Abstract
With only specific exceptions, almost all the symbiotic rhizobia have a set of symbiosis genes that include nodulation- and N2-fixing-related genes. Organisation of the symbiosis genes and their roles in the synthesis of Nod factors (LCOs) and nitrogen fixation are first illustrated and compared. Then the diversity and phylogeny of the nodulation gene nodC are discussed in detail in various rhizobia with narrow or broad host ranges. The relationship between the nodC phylogeny and the rhizobial host range is explored in detail.
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1 The Organisation of Symbiosis-Related Genes in Rhizobial Genomes
1.1 Nodulation-Related Genes
To establish the symbiotic relationship, legumes secrete flavonoid compounds (daidzein, luteolin, naringenin, genistein, apigenin, etc.) that inducing rhizobia to produce the nodulation factors (NFs), which are modified lipochitooligosaccharides (LCOs). In return, the NFs can be perceived by the receptor of the host legumes and stimulate the root hairs to deform. Almost all the symbiotic rhizobia need NFs to trigger nodule initiation in most legumes, except that NFs are not necessarily involved in the Bradyrhizobium-Aeschynomene symbiosis (Giraud et al. 2007).
The basic structure of LCOs consists of two parts: three to five units of N-acetylglucosamine (GlcNAc) and a long-chain (C16 to C20) saturated or unsaturated fatty acid linked to the sugar at the non-reduced end of this oligosaccharide (Fig. 5.1). Disruption of either of the two parts of the LCO will lead to the failure of nodulation on legumes.
There are more than 30 different nod, nol and noe genes involved in the synthesis and secretion of the LCOs (Table 5.1, Figs. 5.2, 5.3, and 5.4). Common nodulation genes (nodABC, nodD, nodIJ) exist in all symbiotic rhizobia except some Bradyrhizobium strains (Giraud et al. 2007). (Iso)flavonoids from legumes diffuse across the membrane of the rhizobia and induce the synthesis of NodD protein to activate transcription of other nodulation genes involved in the production of LCOs and their modification (Figs. 5.3 and 5.4).
The nodABC genes, usually existing in an operon (Fig. 5.2), encode for the proteins required to synthesise the basic structure of the LCO. This is then modified by species-specific enzymes resulting in various substitutions on both the reducing and non-reducing end, including glycosylation, sulphation and methylation (Fig. 5.4) (Long 1996). The substitutions are specific for each host legume and offer a certain level of symbiotic specificity (Long 1996; Lewin et al. 1990). The specific structure of LCOs is known to be essential for recognition by specific host NF receptors (NFRs), which are receptor kinases containing lysine motifs (LysM) (Nelson and Sadowsky 2015). A plant may have one or more different NFRs. For example, the promiscuous legume Sophora flavescens may have distinct NFRs because it can be nodulated by different nodC-specific rhizobia secreting different NFs (Jiao et al. 2015a; Liu et al. 2018a).
The functions of various nodulation genes involved in the synthesis and modification of LCOs are shown in Fig. 5.4 and Table 5.1.
1.2 Nitrogen-Fixing-Related Genes in Rhizobia
Relatively inert atmospheric nitrogen (N2) in air cannot be utilised directly by plants and animals. In nature, only some prokaryotic microorganisms, termed diazotrophs, can convert N2 into the more reactive nitrogen compound ammonia (NH3) through the enzyme nitrogenase (or dinitrogenase), with consumption of ATP and release of hydrogen (H2) (Fig. 5.5a). Ammonia is then delivered to α-ketoglutarate/glutamate to form glutamate/glutamine and is further transmitted to other amino acids and N-containing compounds in N metabolism (Fig. 5.5b).
