Next Article in Journal
Identification of CmbHLH Transcription Factor Family and Excavation of CmbHLHs Resistant to Necrotrophic Fungus Alternaria in Chrysanthemum
Next Article in Special Issue
Genomic Insights of Alnus-Infective Frankia Strains Reveal Unique Genetic Features and New Evidence on Their Host-Restricted Lifestyle
Previous Article in Journal
Functional Assessment of a New PBX1 Variant in a 46,XY Fetus with Severe Syndromic Difference of Sexual Development through CRISPR-Cas9 Gene Editing
Previous Article in Special Issue
Comparative Genomics Provides Insights into the Taxonomy of Azoarcus and Reveals Separate Origins of Nif Genes in the Proposed Azoarcus and Aromatoleum Genera
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Genes
Volume 14
Issue 2
10.3390/genes14020274
genes-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Adaptive Evolution of Rhizobial Symbiosis beyond Horizontal Gene Transfer: From Genome Innovation to Regulation Reconstruction

by
Sheng Liu
1,2,
Jian Jiao
1,2 and
Chang-Fu Tian
1,2,*
1
State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural University, Beijing 100193, China
2
MOA Key Laboratory of Soil Microbiology, Rhizobium Research Center, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Genes 2023, 14(2), 274; https://doi.org/10.3390/genes14020274
Submission received: 16 December 2022 / Revised: 17 January 2023 / Accepted: 18 January 2023 / Published: 20 January 2023
(This article belongs to the Special Issue Evolution of Root Nodule Symbioses)
Browse Figures
Versions Notes

Abstract

:
There are ubiquitous variations in symbiotic performance of different rhizobial strains associated with the same legume host in agricultural practices. This is due to polymorphisms of symbiosis genes and/or largely unexplored variations in integration efficiency of symbiotic function. Here, we reviewed cumulative evidence on integration mechanisms of symbiosis genes. Experimental evolution, in concert with reverse genetic studies based on pangenomics, suggests that gain of the same circuit of key symbiosis genes through horizontal gene transfer is necessary but sometimes insufficient for bacteria to establish an effective symbiosis with legumes. An intact genomic background of the recipient may not support the proper expression or functioning of newly acquired key symbiosis genes. Further adaptive evolution, through genome innovation and reconstruction of regulation networks, may confer the recipient of nascent nodulation and nitrogen fixation ability. Other accessory genes, either co-transferred with key symbiosis genes or stochastically transferred, may provide the recipient with additional adaptability in ever-fluctuating host and soil niches. Successful integrations of these accessory genes with the rewired core network, regarding both symbiotic and edaphic fitness, can optimize symbiotic efficiency in various natural and agricultural ecosystems. This progress also sheds light on the development of elite rhizobial inoculants using synthetic biology procedures.

1. Introduction

Rhizobia refer to a polyphyletic group of Gram-negative bacteria that induce nodule formation on roots, or occasionally stems, of leguminous plants, where they reduce N2 into ammonia [1]. Rhizobia live in soils saprophytically and, under suitable conditions, enter into an intracellular symbiotic relationship with compatible plant hosts, which requires a multi-step molecular “dialogue” between symbiotic partners during rhizoplane colonization, infection, nodule organogenesis and senescence [2,3]. This represents a typical facultative lifecycle of microsymbionts [4]. Within the infected legume nodule cells, rhizobia proliferate and then undergo either terminal or non-terminal differentiation into nitrogen-fixing bacteroids, which are surrounded by plant-derived membrane to form the organelle-like symbiosome [5]. The terminal differentiation due to irreversible loss of cell division ability is typically initiated by nodule-specific cysteine-rich (NCR) peptides from host legume species of the Inverted Repeat Lacking Clade (IRLC, e.g., alfalfa and pea) and Aeschynomene [6,7,8,9]. This terminal differentiation phenomenon is however not observed for bacteroids in other legumes, e.g., soybean and common bean [10]. Legume hosts provide carbon and other essential resources for bacteroids to support the energetically expensive but O2-sensitive nitrogen-fixing reaction [2]. To allow respiration of bacteroids but avoid nitrogenase inactivation, free O2 in host cells is modulated by leghemoglobins as low as ~50 nM [11,12,13,14]. These distinct features support the rhizobium–legume symbiotic nitrogen fixation (SNF) as the most efficient biological nitrogen fixation system in nature. About 40 million tons of N are fixed by the rhizobium–legume SNF per year, accounting for about 65% of the total input of biological nitrogen fixation in agricultural systems [15]. Meanwhile, many legume species, e.g., soybean, common bean and alfalfa, are important food and forage crops, globally contributing to the sustainable agriculture.
Rhizobial SNF is an adaptive trait evolved in a subset of free-living soil bacteria. This symbiotic trait is mainly attributable to key nodulation and nitrogen fixation genes [16,17], which are generally clustered as two key gene circuits on symbiosis islands or symbiosis plasmids [18,19]. These key symbiosis genes have been found in more than 200 validly published rhizobium species, belonging to 18 genera of Alpha- and Betaproteobacteria [1], except some Bradyrhizobium strains that can establish symbiosis with certain Aeschynomene species or soybean in nod-independent ways [20,21,22]. The most recent common ancestor of Rhizobiales members did not possess key symbiosis genes [23], and Alpha- and Betaproteobacteria are over-represented in the core root microbiome of terrestrial plants [24,25]. Cumulative evidence based on molecular phylogenies and comparative genomics [23,26,27,28] supports the multiple origin hypothesis for rhizobia: predisposed soil bacteria with different taxonomic affiliations have evolved to rhizobia by obtaining key symbiosis genes repeatedly and independently [16,29].
Despite the polyphyletic diversity pattern of rhizobia, obtaining key symbiosis genes through horizontal gene transfer (HGT) does not guarantee the recipient bacterium an effective symbiotic ability [30,31]. Introducing key symbiosis gene circuits into non-rhizobia, e.g., Agrobacterium tumefaciens, Escherichia coli and Ralstonia solanacearum, confers on these recipients the ability of inducing nodule-like structures on test legumes [30,31], or even morphologically normal and infected nodules after selection in an experimental evolution screen on R. solanacearum derivatives [31]. However, these evolved strains are still not capable of fixing nitrogen [30,31,32,33]. By contrast, clones of nascent nitrogen fixation ability are more likely to evolve, under both field and laboratory conditions, from soil bacteria belonging to typical rhizobial genera, e.g., Mesorhizobium and Sinorhizobium [34,35,36,37,38]. These findings suggest a strong recipient-dependent effect. It is noteworthy that there are also extensive efficiency variations in symbiotic interactions between closely related rhizobia associated with the same legume under both controlled and fluctuating field conditions, which significantly affect the inoculation efficiency of rhizobial inoculants in agriculture practices [39,40]. For example, some indigenous rhizobia with low efficiency of nitrogen fixation show superior local fitness, which challenged the performance of introduced commercial rhizobium inoculants [34,39,41]. An elite rhizobial inoculant needs to fulfil at least the following criteria: (1) survival under fluctuating edaphic conditions; (2) efficient rhizoplane colonization; (3) successful integration of symbiosis genes and compatible symbiotic interactions with hosts (Figure 1). This review aimed to summarize our current understanding of rhizobial adaptive evolution, particularly on genome innovations and network rewiring processes, underlying the successful integration of key symbiosis circuits in diverse bacteria.

2. Genome Innovations after Receiving Key Symbiosis Genes

Although the relative importance of different DNA uptake mechanisms (transduction, transformation and conjugation; Figure 2) in acquiring key symbiosis genes is rarely investigated in rhizobia, genetic diversity of field isolates and experimental evolution studies provide strong evidence for HGT of key symbiosis genes [34,35,36,37,38]. The recipient-dependent integration efficiency of key symbiosis genes is consistent with that the evolution of any trait is an individual innovation constrained by ancestral conserved traits. At the genomic level, adaptive evolution is a process in which heritable variability that arises constantly from the interaction between organisms and the n-dimensional niche is selected and fixed [42,43,44]. According to the infinitesimal model of evolution, adaptation is driven by the accumulation of numerous mutations, and each one has an infinitesimal influence, highlighting the genetic complexity of adaptive traits as quantitative [45]. Moreover, a large number of standing studies also emphasized that specific genes or loci may contribute to adaptation in qualitative ways in the context of adaptive evolution of pangenome [46,47]. Here, we summarize known evolutionary processes shaping genome innovations post receiving key symbiosis genes in model rhizobia (Figure 2).

