodulation [7,8,9,10]. Notably, flavonoids also appear to play a central role in the actinorhizal symbiosis: expression of flavonoid biosynthetic genes is increased in the interaction [11], flavonoids can enhance nodulation [12,13], and the repression of flavonoid production reduces nodulation [14]. This points to a universal role for these compounds in nodulation. As actinorhizal nodulation predates the appearance of legumes this suggests either ancient origins for, or convergent evolution of, the role of flavonoids in nodulation. While it is clear the main role for flavonoids in legume nodulation is to induce Nod factor production by rhizobia, they also regulate other rhizobial responses that are important for symbiosis (reviewed in [15,16] including alterations in growth and motility [17,18]. In the broad host rhizobia NGR234 flavonoids can also induce IAA biosynthesis [19]. While these effects may not be strictly required for the symbiosis in artificial lab conditions their contribution in natural environments should not be underestimated as they may impact on competiveness in the field [20]. In addition to their role in nodulation, secreted flavonoids have other roles in the rhizosphere, particularly in P and Fe acquisition [21,22].
Extensive knowledge of the rhizobial genes responsible for variation in Nod factors has been acquired, for instance galegoid legumes recognize Nod factors that feature alpha-beta-unsaturated fatty acids, while within that group Medicago spp. further require that Nod factors be sulphated [23,24,25]. However, even though flavonoids have been studied extensively in legumes, relatively little information is available on which flavonoids play a role in determination of host range. Early work in this area focused on the identification of the key flavonoids being produced and their effects on the rhizobia. The arrival of legume model systems along with new molecular tools offers an opportunity to dissect which flavonoids matter the most in a given interaction and to study when and where they are produced. Research in soybean and M. truncatula have highlighted key flavonoids required for the initiation and progression of infection, referred to herein as infection flavonoids, as well as a potential role for flavonoids as phytoalexins acting to reinforce specificity in nodulation. In contrast, relatively little progress has been made on the regulation of the production of flavonoids during nodulation. A relationship between flavonoid production and the carbon-nitrogen status is evident, and this may be reflected in flavonoid production in nodules.