The nitrogenase complex is composed of two main functional subunits, dinitrogenase reductase (NifH, γ2 homodimeric azoferredoxin, Fe protein) and dinitrogenase (NifD/K, α2β2 heterotetrameric molybdoferredoxin, MoFe) (Hageman and Burris 1978; Kneip et al. 2007). The activity of nitrogenase is positively and negatively regulated by NifA and NifL proteins, respectively. NifA, in conjunction with RpoN (σ54 transcriptional factor), activates the transcription of nitrogen fixation genes, such as the nifHDKE and fixABCX operons (Jimenez-Guerrero et al. 2017). Moreover, FixK also induces the transcription of other nitrogen fixation genes, such as the fixNOQP and fixGHIS operons (Jimenez-Guerrero et al. 2017). At least 15 proteins are involved in the maturation, stability and activity of nitrogenase. Another eight proteins participate in the synthesis of FeMo cofactor (FeMo-co, containing iron and molybdenum used for transporting electron to molecular N2) (Table 5.2). Additionally, electron donor and transport are necessary to provide electron to nitrogenase (Table 5.2).
The organisation of nif and fix genes of Sinorhizobium meliloti and Bradyrhizobium japonicum (now B. diazoefficiens) (Fischer 1994) is shown in Fig. 5.6. These nitrogen fixation genes are organised in distinct clusters whose structure and genomic location are species specific (Fig. 5.6) (Fischer 1994). For a detailed description of the organisation and location, refer to the review paper of Fischer (Fischer 1994).
1.3 Symbiosis-Related Functions: Exopolysaccharides, Secretion Systems and Others
Besides the genes directly related to the nodulation and nitrogen fixation mentioned above, there are many other genes or determinants in rhizobia that are involved in symbiosis (Table 5.3) (Shamseldin 2013; Liu et al. 2018b). Mutation of these genes in different rhizobia will lead to a change of nitrogen fixation efficiency or an alteration in specificity for host plants.
Mutation of genes related to the synthesis of exopolysaccharides (exo) in Sinorhizobium meliloti resulted in ineffective nodules on alfalfa containing no bacteroids (Leigh et al. 1985). MucR1, an ancestral zinc finger regulator, is essential for supporting nitrogen fixation of Sinorhizobium fredii CCBAU 45436 within soybean nodules and regulates the production of exopolysaccharides of this strain under free-living conditions (Jiao et al. 2016).
Different rhizobia use different secretion systems – type III, type IV and type VI – to transport effector proteins into host cells (Nelson and Sadowsky 2015). These secretion systems have an effect on rhizobial host specificity and the nodule number on legumes (Nelson and Sadowsky 2015). Abolition of type III secretion systems (TTSS or T3SS) can affect nodule formation in different ways, ranging from no effect to a reduction or an increase in nodule number (Marie et al. 2001). The proteins secreted through TTSS may induce or suppress plant defence responses and thereby prevent or increase symbiotic efficiency (Marie et al. 2001; Nelson and Sadowsky 2015). A T3SS mutant of Bradyrhizobium elkanii USDA61 could overcome nodulation restriction in a soybean variety carrying the Rj4 allele, implying that the incompatibility is partly mediated by effector-triggered immunity (Faruque et al. 2015).
Mutation of several specific genes (Table 5.3) involved in metabolic pathways, transporters, chemotaxis and mobility in strain B. diazoefficiens USDA 110 can change its host range from soybean to Sophora flavescens, a promiscuous legume (Liu et al. 2018b). In addition, the nitrogen efficiency of these mutants inoculated on soybean decreased to some extent (Liu et al. 2018b).
2 Phylogenetic Diversity of Symbiosis Gene nodC
2.1 Phylogenetic Diversity of the Nodulation Gene nodC
As described in Sect. 5.1 of this chapter, the nodC gene, as well as other common genes, is conserved in all symbiotic rhizobia except some bradyrhizobia associated with Aeschynomene. The presence or not of the common genes is the essential characteristic of symbiotic rhizobia. Besides, phylogenetic positions and genetic diversity of nodC genes in rhizobia can reflect the host specificity and host range to some extent.
2.1.1 Specific Legumes and Rhizobia Bearing Highly Distinct nodC Genes
Some legumes only select specific rhizobia (or symbiotic varieties, abbr. sv.) with highly conserved and distinct nodC gene sequences. Common examples of these kinds of legumes include chickpea (Cicer arietinum), Chinese milk vetch (Astragalus sinicus), Amorpha fruticosa and Trifolium spp.