2.1. Continuous Evolution of Key Symbiosis Genes

The common nodABC genes are responsible for the synthesis of N-acetylglucosamine oligosaccharide backbone of nodulation factors (NFs), which are secreted through NodIJ and determine host specificity; while nifHDK and nifENB are nitrogenase structural and FeMo-co biosynthesis genes, respectively [16,17]. These nod and nif genes, together with their transcriptional activator genes nodD and nifA, can be considered as key symbiosis genes providing nodulation and nitrogen fixation potential, respectively (Figure 1). The nodulation genes play a crucial role in the adaptation of NF-dependent rhizobia to their hosts, as the match between NFs and host NF receptors directly determines whether a symbiotic relationship can be initiated [3]. Homologs of canonical nodABC and nodH, involved in NF synthesis and modification, have been found in certain Frankia strains, which are more deeply rooted than those from rhizobia [48,49,50]. A nodC gene from Frankia Dg1 restores the ability of a nodC mutant of Rhizobium leguminosarum A34 to induce root hair deformation (but not nodulation) [48]. Paralogs of nodIJ, involved in secreting NFs in rhizobia, are only found in Betaproteobacteria but not in those rhizobia belonging to Alphaproteobacteria [51]. Homologs of NodD, sensing host signals and activating the transcription of nodulation genes, are present in all rhizobia including those lacking nodABC [20,52]. Therefore, it seems that the circuit of key nodulation genes had been naturally assembled through multiple events of gene duplication, vertical and horizontal evolution [53].
The extraordinary variety of legume species and hence the NF receptors likely select rhizobia producing compatible NFs out of those secreting NFs varying in the length and modifications of N-acetylglucosamine oligosaccharide backbone [54]. This view has been elegantly proved in a pioneer study where NodA from Sinorhizobium meliloti but not that from Rhizobium tropici can transfer unsaturated C16 fatty acids onto the NF backbone, leading to host specificity [55]. NodC determines the length of NF backbone [56], and variations in nodC among S. meliloti strains determine host specificity with different Medicago species [57]. This and similar evidence supports a rational proposal of rhizobial “symbiovar” that is distinguished by the host range and corresponding variation of key symbiosis genes, e.g., nodA and nodC that have been widely used in rhizobial diversity studies [58,59].
Notably, different cocktails of NFs can be secreted by the same strain under fluctuating conditions, e.g., pH [60], but the underlying mechanisms remain elusive. Three distinct nodA genes are present in two broad-host-range strains R. tropici CIAT 899 and Rhizobium sp. PRF 81 [61]. Rhizobial NodD can specifically sense symbiotic signals out of the cocktail of legume root exudates e.g., flavonoids, and the number of nodD copies varies among rhizobia [62,63]. A NodD from the broad-host-range strain MPIK3030 is sensitive to a broader range of flavonoids than three NodDs of S. meliloti [64]. Functional differentiation between NodD copies in the same rhizobium, e.g., S. meliloti, Sinorhizobium fredii, R. tropici and Bradyrhizobium diazoefficiens, has been demonstrated [65,66]. Interestingly, different nodD combinations out of five copies in R. tropici CIAT 899 are required for nodulation on different hosts [67]. There is evidence showing recognition of cereal root exudates by NodD1 from the broad-host-range S. fredii NGR234 and subsequent induction of nod genes [68]. Ample evidence also demonstrates that different rhizobial species that nodulate the same plant can secrete NFs of different length and structures [54,69], and their nodulation genes, e.g., those from Bradyrhizobium and Sinorhizobium nodulating soybeans, show a genus-dependent evolutionary history [52,70,71]. Moreover, certain rhizobia show a broad-host-range nodulation ability not only due to their NF cocktails [72]. On the other hand, some photosynthetic Bradyrhizobium strains, lacking the canonical nodulation genes nodABC, have evolved an ability to induce nodules on some Aeschynomene species in an NF-independent way [20], while introducing a symbiosis plasmid carrying canonical nodulation genes can block this unique symbiosis [73].
These non-exhaustive examples support a continuous evolution model of the rhizobial nodulation gene circuit in various bacterial recipients, which at least involves gene divergence, gene duplication and/or loss (Figure 2). In contrast to the nodulation gene circuit, key genes (nifHDKENB) for producing nitrogenase and its FeMo-co show a much broader phyletic distribution in both bacteria and archaea. Recent molecular evolution analysis supports a bacteria-first hypothesis for the origin of nitrogen fixation genes [74]. In Proteobacteria including both rhizobia and non-symbiotic diazotrophs, key nitrogen fixation genes are directly activated by NifA [11]. Among rhizobia, the nitrogen fixation gene circuit can be horizontally transferred together with the nodulation gene circuit, as a symbiosis island or within a symbiosis plasmid, under both laboratory and field conditions [35,36]. However, key nitrogen fixation genes that are active in nodules can have close non-symbiotic homologs in the same genome of certain Bradyrhizobium strains or in non-rhizobial strains of the same genus [26,75]. Moreover, there is evidence showing HGT events with the nodulation gene circuit but not nitrogen fixation genes from Azorhizobium caulinodans to other bacteria [37]. Therefore, the evolutionary history of nodulation and nitrogen fixation gene circuits can be decoupled among diverse rhizobia.

2.2. Horizontal Transfer of Genes beyond Key Symbiosis Genes

There is no doubt that HGT of key symbiosis genes plays a dominant role in shaping rhizobial diversity, thus benefiting both bacterial recipients and associated plant hosts [16,17]. Available genomics analyses show that rhizobia have open pangenomes, indicating that HGT of accessory genes is extensive, while key symbiosis genes are only a small part of the accessory genome [52,76,77]. Among closely related rhizobial species/strains, many detectable HGT events involve plasmid-encoded genes [78,79,80]. For example, in an investigation into 196 R. leguminosarum sv. trifolii genomes belonging to a five-species complex, 171 genes including symbiosis genes were shown to have inter-species introgression, with symbiosis genes showing a distinct selection signature [78]. Notably, some introgression genes of the fixNOQPGHIS cluster exhibit multiple genomic locations and can be independent on symbiosis plasmid-associated introgression events [78]. Similarly, another or multiple fixNOQPGHIS copies, not localized on the symbiosis island/plasmid, can be found in many rhizobial genomes [34,81]. This is consistent with the fact that fixNOQP and fixGHIS are required for assembly and function of the cbb3 high-affinity terminal oxidase under both free-living microaerobic and symbiotic conditions [81,82]. On the other hand, these findings also support that fix genes integrated into symbiosis island/plasmid may be an adaptive trait in terms of fast spreading of the symbiotic ability among soil bacteria.
Among genes co-localized with key symbiosis genes of some broad-host-range rhizobia, those encoding type III secretion system (T3SS) and its effector proteins have received considerable attention and investigation. Different effector proteins or natural variation of the same effector can positively, neutrally, or negatively affect symbiotic compatibility depending on host genotypes [83,84,85,86]. A similar scenario fits with the type IV secretion system (T4SS). In certain Mesorhizobium strains lacking T3SS, host range change can be mediated by mutations in vir genes encoding the T4SS components or in genes encoding effector proteins [87]. The T4SS gene clusters are localized on the symbiosis island of Mesorhizobium, and the phylogeny of traG, encoding a substrate receptor of T4SS, is similar to that of key symbiosis genes (nod and nif) [88]. Moreover, there are multiple lines of evidence supporting coordinated transcriptional regulation of T3SS or T4SS genes and nod genes by NodD and legume root exudates [83,87,88,89,90]. The proximity of conditional beneficial genes and key symbiosis genes on symbiosis island/plasmid, and their co-transfer between different bacteria are evolutionarily meaningful, because they contribute to fast spreading of symbiotic functions, particularly when rhizobia are interacting with different legume hosts.
In rhizobia with multipartite genome architecture, the existence of accessory plasmids with conjugative transfer ability makes HGT easier to happen. Genome sequence analyses of 92 reference strains of Rhizobiaceae show that gene acquisition events related to accessory plasmids introduced more genes into the genomes of nitrogen-fixing species, which expanded the metabolic ability of rhizobial species and may facilitate the adaptation to various environmental conditions [91]. In S. meliloti, accessory plasmids are similar in many ways to the symbiosis plasmid, and HGT between these plasmids contributes to the gene content of the symbiosis plasmid and the constantly evolving symbiotic phenotypes [92]. A stress-tolerant alfalfa microsymbiont S. meliloti B401 has a highly similar genomic background with the model strain S. meliloti 1021, but with an additional set of genes encoding the uptake system for betaine and choline on the symbiosis plasmid, which might partially explain its high levels of SNF under both humid and semiarid environments [93]. Among tested Sinorhizobium strains showing different symbiotic performance on certain soybean cultivars, an elite strain has three accessory zinc transporter genes (zip1, zip2 and c06450 localized on the chromid or accessory plasmid) in addition to the conserved chromosomal znuABC (high affinity zinc transporter), which make cumulative contributions to the zinc homeostasis and nodulation compatibility [94].
Genes on accessory plasmids, in some cases, may only be beneficial to rhizobia but harmful to the plant, an evolutionary scenario similar to parasitism. For example, certain Sinorhizobium strains carry the hrrP gene on accessory plasmids, and HrrP degrades the host-derived NCR peptides, providing adaptability to the microsymbionts at the expense of the host fitness [95]. The transfer of certain accessory plasmids between S. meliloti strains enhances competitive nodulation ability of the recipient on alfalfa plants, but with reduced nitrogen fixation ability [96]. These cases suggest the transformation of beneficial rhizobia into a more exploitative way of life mediated by accessory genes on plasmids [95,96].