2. Flavonoids as Determinants of Host Range

2.1. Flavonoids as Infection Signals

Flavonoids are low molecular weight secondary metabolites that are produced in plants. They are based upon a fifteen-carbon skeleton consisting of two benzene rings and are biosynthesized by phenylpropanoid pathway. Plants produce a large array of flavonoids. Rosids in particular have undergone a lineage-specific expansion of the Chalcone synthase (CHS) gene family, which encodes the first committed enzyme of flavonoid biosynthesis, and legumes have had a further expansion of one branch of the CHS gene family [26]. Isoflavonoids are a signature characteristic of legumes [27]. The enzymes involved in isoflavonoid synthesis have been identified. Isoliquiritigenin is produced by a legume-specific enzyme, Chalcone reductase (CHR), acting in combination with CHS (reviewed in [28]). The enzyme Chalcone isomerase (CHI) then coverts chalcones to flavanones. Legumes have evolved a novel isoform of CHI that has a preference for isoliquiritigenin as a substrate, in contrast to non-legume CHIs that prefer liquiritigenin. Further action by Isoflavone synthase (IFS) leads to production of isoflavones (a type of isoflavonoids), such as daidzein or genistein (Figure 1).
The diversity of (iso)flavonoids in legumes appears to be driven in part by the role of these compounds in nodulation. Although legumes produce many flavonoids, only specific subsets have roles in nodulation. To act as nodulation signals flavonoids must be secreted from the roots into the rhizosphere, which includes the root surface and inside infection threads (which are effectively extracellular compartments), where they induce nod gene expression [29,30,31,32,33,34,35,36]. The continued induction of the Nod factor biosynthesis operon throughout the infection process is crucial [37,38]. Consequently, the production and release of flavonoids is central to how host-symbiont specificity is achieved. To illustrate this point we’ll consider the flavone luteolin and the chalcone 4, 4′-dihydroxy-2′-methoxychalcone (methoxychalcone) in the Medicago-Sinorhizobium meliloti symbiosis. Luteolin is not legume-specific and is found in many plant families [39]. Although it was the first flavonoid identified as a nod gene inducer, it can induce nod genes across a diverse array of symbionts, including S. meliloti, Rhizobium galegae, and different subtypes of R. leguminosarum, suggesting a lack of specificity [35,40,41]. The non-specific nod gene-inducing activity of luteolin is further demonstrated by its ability to activate the NodD of Mesorhizobium ciceri, which specifically nodulates chickpea [42]. Furthermore, tests using M. ciceri NodD shows it is not activated by alfalfa, pea, and clover root exudates, suggesting that luteolin is not a key nod gene-inducer in these species. In fact, although luteolin can induce expression of S. meliloti nodulation genes [35] and exogenous application of luteolin can enhance nodulation [43], it has never been detected in Medicago root exudates or in nodules [34]. Luteolin is instead secreted in large quantities from germinating seeds, and roles for luteolin as a rhizobial chemoattractant, as well as in biofilm formation and motility, have been proposed [17,44].
In contrast with luteolin, methoxychalcone meets most of the criteria for a host infection signal. While many flavonoids are produced in Medicago spp., only a few are present in root exudates, and just four are symbiotically induced (Table 1) including methoxychalcone. Methoxychalcone levels are induced by S. meliloti, and it is the strongest nod gene inducer identified in Medicago root exudates having significantly enhanced activity over luteolin [34,45,46]. Methoxychalcone is produced from isoliquiritigenin by the enzyme CHALCONE-O-METHYLTRANSFERASE (ChOMT) and is therefore legume-specific [47,48] (Figure 1). Our recent study has shown that the M. truncatula orthologue, ChOMT1, and three other close homologues (ChOMT2, ChOMT3, and ChOMT4), were induced in root hairs of rhizobially inoculated plants, and two of these are highly expressed in the infection zone of mature nodules [49,50,51]. Interestingly, although soybean has six ChOMTs, none are induced in root hairs during infection by Bradyrhizobium, suggesting that production of methoxychalcone is not a general response to rhizobial infection in legumes [52]. Methoxychalcone was also found in Vicia sativa root exudates upon rhizobial inoculation and was shown to also have nod gene inducing activity with R. leguminosarum bv. viciae, and R. leguminosarum bv. trifolii, suggesting that it may have a role in infection in other Trifolieae [53]. Methoxychalcone has also been reported in two other IRLC clade legumes in non-symbiotic contexts [54,55]. Determination of the relative contribution of methoxychalcone to infection and its importance to host range boundaries awaits further studies.
In the soybean-Bradyrhizobium symbiosis, genistein and daidzein are proven to be crucial infection signals: they both induce nod genes in B. japonicum [56,57], they are present in root exudates, and their production is induced by Bradyrhizobium and by Nod factors [58]. The most critical evidence is that knockdown of IFS greatly reduces the levels of these isoflavonoids and completely blocks nodulation [10]. However, contribution of other related flavonoids cannot be ruled out: genistein is a precursor for prunetin which is symbiotically induced (Table 1; [59]) and is a relatively strong and selective nod gene-inducer in Bradyrhizobium, activating NodD from B. japonicum but not B. elkanii [60]. A shared characteristic of these infection flavonoids is that they are symbiotically induced [58]. It is well recognized that rhizobia significantly change the flavonoid profile of their host [61,62,63]), and many of symbiotically up-regulated flavonoids have nod gene-inducing activity. Furthermore, these changes in flavonoid composition require that the interaction be compatible (i.e., they are not induced by heterologous rhizobia) and are therefore not part of a general defense response to bacteria, but instead are a hallmark of symbiosis [46,62].
Based on this discussion we can define the following key characteristics of infection flavonoids:
  • “strong” inducers of nod genes in homologous rhizobia
  • secreted by roots (i.e., found in root exudate)
  • increased biosynthesis in response to rhizobia or Nod factors
  • required for rhizobial infection (i.e., genetic evidence)
In other legumes many nod gene-inducing flavonoids have been identified (reviewed in [64,65], but only a subset of nod gene-inducers are secreted and fewer still are symbiotically enhanced (Table 1).
The main limitation in identifying infection flavonoids is characterizing their production in the host plants. Genetic evidence implicating specific flavonoids is lacking even in well-established models such as the Lotus japonicus-M. loti symbiosis. This is partly due to limited knowledge of the flavonoids involved in nod gene activation, although some knowledge of exudate components has been obtained from L. pedunculatus [69,70]. In other legumes, where this information is available (Table 1), knowledge of the biosynthetic pathways is lacking and genetic resources are limited.