Four species, first Mesorhizobium ciceri (Nour et al. 1994) and M. mediterraneum (Nour et al. 1995), which were described as Rhizobium before the genus Mesorhizobium was created (Jarvis et al. 1997), and more recently M. muleiense (Zhang et al. 2012) and M. wenxiniae (Zhang et al. 2018a), were isolated from root nodules of chickpea, but certain isolates of several other species, including M. tianshanense, M. amorphae (Rivas et al. 2007) and M. opportunistum (Laranjo et al. 2012), also nodulate chickpea. All these chickpea symbionts have highly similar nodC gene sequences, indicating that a single symbiovar, sv. ciceri, has been transferred among multiple species. Detailed discussion of chickpea mesorhizobia and nodC gene phylogeny can be found in Chap. 7 of this book.
Astragalus sinicus is another highly specific legume. It differs from other nodulating species of this genus in that it is only nodulated by mesorhizobia (M. huakuii, M. qingshengii and M. jarvisii sv. astragali) that have a specific and conserved nodC gene sequence (Zhang et al. 2018b), as seen in the phylogenetic tree (Fig. 5.7). The majority of isolates from root nodules of A. sinicus grown in acidic soils of Xinyang, central China, were classified as M. jarvisii (Zhang et al. 2018b). The nodC genes of these isolates were almost identical to the nodC genes in previously described A. sinicus mesorhizobia in M. huakuii and M. qingshengii (Zhang et al. 2018b) and different from that of the type strain (ATCC 33669T ) of M. jarvisii, which was isolated originally from Lotus corniculatus. Therefore, a novel symbiotic variety M. jarvisii sv. astragali was proposed (Zhang et al. 2018b). The highly conserved nodC genes among these different mesorhizobia provide more evidence for lateral gene transfer in rhizobia and high selection pressure by the host legume.
No other sequences were found to be close to the nodC gene sequence of M. amorphae type strain ACCC 19665T associated with Amorpha fruticosa (Fig. 5.7). No evidence was obtained that this strain ACCC 19665T could form symbioses with any other host plant except for its host plant A. fruticosa, further confirming the specific symbiosis between A. fruticosa and M. amorphae in both China and America (Wang et al. 1999, 2002). Even the promiscuous legume Sophora flavescens could not be nodulated by this specific rhizobial strain ACCC 19665T (Jiao et al. 2015a).
Various Mesorhizobium species were isolated from Caragana spp., shrubby legumes mainly growing in the arid and semi-arid regions of Asia and Eastern Europe. Analyses of the nodC genes of these different Caragana-associated mesorhizobia showed that they had more than 93% sequence similarity (Chen et al. 2008). In addition, the nodC genes of these mesorhizobia showed close phylogenetic relationship with those of other rhizobia isolated from legumes belonging to same tribe Galegeae (Ji et al. 2015). Selection of distinct nodC types of different mesorhizobia by Caragana spp. was also demonstrated previously by Li et al. (Li et al. 2012). For further details on the symbiotic relationship between Caragana and different rhizobia, the reader should refer to Chap. 8 of this book.
Another specific symbiosis with evidence for selection pressure by legumes is the partnership between various mesorhizobia and various endemic species of Sophora growing in New Zealand. All the rhizobia from Sophora growing there belong to Mesorhizobium and bear highly similar nodC (and nifH) gene sequences (Nguyen et al. 2017). This is very different from the very diverse rhizobia of multiple genera isolated from Sophora flavescens grown in different regions in China (Fig. 5.7) (Jiao et al. 2015a). However, the two species, M. cantuariense and M. waimense, isolated from Sophora spp. in New Zealand, had high nodC gene sequence similarities to those of some of the mesorhizobia isolated from China (Fig. 5.7). Therefore, the nodC gene corresponding to Sophora mesorhizobia in New Zealand and China may have a common origin. Detailed discussion of Sophora rhizobia can be found in Chap. 7 of this book.