2.3. Gene Inactivation, Gene Loss and Genome Rearrangement in Symbiosis Plasmid/Islands

As facultative microorganisms, rhizobia face a very complex and fluctuating environment, and undergo a great ecological shift. The relatively large and plastic genome generally support the adaptability; however, some of the pre-existing genes or metabolic pathways may sometimes be harmful when they shift to a new habitat or lifestyle. In this case, loss or inactivation of the corresponding genes under purifying selection pressure can provide them with adaptive advantages. At the stage of host infection, some secreted effector proteins or virulence systems may trigger the immune response of certain hosts, thus affecting the cell entry. For example, T3SS and its effectors have been independently reported to be key factors limiting rhizobial compatibility during adaptive evolution under the selection of new hosts [31,84,85,97]. This can be mediated by transient hypermutability stage before infection due to a mutagenesis imuABC cassette on the symbiosis plasmid [98], and/or by insertion mutation and gene loss mediated by transposable insertion sequences (ISs) that are enriched on the symbiosis plasmid or symbiosis island [84,85,97].
Phyletic distribution analysis shows that imuABC genes are over-represented in rhizobia harboring symbiosis plasmids. The imuABC genes encode error-prone DNA polymerase, the expression of which can lead to high-frequency mutations [98]. In the experimental evolution studies conducted by the Masson-Boivin laboratory, when symbiosis genes were transferred together with the mutagenesis imuABC cassette, the mutation rate of the recipient genome increased and the evolution of soil bacteria to rhizobium accelerated [98]. Exposure to either plant culture medium or Mimosa plants triggered transient hyper-mutagenesis of the recipient bacteria. Adaptive mutations leading to major phenotypic changes were identified: stop mutations of structural T3SS component hrcV led to nodulation [31]; stop mutations in virulence regulatory factor hrpG or mutations in the promoter region or frameshift mutations in its upstream sigma factor prhI and vsrA genes led to primitive infection of nodule cells [32,98]. Missense mutations in the global regulatory factor efpR, or intergenic mutations in the upstream of unknown functional genes [33], or mutations in two different components of the Phc quorum sensing system, phcB or phcQ, lead to massive infection of nodule cells, separately [99]. Following saprophytic-symbiotic lifestyle shift guarantees the mutations beneficial to the plant host being preserved [17]. The imuABC-based transient mutagenesis, together with the following host selection, represent a two-step evolutionary scenario of rhizobial adaptation [100]. This is supported by the fact that both natural and experimental processes result in rapid genetic diversification dominated by purifying selection [100].
Transposable elements (TEs) were considered as the “junk” and “selfish” components of genome, while cumulative evidence suggests that they are important players in the evolution of both eukaryotes and prokaryotes [101]. TEs amplify to very high copy numbers when entering into a new niche, resulting in a large number of variations, making cellular organisms adapt to the new environment quickly [102]. The IS is the most common TE in bacteria. In addition to disrupting the gene by insertion, ISs can also promote gene inversion, deletion, duplication, and fusion of two replicons [103,104]. Most rhizobial genomes are rich in IS elements that are concentrated in packages of symbiosis genes. For example, in S. fredii NGR234, up to 18% of the symbiosis plasmid pNGR234a are mosaic sequences and ISs [105]; ISs are also abundant on the symbiosis plasmids of other Sinorhizobium strains [84,106], and on the 500-kb symbiosis island embedded on the chromosome of symbiotic Mesorhizobium and Bradyrhizobium strains [19,107,108]. By contrast, ISs are rarely present on the nif islands of most sequenced non-symbiotic Bradyrhizobium strains [109], implying a relatively limited evolutionary potential of key nif genes compared to those genes modulating symbiotic compatibility. Indeed, adaptive evolution of symbiotic compatibility due to gene insertion and loss in the T3SS gene cluster mediated by ISs have been observed in the experimental evolutionary studies of Sinorhizobium and Bradyrhizobium strains associated with soybeans [84,85,97]. Gene loss is mediated by homologous recombination of ISs [97], and insertion mutation rates are in line with a niche differentiation model of ISs [110]. In addition, gene duplication within the symbiosis island mediated by homologous recombination between IS copies also exists in nature [97].
The major active ISs, in the adaptive evolution of Sinorhizobium strains, display broader phyletic and replicon distribution than other ISs, and prefer target sequences with AT-rich content, which is a characteristic feature of symbiosis plasmids [84]. Recently, such biased distribution and insertion rates of ISs are experimentally demonstrated by using an intracellular “common garden” approach adapted from conventional ecology [110]. In this genome ecology experiment, conditional lethal sacB gene of low, medium or high GC content was individually inserted into three replicons of a model bacterium S. fredii to trap transposable ISs in the process of adaptive evolution [110]. Xenogeneic sacB of low and medium GC% in the low GC% symbiosis plasmid are preferred by major active ISs, and such preference is dependent on MucR, a conserved xenogeneic silencer in Alphaproteobacteria [111,112]. This is at least partially due to MucR also preferring to target AT-rich DNA sequences of the symbiosis plasmid and possessing a DNA-bridging ability that may facilitate transposition [111,112]. Notably, in addition to other copies, mucR can be found on the symbiosis plasmid or other transferable genomic regions [113]. The processes mentioned above mediated by ISs and MucR, together with the imuABC-dependent hypermutations, may shape the gene content, gene order and genetic variation of the constantly evolving symbiosis gene circuits on symbiosis island/plasmid, contributing to the fast adaptive evolution of rhizobial symbiotic compatibility. Particularly, genome rearrangement in the symbiosis plasmid mediated by ISs may facilitate the assembly of key symbiosis gene circuits with new symbiotic players, which further supports the innovation and fast spreading of symbiotic function to other soil bacteria. These molecular evolutionary mechanisms can also help people better understand, modify and utilize these genome modification tools, so as to promote the domestication or genetic stability of inoculants.

3. Reconstruction of Regulatory Networks

The rhizobium symbiosis involves biological processes including communication with plant host, migration to the rhizosphere, rhizoplane colonization, induction of nodule and infection thread, intracellular host infection, accommodation in the plant cell, morphological differentiation, lifestyle change and cell function specialization [2]. This represents a typical complicated trait that needs not only key symbiosis genes but also a large number of core and lineage-specific functions [16,52,114,115]. Together with scattered genetic evidence, recent advances in high-throughput analyses of rhizobial fitness genes, metabolic and regulation networks during lifestyle adaptations, are providing more insight into the integration mechanisms of symbiotic function within bacterial recipients.

3.1. Recruitment of Indigenous Functions to Support Symbiosis

Like any bacteria-plant interactions, the rhizobium–legume symbiosis is a complex and delicate process, which involves the cooperation of multiple cellular functions. Metabolic modeling of S. meliloti suggests that chromid genes are more actively involved in rhizosphere fitness than in bulk soils, while chromosome has a similar contribution to fitness in two niches [116,117]. A large number of R. leguminosarum genes are differentially expressed in rhizospheres of pea, alfalfa and sugar beet [118]. Some host-specific genes are related to C metabolism, and many are located on the non-symbiosis accessory plasmids [118]. These findings indicate that non-symbiosis genes are extensively involved in rhizosphere fitness. By using the transposon insertion sequencing method, about 600 genes of R. leguminosarum are identified as fitness genes during lifestyle adaptations from rhizosphere to symbiosis with pea plants [115]. Comparative transcriptomics independently demonstrates that hundreds of rhizobial genes are differentially expressed in nodules compared to free-living cells [114,119,120,121,122]. Metabolic modeling suggests global coordination of carbon and nitrogen allocation in bacteroids [123]. The broad-host-range strain S. fredii NGR234 shows considerable differences in transcriptomes of bacteroids in Leucaena leucocephala and Vigna unguiculata [121]. Key nitrogen fixation genes on the symbiosis plasmid of S. fredii strains in Glycine nodules are characterized by high connectivity in both intra- and inter-replicon co-expression analyses [114], which allow further identification of chromosomal core znu and accessory mdt operons involved in host-specific symbiotic adaptation [114]. However, functional characterizations post genome-wide surveys are usually limited [114,115].
Based on scattered genetic and molecular biological evidence, a general picture of extensive recruitment of core and accessory functions, in addition to key nodulation and nitrogen fixation genes, in optimizing symbiotic efficiency has been proposed earlier [16,17]. The list of core and accessory functions contributing to rhizobial fitness, from rhizosphere to rhizoplane to nodules, is ever-increasing (above 900 genes) and usually in a strain–host-dependent manner [52], e.g., motility and chemotaxis [124], surface polysaccharides [125,126,127,128,129], outer membrane vesicles [130], quorum sensing [131,132,133,134,135], T1SS, T3SS, T4SS and T6SS [136,137,138,139,140,141,142], dicarboxylate transport [143], poly-3-hydroxybutyrate [144,145,146], transporters of branched amino acids [147,148,149], uptake of ions (phosphorus [150,151,152], potassium [153,154], molybdenum [155], iron [156,157], sulfur [155], zinc [94] and manganese [158]), nitrate reduction [40], NO modulation [159,160], oxygen limitation responses [40,161,162,163], cell cycle [164,165,166], peptide importers [167,168,169,170,171], regulatory non-coding RNAs (e.g., globally acting trans-small RNA AbcR1/2 and those fragments derived from transfer RNA) [172,173] and carbon–nitrogen metabolism coordination by nitrogen-related phosphotransferase system [153,174,175]. These efforts indicate that the successful integration of key nodulation and nitrogen fixation circuits in various bacterial recipients involves systematic and dynamic coordination with other functions during the establishment of symbiosis.