2.2. Flavonoid Phytoalexins as Determinants of Host Range

Several studies have shown that in addition to nod gene-inducing flavonoids the production of phytoalexin flavonoids with anti-bacterial and/or anti-fungal activity is increased during nodulation [63,67,68,71]. The production of phytoalexins during nodulation may at first seem counter-intuitive, but it is clear these phytoalexins are produced during successful interactions and are not part of a generalized defence response to rhizobia. Furthermore many of these have no nod gene inducing activity [72], and some, like medicarpin, can antagonize nod gene induction [31]. In addition, many nod gene-inducing flavonoids are also phytoalexins. For example, methoxychalcone has potent antibacterial activity against gram-positive bacteria [73] and is induced by the elicitor chitosan in pea [74], and genistein has both antifungal and antibacterial activity [75,76]. Furthermore, the M. truncatula ChOMT1 gene is inducible by pathogens, consistent with a role for methoxychalcone as a phytoalexin (Medicago Gene Expression Atlas; Figure 2). The apparently universal role of flavonoids as phytolexins in plants suggests that, along with their role in determining rhizobial host-range, their role in defense was likely a key driver in the expansion and diversification of these compounds in legumes. One phytoalexin, medicarpin, is induced in S. meliloti-M. truncatula interactions and by fungal pathogens [67,77,78].
Medicarpin is produced by Medicago spp. and other legumes and belongs to a special class of highly diversified isoflavonoid-derived compounds called pterocarpans, including pisatin from pea, and glyceollin from soybean (reviewed in [82,83,84]). Like other isoflavonoids medicarpin is produced through the action of CHR, CHI, and IFS but it additonally requires the action of several other enzymes including VESTITONE REDUCTASE (VR) which catalyses the penultimate step in medicarpin biosynthesis [85,86]. The role of these compounds in the symbiosis has not been clarified, but the finding that the Medicago symbiont S. meliloti, but not Bradyrhizobium japonicum and M. loti, is resistant to medicarpin [87], lead to the suggestion of a role for this compound in selection for homologous rhizobia [67]. In support of this idea, recent gene expression studies of VR in M. truncatula roots revealed increased expression at the sites of rhizobial infection, both in infected root hairs and in the nodule [49,51], suggesting that rhizobia are exposed to medicarpin during infection. Similarly, the soybean symbionts B. japonicum and S. fredii acquire resistance to glyceollin when exposed to genistein and daidzein [88].
The idea of manipulation of the rhizosphere by the host to favour compatible symbionts has been steadily gaining ground. In Rhizobium etli, genes encoding multidrug resistance proteins were identified that conferred resistance to the flavonoids coumarate and naringenin as well as to the pterocarpans phaseollin and phaseollidin; loss of one of these genes led to a 40% reduction of nodulation on Phaseolus vulgaris [89]. Similarly, the loss of a multidrug efflux pump component in B. japonicum caused a strong decrease in symbiotic nitrogen-fixation activity in soybean, but not in the alternative hosts mung bean and cowpea, suggesting rhizobia have acquired adapatations to specific phytoalexins in host rhizospheres [90]. Other types of compounds will likely play similar roles in rhizobial selection. Rhizobium mutants that were susceptible to mimosine, a phytoalexin found in root exudates and nodules of Mimosa and Leucaena spp., had greatly reduced nodule occupancy on L. leucocephala when co-inoculated with the WT strain [91].