Other specific rhizobial species/symbiotic variety (sv.) symbioses include Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Sinorhizobium/Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Sinorhizobium/Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii) (Andrews and Andrews 2017). These rhizobial symbiotic varieties possess distinct nodC genes different from other rhizobia (Fig. 5.7), and they do not cross-nodulate with other legumes.
Gene transfers laterally among different genera and species in rhizobia are common. Identical nodC genes were found among different strains of Mesorhizobium septentrionale and Rhizobium mongolense CCBAU 11559, in Sinorhizobium fredii CCBAU 03373 and Mesorhizobium temperatum SDW 018T (Fig. 5.7) (Jiao et al. 2015a). The nodC gene was apparently also transferred into the Aminobacter strain BA135 from Mesorhizobium (Estrella et al. 2009). Gene transfers among different rhizobia are further discussed in Chap. 6 of this book.
2.1.2 Promiscuous Legumes and Highly Diverse nodC-Gene-Bearing Rhizobia
Besides the specific symbioses between specific legumes and certain rhizobial species with distinct nodC genes, mentioned above, there are many non-specific or promiscuous legumes that can be nodulated by various rhizobia bearing different nodC genes. Legumes of this kind include soybean (Glycine max) (Zhang et al. 2011), wild soybean (Glycine soja) (Wu et al. 2011), Sophora flavescens (Jiao et al. 2015a) and Sophora alopecuroides (Zhao et al. 2010), common bean (Phaseolus vulgaris) (Wang et al. 2016; Laguerre et al. 2001), Astragalus spp. (Zhao et al. 2008), Caragana spp. (Lu et al. 2009; Yan et al. 2017), peanut (Arachis hypogaea) (Chen et al. 2016), Centrosema (Ramírez-Bahena et al. 2013), Lotus spp. (Estrella et al. 2009; Lorite et al. 2018; Sullivan et al. 1996) and others.
2.1.2.1 Soybean and Its Rhizobia
Soybean can be nodulated by two genera of rhizobia, Bradyrhizobium and Sinorhizobium (syn. Ensifer) (Zhang et al. 2011; Tian et al. 2012). Phylogeny of the nodC genes of these soybean rhizobia assigned them to three branches: I to III (Fig. 5.8). Branches I and II include several species in the genera Sinorhizobium/Ensifer and Bradyrhizobium, respectively. Different species within each of these two branches (I and II) have identical or almost identical nodC gene sequences. Only Bradyrhizobium elkanii has distinctly different nodC gene sequences, belonging to Branch III, which are not close to the other bradyrhizobia and fast growers in Sinorhizobium/Ensifer (Fig. 5.8).
The identical LCOs secreted by different soybean-nodulating Sinorhizobium spp. (Wang et al. 2018; Bec-Ferte et al. 1994), B. diazoefficiens (formerly B. japonicum) USDA 110 and B. elkanii USDA 61 (Liu et al. 2018b; Sanjuan et al. 1992; D’Haeze and Holsters 2002) may allow these rhizobia to have a common host plant, soybean, despite their distinct nodC gene sequence and phylogenetic position. All the LCOs of soybean rhizobia have a common substituent group (2-O-methyl fucosyl) on the reducing terminal (D’Haeze and Holsters 2002), though the deletion of this residue does not affect nodulation on soybean or on the promiscuous legume Sophora flavescens (Liu et al. 2018b).
2.1.2.2 Sophora and Its Rhizobia
Comparably, the promiscuous legumes S. flavescens and S. alopecuroides can be nodulated by more than five genera of rhizobia (Jiao et al. 2015a; Zhao et al. 2010) (detailed discussion can be found in Chaps. 7 and 8 of this book). Various rhizobia bearing dissimilar nodC gene sequences and originating from different cross-nodulation groups can effectively nodulate S. flavescens (Fig. 5.7) (Jiao et al. 2015a). Mutants of the nodC gene in different representative rhizobial species failed to nodulate either S. flavescens or their usual host plants, demonstrating the indispensability of the nodC gene or the Nod factor in launching root nodule formation (Liu et al. 2018a). Furthermore, abolition of Nod factor-decorative genes did not change nodulation activity, although it did decrease or increase N2-fixing efficiency (Liu et al. 2018a).