3.2. Integration of Key Symbiosis Circuits with Recipient Regulation Network

Although all key nitrogen-fixing genes are directly activated by NifA in Proteobacteria [11], a constitutive expression of nitrogenase should be avoided under fluctuating conditions. The nifA gene can be transcriptionally activated by different upstream regulators, e.g., the FixL-FixJ two-component system in S. meliloti [176], the FixL-FixJ-FixK cascade in A. caulinodans [177,178], the redox responsive regulator RegR and its upstream kinases in B. diazoefficiens [162,179,180]. Nitrogenase is O2 sensitive and microaerobic fitness machineries seem to be relatively conserved in test rhizobia. The fixNOQP operon, encoding the cbb3 terminal oxidase, is transcriptionally activated by the FixL-FixJ-FixK cascade in S. meliloti, A. caulinodans and B. diazoefficiens [176,177,181,182,183], and the hFixL-FxkR-FixKf-FnrN cascade in R. etli and R. leguminosarum [163,184]. On the other hand, NifA can activate the transcription of fixABCX, encoding an electron bifurcating complex that provides low-potential reducing equivalents for nitrogenase [185], in S. meliloti, R. etli and R. leguminosarum [186,187,188,189]. Ferredoxin, likely reduced by FixABCX during nitrogen fixation [185], is a reductant of nitrogenase and its gene transcription is also activated by NifA in S. meliloti, B. diazoefficiens and R. etli [190,191]. Available transcriptomic evidence in B. diazoefficiens, S. meliloti and R. etli indicates that NifA may regulate more functional genes, e.g., molybdenum transporter, cytochrome P450 proteins, GroES, GroEL and uptake hydrogenase in a strain-dependent manner [161,189,190]. Notably, stringent sets of NifA regulon in these three rhizobia (19–67 genes) are on the symbiosis plasmid or symbiosis island with rare exceptions [161,189,190]. These findings imply that the integration of the key nitrogen fixation gene circuit in terms of transcriptional activation is strain-dependent, and the transcriptional regulation network of bacterial recipients seems to be limitedly subject to direct interference by NifA.
An efficient nitrogen fixation process of rhizobia is structurally ensured by nodule organogenesis that is initiated by specific recognition of host symbiotic signals by NodD in most rhizobia. The divergence of NodD and multiple NodD copies facilitate rhizobia efficiently establishing symbiosis under fluctuating conditions and/or exploring more host plants [64,67,68,192,193]. Available studies support a model where a primary NodD binds DNA in the absence of host symbiotic signals while signal–NodD binding enhances DNA bending that allows transcription [194,195]. NodD autoregulates its own transcription in R. leguminosarum bv. trifolii and R. leguminosarum bv. viciae [196,197]. When two or more NodDs are encoded within a genome, these NodDs usually act as a coordination module in a rhizobium- and condition-dependent way. For example, a second NodD copy in some R. leguminosarum bv. trifolii strains enhances nodule colonization competitiveness [198]. In S. meliloti, NodD1Sm and NodD2Sm respond to plant signals and the overexpressed NodD3Sm can function without flavonoids [62,199]. Among five NodD copies of R. tropici CIAT899, nodD2Rt expression is induced by osmotic stress, and the engineered overexpression of NodD2Rt alone is sufficient to replace the other NodD copies [200]. Mesorhizobium loti R7A has two NodD1Ml and NodD2Ml, showing a degree of functional redundancy [201]. More detailed investigation demonstrates that NodD1Ml mainly function in infection threads while NodD2Ml primarily acts in the rhizosphere and within nodules [202]. This observed division of labor is likely due to their divergence at the signal binding cleft [202]. Noteworthy, NodD2Ml activity is negatively affected by NodD1Ml at the pre-infection stage [202]. Two NodD copies are also found in other rhizobia, e.g., S. fredii and B. diazoefficiens, where NodD2 can negatively regulate the transcription of nodD1 [193,203,204]. The nodD2Sf mutant shows impaired nodulation on soybean but improved compatibility with Lotus species [205]. Collectively, these findings suggest a working model where rhizobial NodD and its regulon may be divergently selected in at least two dimensions: 1) from rhizosphere to rhizoplane to infection threads to nodules; 2) different host plants.
Various variables in these niches may interact with the key symbiotic interaction signaling pathway/network. Indeed, NFs are required for the biofilm establishment [206,207], which generally enhances bacterial resilience to various stress factors [208]. The production of exopolysaccharide (EPS), a common component of biofilm matrix, is negatively regulated by NodD in S. fredii [65,209] while positively regulated by the NodD3-SyrM-SyrA regulatory module in S. meliloti [210]. This is in line with the fact that EPS is an important symbiotic signal for the host infection of S. meliloti but dispensable in S. fredii symbiosis with test legumes [211,212]. In the presence of symbiotic signal daidzein, S. fredii NGR234 produces the phytohormone indole-3-acetic acid (IAA) in a NodD-dependent manner, and overexpression of NodD2Sf enhances the transcription of IAA synthesis genes and IAA production [213]. The positive regulation of IAA production by NodD is also found in R. tropici CIAT 899 [192]. There is evidence showing that flavonoids induce an NodD-dependent expression of traI that is responsible for the synthesis of short-chain quorum-sensing 3-oxo-C8-HSL in S. fredii [207]. Independent studies also reveal that the transcription of T3SS and effector coding genes depends on the positive regulator TtsI, while the expression of ttsI can be activated by NodD and plant flavonoids [214]. In NodD3Sm over-expressing S. meliloti, more than 200 genes are differentially expressed including upregulated EPS biosynthesis, and downregulated motility and chemotaxis functions [215]. Among those upregulated genes (above 70 genes), 69% are located on the chromosome and chromid [215]. Although a systematic survey of direct targets of NodD is not available yet, these examples suggest that NodDs have been evolving to differentially modulate other non-symbiosis functions to improve fitness from rhizosphere to rhizoplane to infection in a strain–host-dependent manner.
In addition to NodD, lineage-specific parts regulating nod genes have been identified in a few model rhizobia, e.g., the two-component system NodV-NodW, NwsB and NolA in B. diazoefficiens [204], SyrM, a NodD homolog, in Sinorhizobium [210,216,217], NolR homologs in Sinorhizobium and Rhizobium [218,219,220,221,222]. NodV-NodW positively regulates nodulation genes and is essential for symbiosis with mung bean, cowpea and Siratro, but only marginally contributes to nodulation on soybean [223]. NwsB, a homolog of NodW, is required for both induction and the population density-dependent repression of nodulation genes [224]. NolA induces nodD2Bd and consequently represses the transcription of nodulation genes [225]. SyrMSm activates nodD3Sm transcription and NodD3Sm induces syrMSm, forming a self-amplifying circuit in S. meliloti [210]. NodD1Sf induces the transcription of SyrMSf that in turn induces NodD2Sf that represses nodulation genes in S. fredii [216]. Chromosomal NolR directly targets nodD1Sm, nodD2Sm and nodABCSm operons in S. meliloti [220,226,227] and downregulates nodulation and T3SS genes in S. fredii [222].
MucR/RosR/Ros/MI (hereafter MucR), a conserved zinc-finger regulator in Alphaproteobacteria, enhances the induction of key nodulation genes by the host signal luteolin in S. meliloti [228]. The disruption of mucR leads to delayed nodule development in the S. meliloti-alfalfa pair [228], reduced nodulation competitiveness in R. etli (common bean) [229], impaired nodulation and nitrogen fixation in R. leguminosarum bv. trifolii (clover) [230] and deficient nitrogen fixation in broad-host-range S. fredii strains (e.g., increased nodule number on soybean while decreased nodule number on Lotus burttii) [231,232]. Available transcriptomic analyses independently show that MucR is a pleiotropic regulator, e.g., in R. leguminosarum bv. trifolii, S. meliloti, S. fredii and other members of Alphaproteobacteria [113,228,231,232,233,234] (Figure 3). MucR autoregulates its transcription and recent ChIP-seq analysis further revealed more than 1350 direct target genes of MucR in the multipartite genome of S. fredii [111], among which a considerable number of known circuits were identified, e.g., NodD2Sf [193,203], TtsI, T3SS and its effector NopP [84], SyrB (negative regulator for SyrM in S. meliloti) [235], pilus assembly (Cpa), motility (Fla/Fli/Mot/Flg) and chemotaxis (Che/Mcp) [124], diguanylate cyclases [236], general stress response (RpoE5 and CspA8) [237], surface polysaccharides (ExoY and Uxs1) [238,239], carbon–nitrogen metabolism coordination (PtsN3) [153,174], nitric oxide reduction (Nor) [40], and uptake of potassium (Kdp) [153,154], iron (RirA) [156] and phosphorus (PhoUB) [150]. It should be noted that MucR rarely activates its target genes and prefers to bind AT-rich DNA (periodic repeats of “Ts”) that represents a characteristic feature of the symbiosis plasmid, genomic islands and xenogeneic DNA [111]. More molecular biology evidence shows that MucR shares convergently evolved features of xenogeneic silencers with H-NS, Lsr2, MvaT and Rok from either Gram-positive or Gram-negative bacteria [112], i.e., oligomerization mediated by N-terminal domain and forming DNA-protein-DNA bridging complex. The importance of these convergent functions in integrating symbiosis/pathogenesis functions is demonstrated by the H-NS from E. coli being interchangeable with MucR from S. fredii in the hemolysis activity assay and symbiotic performance [112]. Indeed, H-NS and other functional H-NS/MucR or Lsr2/MucR chimeric proteins, show similar ChIP-seq profiles in the multipartite genome of S. fredii and share 286 target genes including those encoding NodD2Sf, TtsI, T3SS, NopP, RirA, ExoY, Uxs1, TraI, TraR and VisN [112]. This evidence highlights that the convergent xenogeneic silencer MucR predisposes Alphaproteobacteria to integrate AT-rich symbiosis genes.