2.3. Manipulation of Host Range

As discussed above, the two most crucial factors controlling host range are rhizobial Nod factors and the flavonoids that induce their biosynthesis. Knowledge of flavonoid and Nod factor specificities has brought with it the ability to manipulate host range. In soil populations of rhizobia host range barriers can be overcome by lateral transfer of Symbiosis plasmids, in which encode the flavonoid sensor NodD and the Nod factor biosynthesis enzymes for interactions with a specific host [92]. Numerous efforts have shown that transfer of either the nodD gene, Nod factor biosynthesis genes or both are sufficent to overcome host-range limits [93], even allowing the pathogen Agrobacterium tumefaciens to nodulate some legumes, albeit ineffectively. Perhaps the most impressive effort in this area was by Radutoiu et al. [94], who modified both the symbiont and host to break a host-range barrier. To achieve this, they used L. japonicus compatible symbionts carrying a flavonoid-independent NodD activators to nodulate M. truncatula roots transgenically expressing the L. japonicus Nod factor-receptors. In this case, the flavonoid-independent M. loti was able to initiate infection threads and induce underdeveloped nodules on the root, but the infections were mainly arrested in the epidermis, while the flavonoid-independent R. leguminosarum strain progressed further into to the nodule and then aborted. It was suggested that the difference in infection progression for the two strains could be due to the relative similarity of the R. leguminosarum Nod factor to the S. meliloti Nod factor or to differences in surface exopolysaccharides in the strains. Another possibility is that medicarpin, which is known to be toxic to M. loti [87] and other phytoalexins such as methoxychalcone, played a role. More studies are needed to better understand the relative contributions of phytoalexins in host range and rhizosphere competition.

3. C/N Status May Play a Central Role in the Regulation of Flavonoid Levels in Nodules

While much attention in the nodulation field has been focussed on the role of flavonoids, relatively little is known about how their production is regulated. Bhagwat and Thomas (1982) [95] discovered factors in root exudate that promoted nodulation and that could be supressed by the presence of fixed nitrogen. Later, the role of flavonoids in nodulation was revealed and a later study showed that the production of flavonoids is upregulated by low soil nitrogen, which is concordant with the role of flavonoids in nodulation [96]. This relationship between carbon/nitrogen ratios and phenylpropanoid metabolism appears to be a general phenomenon in plants [97,98,99,100,101]. Higher flavonoid levels in the roots, as discussed above, strongly promotes infection through upregulation of nod genes and other responses in the rhizobia. Conversely, rhizobial nod gene expression is repressed by the presence of ammonium in S. meliloti and B. japonicum [102,103], reviewed in [104]. These two systems appear, therefore, to act together to regulate infection at different nitrogen availabilities, with the level of available nitrogen controlling plant production of flavonoids but also directly regulating nod gene expression in the rhizobia. Fitting with this, the expression of host flavonoid biosynthetic genes and rhizobial nod genes is highest in the apex and lowest in the N-fixation zone of M. truncatula nodules [50]. This increase in flavonoid biosynthesis genes is accompanied by very low nitrate levels in the nodule relative to the root [105], whereas in the nitrogen-fixation zone the expression of flavonoid biosynthetic genes is greatly reduced as is the expression of rhizobial nod genes, both potentially a consequence of the ammonia being produced (Figure 3). Indeed, the sensitivity of the nod operon to ammonia may explain the near absence of infection threads in the nitrogen fixation zone, while in the infection zone Nod factor signalling induces the production of more flavonoids in a positive feedback loop. The situation in nodule primordia, which is heavily colonized with infection threads but devoid of nitrogen-fixing rhizobia, is similar to that in the nodule apex; in these tissues flavonoid production is high to promote infection (Figure 3; [50]). These observations are circumstantial and require further investigation to determine whether localised nitrogen regulation of host flavonoid synthesis and regulation of nod genes by fixed ammonia operate together to define nodule zones. In summary, progress on the regulation of flavonoid production in legumes is limited. In general, the production of flavonoids in plant tissues is stimulated by high C/N ratios, and in legumes low N leads to enhanced secretion of nod gene-inducing flavonoids from roots. As flavonoids are critical for rhizobial infection this is likely one of the key mechanisms by which nutrient availability regulates nodulation. This regulation may also be relevant in nodules, where the production of key infection flavonoids appears to be restricted to differentiating tissues and excluded from the nitrogen fixation zone.