Surprisingly, although identical Nod factors were produced by S. fredii CCBAU 45436 and B. diazoefficiens USDA 110 and they had common host range, the latter could not nodulate S. flavescens (Jiao et al. 2015a). Several mutants were selected from a Tn5 library of USDA 110, and they altered the host range from soybean to S. flavescens (Liu et al. 2018a, b). However, these mutated genes were not related directly to the structural genes of Nod factor synthesis but were involved in metabolic pathways, transporters, chemotaxis and mobility (Liu et al. 2018b). These mutants may have lost their immunostimulation of the S. flavescens plant, so that they were allowed to enter the nodule cells and form functional nodules.
2.1.2.3 Common Bean (Phaseolus vulgaris) and Its Rhizobia
Common bean (Phaseolus vulgaris) is another promiscuous legume that can be nodulated mainly by species in genus of Rhizobium, including R. etli (Segovia et al. 1993), R. leguminosarum (García-Fraile et al. 2010; Mulas et al. 2011), R. lusitanum (Valverde et al. 2006), R. gallicum and R. giardinii (Amarger et al. 1997), R. phaseoli (Ramírez-Bahena et al. 2008), R. tropici (Amarger et al. 1994; Martinez-Romero et al. 1991), R. leucaenae (Ribeiro et al. 2012), R. paranaense (Dall’Agnol et al. 2014), R. vallis (Wang et al. 2011) and R. sophoriadicis (Ormeño-Orrillo et al. 2018; Jiao et al. 2015b). Additionally, minor isolates in genera of Agrobacterium (Wang et al. 2016), Bradyrhizobium (Cao et al. 2014), Ensifer (Wang et al. 2016) and non-nodulating Phyllobacterium (Flores-Félix et al. 2012) were reported to be isolated from root nodules of P. vulgaris grown in China, Mexico and Spain.
The phylogenetic pattern of nodC genes of different P. vulgaris-nodulating rhizobia is highly host-specific and mainly consisted of two clusters: I and VI, corresponding to symbiovar (sv.) phaseoli and sv. tropici, respectively (Fig. 5.9). Some strains (Y21, SX1660, SX1597, SX1647 and SX1555) in clusters V and VII had nodC genes highly similar (even identical) to those of soybean-nodulating Bradyrhizobium and Sinorhizobium/Ensifer bacteria (Fig. 5.9), suggesting gene lateral transfers coming different rhizobial species. Three clusters (II, III and IV) were distinct and far from the two clusters I and VI (Fig. 5.9).
In the cluster sv. phaseoli, two species of R. sophorae and R. sophoriradicis isolated from Sophora flavescens had highly similar (and even identical) nodC genes to those strains isolated from P. vulgaris (Fig. 5.9). Cross-nodulation demonstrated that these two species could induce effective nodules on P. vulgaris and their original host plant (Jiao et al. 2015b), further indicating the coevolution of nodC gene in P. vulgaris-rhizobia and the host plant (Aguilar et al. 2004).
The conservation of nodC gene sequence in sv. phaseoli and sv. tropici and the selection pressure from P. vulgaris on their rhizobial nodC genes were supported by the identical nodC sequence possessed by different Rhizobium species distributed around the world (Fig. 5.9).These events suggest that these nod genes in Rhizobium spp. sv. phaseoli and sv. tropici evolved from their respective common ancestors.