4. Conclusions and Perspectives

Rhizobia become sustained in the symbiosis with legume plants due to mutualism, and symbiosis gene circuits become retained in a polyphyletic group of more than 200 bacterial species by conferring symbiotic abilities (Figure 1). This has been proposed as a kind of symbiosis within symbiosis [17]. A similar scenario can be applied to pathogenesis and other transferable or synthesized gene circuits. From this point of view, the process of establishing symbiosis with diverse legumes is just one of the alternative options for soil bacteria. As discussed above, the integration of nod/nif gene circuits, involving genome innovations and regulation reconstruction (Figure 2 and Figure 3), is not orthogonal in various recipients, which is consistent with observed rhizobial variations in symbiotic performance. Successful integrations of these key symbiosis circuits in diverse recipients should recruit both “global” and “local” regulatory modules, which constitute a regulatory network that is both physiologically and evolutionarily dynamic responding to ever fluctuating niche dimensions (Figure 2 and Figure 3), e.g., conditions of pH and osmolarity, and resources of oxygen, carbon, nitrogen, phosphorus, iron, zinc, potassium, molybdenum, sulfur and manganese. Moreover, the dynamic growth status and evolution of host plants and other surrounding organisms can reconstruct these niche dimensions, in addition to directly exerting biotic influence on rhizobial fitness in saprophytic and symbiotic life cycles. Therefore, an ever-changing realized niche shapes the adaptive evolution of polyphyletic rhizobia after receiving key symbiosis genes.
It is emerging that convergent xenogeneic silencers, e.g., MucR conserved in Alphaproteobacteria, may represent one of the most important global regulators in integrating conditional beneficial foreign circuits, including key symbiosis genes [112,113] (Figure 3). MucR mainly downregulates its AT-rich target genes across conservation levels [111] and facilitates insertion mutations in AT-rich conditional deleterious genes by ISs [110]. These silencing mechanisms are crucial for managing adaptive pangenome while maintaining metabolic efficiency. However, we know little about putative anti-silencing mechanisms underlying various adaptive regulons of MucR in different niches, from bulk soils to rhizosphere to rhizoplane to nodules (Figure 3). Moreover, most lineage-specific local regulatory modules have not been systematically investigated on a genome-wide scale using molecular biology techniques (Figure 3), besides available correlation transcriptomic analyses. Apparently, systems biology should be more effectively recruited by scientists to facilitate completing a whole picture of rhizobial adaptive evolution involving ever-rewiring regulation networks. This may support further improvement of rhizobial symbiosis in terms of robustness and efficiency through synthetic biology, which involves rational design and systematic optimization of key symbiosis circuits and their integration efficiency within polyphyletic rhizobia.

Author Contributions

C.-F.T., S.L. and J.J. conceived this work; S.L. and C.-F.T. prepared the manuscript; C.-F.T. reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China, grant number 2022YFA0912100; National Natural Science Foundation of China, grant numbers 32070078 and 31900006; and the 2115 Talent Development Program of China Agricultural University to C.F.T.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data sharing not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

nodnodulation
nifnitrogen fixation
NFRnodulation factor receptor
NCRnodule-specific cysteine-rich
IRLCinverted repeat lacking clade
SNFsymbiotic nitrogen fixation
HGThorizontal gene transfer
NFnodulation factor
T1SStype I secretion system
T3SStype III secretion system
T4SStype IV secretion system
T6SStype VI secretion system
NOnitric oxide
ISinsertion sequence
TEtransposable element
EPSexopolysaccharide
APSarabinose-containing polysaccharide
IAAindole-3-acetic acid
ChIP-seqchromatin immunoprecipitation sequencing
SfSinorhizobium fredii
SmSinorhizobium meliloti
RtRhizobium tropici
MlMesorhizobium loti
BdBradyrhizobium diazoefficiens