4. Conclusions and Future Prospects

Legumes produce a large array of flavonoids in both shoots and roots, and the control of when and where specific flavonoids are secreted is a primary determinant of rhizobial host range, controlling the onset of Nod factor signaling. The requirement for host-range restrictions in the legume-rhizobia symbiosis has given rise to a great diversity of flavonoids and Nod factors of which only a few systems have been studied in detail. Recent genetic studies in model systems indicate that rhizobial infection processes are likely controlled by a limited number of key nod gene-inducing flavonoids in each legume. These infection flavonoids are produced locally at infection sites and in nodule primordia and in the infection zone of mature indeterminate nodules, while other flavonoids in seed exudates may play supporting roles (Figure 4). Many of these flavonoids also act as phytoalexins which, along with other symbiosis-induced flavonoids, may have a role in rhizosphere selection of compatible rhizobia and may be important determinants of host range in the field. Since legumes are the third largest plant family, we can predict that the matrix of Nod factor-flavonoid combinations will be immense, providing a rich resource for rhizosphere engineering. However, for this potential to be fully realized more knowledge of specific host determinants is required, particularly the identification of infection flavonoids and the enzymes that produce them, and their corresponding rhizobial NodD proteins.

Acknowledgments

This work was supported by the Biotechnology and Biological Sciences Research Council Grants BB/G023832/1 and BB/L010305/1 and funds were made available from the BBSRC through the John Innes Centre to pay for Open Access charges. The authors would like to than Vinod Kumar for comments on the manuscript, and Julie Ellwood for help with formatting.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. The isoflavonoid biosynthesis pathway. PAL (Phenylalanine ammonia-lyase), C4H (Cinnamate 4-hydroxylase), 4CL (4-coumarate CoA-ligase), CHS (Chalcone synthase), CHR (Chalcone reductase), CHI (Chalcone isomerase), IFS (Isoflavone synthase), ChOMT (Chalcone O-methyltransferase). Legume specific steps are indicated in green.
Figure 1. The isoflavonoid biosynthesis pathway. PAL (Phenylalanine ammonia-lyase), C4H (Cinnamate 4-hydroxylase), 4CL (4-coumarate CoA-ligase), CHS (Chalcone synthase), CHR (Chalcone reductase), CHI (Chalcone isomerase), IFS (Isoflavone synthase), ChOMT (Chalcone O-methyltransferase). Legume specific steps are indicated in green.
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Figure 2. ChOMT1 expression in pathogen-inoculated roots of Medicago truncatula. Data are taken from the Medicago Gene Expression Atlas [79]. Original data for Cotton Root Rot (Phymatotrichopsis omnivore) are from Reference [80], and data for Macrophomina phaseolina were described by the authors of [81]. Data for Ralstonia solanacearum has not been described in a publication. hpi = hours post inoculation. Bars are SD.
Figure 2. ChOMT1 expression in pathogen-inoculated roots of Medicago truncatula. Data are taken from the Medicago Gene Expression Atlas [79]. Original data for Cotton Root Rot (Phymatotrichopsis omnivore) are from Reference [80], and data for Macrophomina phaseolina were described by the authors of [81]. Data for Ralstonia solanacearum has not been described in a publication. hpi = hours post inoculation. Bars are SD.
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Figure 3. The association between high C/N ratios and flavonoids in nodulation. Areas undergoing infection by rhizobia are dominated by flavonoid-induced Nod factor (NF) signalling and accumulate carbon within amyloplasts. In the bacteroid-containing nitrogen fixation zone, carbon stores have been depleted, flavonoid-related gene expression is low and infection threads are mostly absent.