2.1.2.4 Other Promiscuous Legumes
The promiscuous legume genera Caragana and Astragalus and their various rhizobia are discussed in Chap. 7 of this book. Though great diversity was observed in the nodulation genes (nodA, nodC, nodD, nodG, nodP) of Caragana-Astragalus-Glycyrrhiza-nodulating rhizobia and most representative strains presented unique nodulation gene types, they all clustered in a large group (Ji et al. 2015; Chen et al. 2008). The type strains for species Mesorhizobium metallidurans, M. amorphae and M. mediterraneum, isolated from Anthyllis, Amorpha and Cicer, respectively, formed three deep branches deviating from the strains isolated from the genera Caragana, Astragalus, Glycyrrhiza and Oxytropis, all belonging to Tribe Galegeae (Ji et al. 2015). This point suggested a consanguineous affiliation of rhizobial nodulation genes in the rhizobia nodulating with the same legume genus or tribe (Li et al. 2012). In addition, effects of geographic isolation on the divergence of the nodulation genes have been observed (Ji et al. 2015).
A comparison of the genome of Rhizobium yanglingense strain CCBAU 01603 with those of Caragana-Astragalus-nodulating Mesorhizobium spp. led to the interesting observation that these rhizobia had evolutionarily conserved nodE, nodO, T1SS and hydrogenase systems, allowing them to have common host ranges (Yan et al. 2017).
Peanut (Arachis hypogaea) is another promiscuous legume that can be nodulated by different rhizobial species, although all the effective peanut rhizobia belong to slow-growing Bradyrhizobium (see Chap. 7). Comparison of nodC (and nodA) sequences also indicated the high diversity of peanut isolates (Santos et al. 2017; Chen et al. 2016). The nodC genes of different B. arachidis strains are not completely identical, and strain CCBAU 33067 is far from the other three strains (Fig. 5.10) (Wang et al. 2013b). Surprisingly, two bradyrhizobial species, B. guangdongense CCBAU 51649 and B. guangxiense CCBAU 53363, which were isolated from peanut grown in different provinces, had completely identical and distinct nodC genes occupying a separate branch in the phylogenetic tree (Fig. 5.10), suggesting the independent origin of their nodC genes. Phylogenetic analyses based on 16S rRNA genes and housekeeping genes of these two peanut bradyrhizobial species confirmed the dissimilarities between B. guangdongense and B. guangxiense, and they differ from other known species (Li et al. 2015).
One strain, CCBAU 23160, isolated from a peanut nodule, had nodC and nifH genes identical to those of the type strain of B. lablabi CCBAU 23086T, suggesting that these two strains may have the same host spectrum (Chang et al. 2011).
Like peanut, Centrosema is also a promiscuous legume nodulated by various Bradyrhizobium species (Ramírez-Bahena et al. 2013). The nodC genes of the strains associated with Centrosema spp. were also divergent among themselves and found in different branches (Fig. 5.10) (Ramírez-Bahena et al. 2013).
From the extensive literature, we see that Lotus rhizobia are dispersed among nearly 20 species in 5 genera (Mesorhizobium, Bradyrhizobium, Rhizobium, Ensifer/Sinorhizobium and Aminobacter) (Lorite et al. 2018). However, the majority of the Lotus tenuis isolates appeared to be in the genus Mesorhizobium, with some in Rhizobium (Estrella et al. 2009). All the mesorhizobia from Lotus tenuis had nodC genes similar to narrow host range strains of Mesorhizobium japonicum MAFF303099T and R7A but far from broad host range strain M. loti NZP2037 (Estrella et al. 2009). Aminobacter aminovorans strain BA135 was first isolated from L. tenuis, but it had a nodC gene sequence identical to those of some Mesorhizobium species, suggesting lateral transfer between the genera (Estrella et al. 2009).
3 Concluding Remarks and Perspectives
The existence of nodulation genes (nodC and others) is an essential feature of almost all symbiotic rhizobia. Specific legumes prefer distinct nodC-bearing rhizobia for their partners. The nod genes are often tightly linked in the genome, and they can be located on transmissible elements such as plasmids in many fast-growing rhizobia or transposon-like elements in Mesorhizobium loti. The sequence and phylogeny of nodC gene is a good molecular marker for the rhizobial host plant range, and this is determined by strong selection by the host plant.
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Wang, E.T., Young, J.P.W. (2019). Symbiosis Genes: Organisation and Diversity. In: Ecology and Evolution of Rhizobia. Springer, Singapore. https://doi.org/10.1007/978-981-32-9555-1_5
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