References

  1. de Lajudie, P.M.; Andrews, M.; Ardley, J.; Eardly, B.; Jumas-bilak, E.; Kuzmanovic, N.; Lassalle, F.; Lindström, K.; Mhamdi, R.; Martínez-Romero, E.; et al. Minimal Standards for the Description of New Genera and Species of Rhizobia and Agrobacteria. Int. J. Syst. Evol. Microbiol. 2019, 69, 1852–1863. [Google Scholar] [CrossRef]
  2. Poole, P.; Ramachandran, V.; Terpolilli, J. Rhizobia: From Saprophytes to Endosymbionts. Nat. Rev. Microbiol. 2018, 16, 291–303. [Google Scholar] [CrossRef]
  3. Roy, S.; Liu, W.; Nandety, R.S.; Crook, A.; Mysore, K.S.; Pislariu, C.I.; Frugoli, J.; Dickstein, R.; Udvardi, M.K. Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation. Plant Cell 2020, 32, 15–41. [Google Scholar] [CrossRef] [Green Version]
  4. Bordenstein, S.R.; Reznikoff, W.S. Mobile DNA in Obligate Intracellular Bacteria. Nat. Rev. Microbiol. 2005, 3, 688–699. [Google Scholar] [CrossRef]
  5. Coba de la Peña, T.; Fedorova, E.; Pueyo, J.J.; Mercedes Lucas, M. The Symbiosome: Legume and Rhizobia Co-Evolution toward a Nitrogen-Fixing Organelle? Front. Plant Sci. 2018, 8, 2229. [Google Scholar] [CrossRef] [Green Version]
  6. Mergaert, P.; Uchiumi, T.; Alunni, B.; Evanno, G.; Cheron, A.; Catrice, O.; Mausset, A.-E.E.; Barloy-Hubler, F.; Galibert, F.; Kondorosi, A.; et al. Eukaryotic Control on Bacterial Cell Cycle and Differentiation in the Rhizobium-Legume Symbiosis. Proc. Natl. Acad. Sci. USA 2006, 103, 5230–5235. [Google Scholar] [CrossRef] [Green Version]
  7. Van de Velde, W.; Zehirov, G.; Szatmari, A.; Debreczeny, M.; Ishihara, H.; Kevei, Z.; Farkas, A.; Mikulass, K.; Nagy, A.; Tiricz, H.; et al. Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis. Science 2010, 327, 1122–1126. [Google Scholar] [CrossRef]
  8. Montiel, J.; Downie, J.A.; Farkas, A.; Bihari, P.; Herczeg, R.; Bálint, B.; Mergaert, P.; Kereszt, A.; Kondorosi, É. Morphotype of Bacteroids in Different Legumes Correlates with the Number and Type of Symbiotic NCR Peptides. Proc. Natl. Acad. Sci. USA 2017, 114, 5041–5046. [Google Scholar] [CrossRef] [Green Version]
  9. Czernic, P.; Gully, D.; Cartieaux, F.; Moulin, L.; Guefrachi, I.; Patrel, D.; Pierre, O.; Fardoux, J.; Chaintreuil, C.; Nguyen, P.; et al. Convergent Evolution of Endosymbiont Differentiation in Dalbergioid and Inverted Repeat-Lacking Clade Legumes Mediated by Nodule-Specific Cysteine-Rich Peptides. Plant Physiol. 2015, 169, 1254–1265. [Google Scholar] [CrossRef] [Green Version]
  10. Oono, R.; Schmitt, I.; Sprent, J.I.; Denison, R.F. Multiple Evolutionary Origins of Legume Traits Leading to Extreme Rhizobial Differentiation. New Phytol. 2010, 187, 508–520. [Google Scholar] [CrossRef]
  11. Dixon, R.; Kahn, D. Genetic Regulation of Biological Nitrogen Fixation. Nat. Rev. Microbiol. 2004, 2, 621–631. [Google Scholar] [CrossRef] [PubMed]
  12. Becana, M.; Klucas, R.V. Oxidation and Reduction of Leghemoglobin in Root Nodules of Leguminous Plants. Plant Physiol. 1992, 98, 1217–1221. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Ott, T.; van Dongen, J.T.; Günther, C.; Krusell, L.; Desbrosses, G.; Vigeolas, H.; Bock, V.; Czechowski, T.; Geigenberger, P.; Udvardi, M.K. Symbiotic Leghemoglobins are Crucial for Nitrogen Fixation in Legume Root Nodules but not for General Plant Growth and Development. Curr. Biol. 2005, 15, 531–535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Wang, L.; Rubio, M.C.; Xin, X.; Zhang, B.; Fan, Q.; Wang, Q.; Ning, G.; Becana, M.; Duanmu, D. CRISPR/Cas9 Knockout of Leghemoglobin Genes in Lotus Japonicus Uncovers Their Synergistic Roles in Symbiotic Nitrogen Fixation. New Phytol. 2019, 224, 818–832. [Google Scholar] [CrossRef]
  15. Herridge, D.F.; Peoples, M.B.; Boddey, R.M. Global Inputs of Biological Nitrogen Fixation in Agricultural Systems. Plant Soil 2008, 311, 1–18. [Google Scholar] [CrossRef]
  16. Masson-Boivin, C.; Giraud, E.; Perret, X.; Batut, J. Establishing Nitrogen-Fixing Symbiosis with Legumes: How Many Rhizobium Recipes? Trends Microbiol. 2009, 17, 458–466. [Google Scholar] [CrossRef]
  17. Remigi, P.; Zhu, J.; Young, J.P.W.; Masson-Boivin, C. Symbiosis within Symbiosis: Evolving Nitrogen-Fixing Legume Symbionts. Trends Microbiol. 2016, 24, 63–75. [Google Scholar] [CrossRef]
  18. Galibert, F.; Finan, T.M.; Long, S.R.; Puhler, A.; Abola, P.; Ampe, F.; Barloy-Hubler, F.; Barnett, M.J.; Becker, A.; Boistard, P.; et al. The Composite Genome of the Legume Symbiont Sinorhizobium meliloti. Science 2001, 293, 668–672. [Google Scholar] [CrossRef] [Green Version]
  19. Kaneko, T.; Nakamura, Y.; Sato, S.; Minamisawa, K.; Uchiumi, T.; Sasamoto, S.; Watanabe, A.; Idesawa, K.; Iriguchi, M.; Kawashima, K.; et al. Complete Genomic Sequence of Nitrogen-Fixing Symbiotic Bacterium Bradyrhizobium japonicum USDA110. DNA Res. 2002, 9, 189–197. [Google Scholar] [CrossRef]
  20. Giraud, E.; Moulin, L.; Vallenet, D.; Barbe, V.; Cytryn, E.; Avarre, J.C.; Jaubert, M.; Simon, D.; Cartieaux, F.; Prin, Y.; et al. Legumes Symbioses: Absence of Nod Genes in Photosynthetic Bradyrhizobia. Science 2007, 316, 1307–1312. [Google Scholar] [CrossRef]
  21. Okazaki, S.; Tittabutr, P.; Teulet, A.; Thouin, J.; Fardoux, J.; Chaintreuil, C.; Gully, D.; Arrighi, J.-F.; Furuta, N. Rhizobium—Legume Symbiosis in the Absence of Nod Factors: Two Possible Scenarios with or without the T3SS. ISME J. 2015, 10, 64–67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Okazaki, S.; Kaneko, T.; Sato, S.; Saeki, K. Hijacking of Leguminous Nodulation Signaling by the Rhizobial Type III Secretion System. Proc. Natl. Acad. Sci. USA 2013, 110, 17131–17136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Garrido-Oter, R.; Nakano, R.T.; Dombrowski, N.; Ma, K.W.; McHardy, A.C.; Schulze-Lefert, P. Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia. Cell Host Microbe 2018, 24, 155–167. [Google Scholar] [CrossRef] [Green Version]
  24. Banerjee, S.; Schlaeppi, K.; van der Heijden, M.G.A. Keystone Taxa as Drivers of Microbiome Structure and Functioning. Nat. Rev. Microbiol. 2018, 16, 567–576. [Google Scholar] [CrossRef]
  25. Yeoh, Y.K.; Dennis, P.G.; Paungfoo-Lonhienne, C.; Weber, L.; Brackin, R.; Ragan, M.A.; Schmidt, S.; Hugenholtz, P. Evolutionary Conservation of a Core Root Microbiome across Plant Phyla along a Tropical Soil Chronosequence. Nat. Commun. 2017, 8, 215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Bontemps, C.; Elliott, G.N.; Simon, M.F.; Dos Reis Junior, F.B.; Gross, E.; Lawton, R.C.; Neto, N.E.; de Fatima Loureiro, M.; De Faria, S.M.; Sprent, J.I.; et al. Burkholderia Species Are Ancient Symbionts of Legumes. Mol. Ecol. 2010, 19, 44–52. [Google Scholar] [CrossRef] [PubMed]
  27. Sachs, J.L.; Skophammer, R.G.; Regus, J.U. Evolutionary Transitions in Bacterial Symbiosis. Proc. Natl. Acad. Sci. USA 2011, 108, 10800–10807. [Google Scholar] [CrossRef] [Green Version]
  28. Wang, S.; Meade, A.; Lam, H.-M.; Luo, H. Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in Rhizobiales. mSystems 2020, 5, e00438-20. [Google Scholar] [CrossRef]
  29. Martinez-Romero, E. Coevolution in Rhizobium-Legume Symbiosis? DNA Cell Biol. 2009, 28, 361–370. [Google Scholar] [CrossRef]