Figure 3. The association between high C/N ratios and flavonoids in nodulation. Areas undergoing infection by rhizobia are dominated by flavonoid-induced Nod factor (NF) signalling and accumulate carbon within amyloplasts. In the bacteroid-containing nitrogen fixation zone, carbon stores have been depleted, flavonoid-related gene expression is low and infection threads are mostly absent.
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Figure 4. The production and secretion of flavonoids at different stages of growth and development in Medicago spp. (Top left) Luteolin and other flavonoids are produced in seed coat and are released in the exudate upon imbibition and may play a role in chemoattraction of rhizobia [17,44,45]. (Top right) Flavonoids are produced in the root hair elongation zone and some are secreted into the rhizosphere [31,48,106]. (Bottom left) ChOMT genes are expressed in rhizobially infected root hairs, suggesting that the nod gene-inducer methoxychalcone is produced locally [50,51]. (Bottom right) ChOMT genes are also expressed in the nodule apex/infection zone where infection threads are present, but not in the nitrogen fixation zone [49,50].
Figure 4. The production and secretion of flavonoids at different stages of growth and development in Medicago spp. (Top left) Luteolin and other flavonoids are produced in seed coat and are released in the exudate upon imbibition and may play a role in chemoattraction of rhizobia [17,44,45]. (Top right) Flavonoids are produced in the root hair elongation zone and some are secreted into the rhizosphere [31,48,106]. (Bottom left) ChOMT genes are expressed in rhizobially infected root hairs, suggesting that the nod gene-inducer methoxychalcone is produced locally [50,51]. (Bottom right) ChOMT genes are also expressed in the nodule apex/infection zone where infection threads are present, but not in the nitrogen fixation zone [49,50].
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Table
Table 1. Rhizobia and Nod factor-induced flavonoids.
Table 1. Rhizobia and Nod factor-induced flavonoids.
Host Species(iso)FlavonoidsTissuesReference
Soybeanisoliquiritigenin 1root/ root hair[59]
liquiritigenin 2
apigenin
prunetin
afrormosin
amino-flavonoid
dihydrokaempferol
genkwanin
naringenin 3
biochanin-A 3
daidzeinroot exudates[58]
genistein
coumestrol
Phaseolus vulgarisgenisteinroot exudates[66]
daidzein [63]
coumestrol
isoliquiritigenin
naringenin
liquiritigenin
Medicago sativamethoxychalconeroot exudates[67]
formononetin 3
medicarpin 2
Vicia sativamethoxychalconeroot exudates[46]
isoliquiritigenin
liquiritigenin
hesperitin
naringenin
7,3′-dihydroxy-4′-methoxyflavanone
7,4′-dihydroxy-3′-methoxyflavanone
5,7,4′-trihydroxy-3′-methoxyflavanone
Trifolium subterraneum4′,7-dihydroxyflavoneroot exudates[61]
Pisum sativumpisatinroot exudate[68]
1 bold indicates are nod gene inducers; 2 glycoside also detected 3 only glycoside detected.

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MDPI and ACS Style

Liu, C.-W.; Murray, J.D. The Role of Flavonoids in Nodulation Host-Range Specificity: An Update. Plants 2016, 5, 33. https://doi.org/10.3390/plants5030033

AMA Style

Liu C-W, Murray JD. The Role of Flavonoids in Nodulation Host-Range Specificity: An Update. Plants. 2016; 5(3):33. https://doi.org/10.3390/plants5030033

Chicago/Turabian Style

Liu, Cheng-Wu, and Jeremy D. Murray. 2016. "The Role of Flavonoids in Nodulation Host-Range Specificity: An Update" Plants 5, no. 3: 33. https://doi.org/10.3390/plants5030033

APA Style

Liu, C.-W., & Murray, J. D. (2016). The Role of Flavonoids in Nodulation Host-Range Specificity: An Update. Plants, 5(3), 33. https://doi.org/10.3390/plants5030033

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