  30. Hirsch, A.M.; Wilson, K.J.; Jones, J.D.G. Rhizobium meliloti Nodulation Genes Allow Agrobacterium tumefaciens and Escherichia coli to Form Pseudonodules on Alfalfa. J. Bacteriol. 1984, 158, 1133–1143. [Google Scholar] [CrossRef]
  31. Marchetti, M.; Capela, D.; Glew, M.; Cruveiller, S.; Chane-Woon-Ming, B.; Gris, C.; Timmers, T.; Poinsot, V.; Gilbert, L.B.; Heeb, P.; et al. Experimental Evolution of a Plant Pathogen into a Legume Symbiont. PLoS Biol. 2010, 8, e1000280. [Google Scholar] [CrossRef] [PubMed]
  32. Guan, S.H.; Gris, C.; Cruveiller, S.; Pouzet, C.; Tasse, L.; Leru, A.; Maillard, A.; Médigue, C.; Batut, J.; Masson-Boivin, C.; et al. Experimental Evolution of Nodule Intracellular Infection in Legume Symbionts. ISME J. 2013, 7, 1367–1377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Capela, D.; Marchetti, M.; Clérissi, C.; Perrier, A.; Guetta, D.; Gris, C.; Valls, M.; Jauneau, A.; Cruveiller, S.; Rocha, E.P.C.; et al. Recruitment of a Lineage-Specific Virulence Regulatory Pathway Promotes Intracellular Infection by a Plant Pathogen Experimentally Evolved into a Legume Symbiont. Mol. Biol. Evol. 2017, 34, 2503–2521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Hill, Y.; Colombi, E.; Bonello, E.; Haskett, T.; Ramsay, J.; O’Hara, G.; Terpolilli, J. Evolution of Diverse Effective N2-Fixing Microsymbionts of Cicer arietinum Following Horizontal Transfer of the Mesorhizobium ciceri CC1192 Symbiosis Integrative and Conjugative Element. Appl. Environ. Microbiol. 2021, 87, e02558-20. [Google Scholar] [CrossRef]
  35. Sullivan, J.T.; Patrick, H.N.; Lowther, W.L.; Scott, D.B.; Ronson, C.W. Nodulating Strains of Rhizobium loti Arise through Chromosomal Symbiotic Gene Transfer in the Environment. Proc. Natl. Acad. Sci. USA 1995, 92, 8985–8989. [Google Scholar] [CrossRef] [Green Version]
  36. Sullivan, J.T.; Ronson, C.W. Evolution of Rhizobia by Acquisition of a 500-kb Symbiosis Island That Integrates into a Phe-tRNA Gene. Proc. Natl. Acad. Sci. USA 1998, 95, 5145–5149. [Google Scholar] [CrossRef] [Green Version]
  37. Ling, J.; Wang, H.; Wu, P.; Li, T.; Tang, Y.; Naseer, N.; Zheng, H.; Masson-boivin, C.; Zhong, Z.; Zhu, J. Plant Nodulation Inducers Enhance Horizontal Gene Transfer of Azorhizobium caulinodans Symbiosis Island. Proc. Natl. Acad. Sci. USA 2016, 113, 13875–13880. [Google Scholar] [CrossRef] [Green Version]
  38. Barcellos, F.G.; Menna, P.; Batista, J.S.D.; Hungria, M.; da Silva Batista, J.S. Evidence of Horizontal Transfer of Symbiotic Genes from a Bradyrhizobium japonicum Inoculant Strain to Indigenous Diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah Soil. Appl. Environ. Microbiol. 2007, 73, 2635–2643. [Google Scholar] [CrossRef] [Green Version]
  39. Brockwell, J.; Bottomley, P.J. Recent Advances in Inoculant Technology and Prospects for the Future. Soil Biol. Biochem. 1995, 27, 683–697. [Google Scholar] [CrossRef]
  40. Liu, L.X.; Li, Q.Q.; Zhang, Y.Z.; Hu, Y.; Jiao, J.; Guo, H.J.; Zhang, X.X.; Zhang, B.; Chen, W.X.; Tian, C.F. The Nitrate-Reduction Gene Cluster Components Exert Lineage-Dependent Contributions to Optimization of Sinorhizobium Symbiosis with Soybeans. Environ. Microbiol. 2017, 19, 4926–4938. [Google Scholar] [CrossRef]
  41. Peoples, M.B.; Brockwell, J.; Hunt, J.R.; Swan, A.D.; Watson, L.; Hayes, R.C.; Li, G.D.; Hackney, B.; Nuttall, J.G.; Davies, S.L.; et al. Factors Affecting the Potential Contributions of N2 Fixation by Legumes in Australian Pasture Systems. Crop Pasture Sci. 2012, 63, 759. [Google Scholar] [CrossRef]
  42. Svensson, E.I.; Berger, D. The Role of Mutation Bias in Adaptive Evolution. Trends Ecol. Evol. 2019, 34, 422–434. [Google Scholar] [CrossRef] [PubMed]
  43. Charlesworth, D.; Barton, N.H.; Charlesworth, B. The Sources of Adaptive Variation. Proc. R. Soc. B-Biol. Sci. 2017, 284, 20162864. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Begon, M.; Townsend, C.R. Ecology: From Individuals to Ecosystems, 5th ed.; Wiley: Hoboken, NJ, USA, 2021; ISBN 978-1-119-27931-0. [Google Scholar]
  45. Barton, N.H.; Etheridge, A.M.; Véber, A. The Infinitesimal Model: Definition, Derivation, and Implications. Theor. Popul. Biol. 2017, 118, 50–73. [Google Scholar] [CrossRef]
  46. Golicz, A.A.; Bayer, P.E.; Bhalla, P.L.; Batley, J.; Edwards, D. Pangenomics Comes of Age: From Bacteria to Plant and Animal Applications. Trends Genet. 2020, 36, 132–145. [Google Scholar] [CrossRef] [PubMed]
  47. McInerney, J.O.; McNally, A.; O’Connell, M.J. Why Prokaryotes Have Pangenomes. Nat. Microbiol. 2017, 2, 17040. [Google Scholar] [CrossRef] [Green Version]
  48. Persson, T.; Battenberg, K.; Demina, I.V.; Vigil-Stenman, T.; Vanden Heuvel, B.; Pujic, P.; Facciotti, M.T.; Wilbanks, E.G.; O’Brien, A.; Fournier, P.; et al. Candidatus Frankia Datiscae Dg1, the Actinobacterial Microsymbiont of Datisca glomerata, Expresses the Canonical nod Genes nodABC in Symbiosis with Its Host Plant. PLoS ONE 2015, 10, e0127630. [Google Scholar] [CrossRef] [Green Version]
  49. Nguyen, T.V.; Wibberg, D.; Battenberg, K.; Blom, J.; Vanden Heuvel, B.; Berry, A.M.; Kalinowski, J.; Pawlowski, K. An Assemblage of Frankia Cluster II Strains from California Contains the Canonical nod Genes and Also the Sulfotransferase Gene nodH. BMC Genom. 2016, 17, 796. [Google Scholar] [CrossRef] [Green Version]
  50. Ktari, A.; Nouioui, I.; Furnholm, T.; Swanson, E.; Ghodhbane-Gtari, F.; Tisa, L.S.; Gtari, M. Permanent Draft Genome Sequence of Frankia sp. NRRL B-16219 Reveals the Presence of Canonical nod Genes, Which Are Highly Homologous to Those Detected in Candidatus Frankia Dg1 Genome. Stand. Genom. Sci. 2017, 12, 51. [Google Scholar] [CrossRef] [Green Version]
  51. Aoki, S.; Ito, M.; Iwasaki, W. From β- to α-Proteobacteria: The Origin and Evolution of Rhizobial Nodulation Genes nodIJ. Mol. Biol. Evol. 2013, 30, 2494–2508. [Google Scholar] [CrossRef]
  52. Tian, C.F.; Zhou, Y.J.; Zhang, Y.M.; Li, Q.Q.; Zhang, Y.Z.; Li, D.F.; Wang, S.; Wang, J.; Gilbert, L.B.; Li, Y.R.; et al. Comparative Genomics of Rhizobia Nodulating Soybean Suggests Extensive Recruitment of Lineage-Specific Genes in Adaptations. Proc. Natl. Acad. Sci. USA 2012, 109, 8629–8634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Tian, C.F.; Young, J.P.W. Evolution of Symbiosis Genes: Vertical and Horizontal Gene Transfer. In Ecology and Evolution of Rhizobia: Principles and Applications; Wang, E.T., Tian, C.F., Chen, W.F., Young, J.P.W., Chen, W.X., Eds.; Springer: Singapore, 2019; pp. 145–152. ISBN 978-981-32-9554-4. [Google Scholar] [CrossRef]
  54. Perret, X.; Staehelin, C.; Broughton, W.J. Molecular Basis of Symbiotic Promiscuity. Microbiol. Mol. Biol. Rev. 2000, 64, 180–201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Roche, P.; Maillet, F.; Plazanet, C.; Debellé, F.; Ferro, M.; Truchet, G.; Promé, J.-C.; Denarié, J. The Common nodABC Genes of Rhizobium meliloti Are Host-Range Determinants. Proc. Natl. Acad. Sci. USA 1996, 93, 15305–15310. [Google Scholar] [CrossRef] [Green Version]
  56. Kamst, E.; Pilling, J.; Raamsdonk, L.M.; Lugtenberg, B.J.; Spaink, H.P. Rhizobium Nodulation Protein NodC Is an Important Determinant of Chitin Oligosaccharide Chain Length in Nod Factor Biosynthesis. J. Bacteriol. 1997, 179, 2103–2108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Barran, L.R.; Bromfield, E.S.P.; Brown, D.C.W. Identification and Cloning of the Bacterial Nodulation Specificity Gene in the Sinorhizobium meliloti-Medicago laciniata Symbiosis. Can. J. Microbiol. 2002, 48, 765–771. [Google Scholar] [CrossRef] [PubMed]
  58. Rogel, M.A.; Ormeño-Orrillo, E.; Martinez Romero, E. Symbiovars in Rhizobia Reflect Bacterial Adaptation to Legumes. Syst. Appl. Microbiol. 2011, 34, 96–104. [Google Scholar] [CrossRef]
  59. Wang, E.T.; Chen, W.F.; Tian, C.F.; Young, J.P.W.; Chen, W.X. Ecology and Evolution of Rhizobia: Principles and Applications; Springer: Singapore, 2019; ISBN 978-981-32-9554-4. [Google Scholar] [CrossRef]
  60. Moron, B.; Soria-Diaz, M.E.; Ault, J.; Verroios, G.; Noreen, S.; Rodriguez-Navarro, D.N.; Gil-Serrano, A.; Thomas-oates, J.; Megias, M.; Sousa, C.; et al. Low pH Changes the Profile of Nodulation Factors Produced by Rhizobium tropici CIAT899. Chem. Biol. 2005, 12, 1029–1040. [Google Scholar] [CrossRef] [Green Version]
  61. Ormeño-Orrillo, E.; Menna, P.; Almeida, L.G.P.; Ollero, F.J.; Nicolás, M.F.; Pains Rodrigues, E.; Shigueyoshi Nakatani, A.; Silva Batista, J.S.; Oliveira Chueire, L.M.; Souza, R.C.; et al. Genomic Basis of Broad Host Range and Environmental Adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 Which Are Used in Inoculants for Common Bean (Phaseolus vulgaris L.). BMC Genom. 2012, 13, 735. [Google Scholar] [CrossRef]
  62. Mulligan, J.T.; Long, S.R. Induction of Rhizobium meliloti nodC Expression by Plant Exudate Requires nodD. Proc. Natl. Acad. Sci. USA 1985, 82, 6609–6613. [Google Scholar] [CrossRef] [Green Version]
  63. Hu, H.; Liu, S.; Yang, Y.; Chang, W.; Hong, G. In Rhizobium leguminosarum, NodD Represses Its Own Transcription by Competing with RNA Polymerase for Binding Sites. Nucleic Acids Res. 2000, 28, 2784–2793. [Google Scholar] [CrossRef] [Green Version]
  64. Györgypal, Z.; Kondorosi, É.; Kondorosi, A. Diverse Signal Sensitivity of NodD Protein Homologs from Narrow and Broad Host Range Rhizobia. Mol. Plant Microbe Interact. 1991, 4, 356–364. [Google Scholar] [CrossRef]
  65. Machado, D.; Krishnan, H.B. nodD Alleles of Sinorhizobium fredii USDA191 Differentially Influence Soybean Nodulation, nodC Expression, and Production of Exopolysaccharides. Curr. Microbiol. 2003, 47, 134–137. [Google Scholar] [CrossRef] [PubMed]
  66. Krishnan, H.B.; Kuo, C.I.; Pueppke, S.G. Elaboration of Flavonoid-Induced Proteins by the Nitrogen-Fixing Soybean Symbiont Rhizobium fredii Is Regulated by Both nodD1 and nodD2, and Is Dependent on the Cultivar-Specificity Locus, nolXWBTUV. Microbiology 1995, 141, 2245–2251. [Google Scholar] [CrossRef] [Green Version]
  67. del Cerro, P.; Rolla-Santos, A.A.P.; Gomes, D.F.; Marks, B.B.; Espuny, M.d.R.; Rodríguez-Carvajal, M.Á.; Soria-Díaz, M.E.; Nakatani, A.S.; Hungria, M.; Ollero, F.J.; et al. Opening the “black Box” of nodD3, nodD4 and nodD5 Genes of Rhizobium tropici Strain CIAT 899. BMC Genom. 2015, 16, 864. [Google Scholar] [CrossRef] [Green Version]
  68. Lestrange, K.K.; Bender, G.L.; Djordjevic, M.A.; Rolfe, B.G.; Redmond, J.W. The Rhizobium Strain NGR234 nodD1 Gene-Product Responds to Activation by the Simple Phenolic-Compounds Vanillin and Isovanillin Present in Wheat Seedling Extracts. Mol. Plant Microbe Interact. 1990, 3, 214–220. [Google Scholar] [CrossRef]
  69. Jiao, Y.S.; Liu, Y.H.; Yan, H.; Wang, E.T.; Tian, C.F.; Chen, W.X.; Guo, B.L.; Chen, W.F. Rhizobial Diversity and Nodulation Characteristics of the Extremely Promiscuous Legume Sophora flavescens. Mol. Plant Microbe Interact. 2015, 28, 1338–1352. [Google Scholar] [CrossRef] [Green Version]
  70. Guo, H.J.; Wang, E.T.; Zhang, X.X.; Li, Q.Q.; Zhang, Y.M.; Tian, C.F.; Chen, W.X. Replicon-Dependent Differentiation of Symbiosis-Related Genes in Sinorhizobium Strains Nodulating Glycine max. Appl. Environ. Microbiol. 2014, 80, 1245–1255. [Google Scholar] [CrossRef] [Green Version]
  71. Zhang, X.X.; Guo, H.J.; Wang, R.; Sui, X.H.; Zhang, Y.M.; Wang, E.T.; Tian, C.F.; Chen, W.X. Genetic Divergence of Bradyrhizobium Nodulating Soybeans as Revealed by Multilocus Sequence Analysis of Genes inside and Outside the Symbiosis Island. Appl. Environ. Microbiol. 2014, 80, 3181–3190. [Google Scholar] [CrossRef]
  72. Pueppke, S.G.; Broughton, W.J. Rhizobium sp. Strain NGR234 and R. fredii USDA257 Share Exceptionally Broad, Nested Host Ranges. Mol. Plant Microbe Interact. 1999, 12, 293–318. [Google Scholar] [CrossRef] [Green Version]
  73. Songwattana, P.; Tittabutr, P.; Wongdee, J.; Teamtisong, K.; Wulandari, D.; Teulet, A.; Fardoux, J.; Boonkerd, N.; Giraud, E.; Teaumroong, N. Symbiotic Properties of a Chimeric Nod-independent Photosynthetic Bradyrhizobium Strain Obtained by Conjugative Transfer of a Symbiotic Plasmid. Environ. Microbiol. 2019, 21, 3442–3454. [Google Scholar] [CrossRef]
  74. Pi, H.W.; Lin, J.J.; Chen, C.A.; Wang, P.H.; Chiang, Y.R.; Huang, C.C.; Young, C.C.; Li, W.H. Origin and Evolution of Nitrogen Fixation in Prokaryotes. Mol. Biol. Evol. 2022, 39, msac181. [Google Scholar] [CrossRef]
  75. Okubo, T.; Piromyou, P.; Tittabutr, P.; Teaumroong, N.; Minamisawa, K. Origin and Evolution of Nitrogen Fixation Genes on Symbiosis Islands and Plasmid in Bradyrhizobium. Microbes Environ. 2016, 31, 260–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Tian, C.F.; Young, J.P.W. Genomics and Evolution of Rhizobia. In Ecology and Evolution of Rhizobia: Principles and Applications; Wang, E.T., Tian, C.F., Chen, W.F., Young, J.P.W., Chen, W.X., Eds.; Springer: Singapore, 2019; pp. 103–119. ISBN 978-981-32-9554-4. [Google Scholar] [CrossRef]
  77. Cui, W.; Zhang, B.; Zhao, R.; Liu, L.; Jiao, J.; Zhang, Z.; Tian, C.-F. Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency. mSystems 2021, 6, e01299-20. [Google Scholar] [CrossRef] [PubMed]
  78. Cavassim, M.I.A.; Moeskjær, S.; Moslemi, C.; Fields, B.; Bachmann, A.; Vilhjálmsson, B.J.; Schierup, M.H.; Young, J.P.W.; Andersen, S.U. Symbiosis Genes Show a Unique Pattern of Introgression and Selection within a Rhizobium leguminosarum Species Complex. Microb. Genom. 2020, 6, e000351. [Google Scholar] [CrossRef] [PubMed]
  79. Perez Carrascal, O.M.; VanInsberghe, D.; Juarez, S.; Polz, M.F.; Vinuesa, P.; Gonzalez, V. Population Genomics of the Symbiotic Plasmids of Sympatric Nitrogen-Fixing Rhizobium Species Associated with Phaseolus vulgaris. Environ. Microbiol. 2016, 18, 2660–2676. [Google Scholar] [CrossRef] [PubMed]
  80. Epstein, B.; Branca, A.; Mudge, J.; Bharti, A.K.; Briskine, R.; Farmer, A.D.; Sugawara, M.; Young, N.D.; Sadowsky, M.J.; Tiffin, P. Population Genomics of the Facultatively Mutualistic Bacteria Sinorhizobium meliloti and S. medicae. PLoS Genet. 2012, 8, e1002868. [Google Scholar] [CrossRef] [PubMed]
  81. Ledermann, R.; Schulte, C.C.M.; Poole, P.S. How Rhizobia Adapt to the Nodule Environment. J. Bacteriol. 2021, 203, e00539-20. [Google Scholar] [CrossRef]
  82. Preisig, O.; Zufferey, R.; Hennecke, H. The Bradyrhizobium japonicum fixGHIS Genes Are Required for the Formation of the High-Affinity cbb3-Type Cytochrome Oxidase. Arch. Microbiol. 1996, 165, 297–305. [Google Scholar] [CrossRef]
  83. Staehelin, C.; Krishnan, H.B. Nodulation Outer Proteins: Double-Edged Swords of Symbiotic Rhizobia. Biochem. J. 2015, 470, 263–274. [Google Scholar] [CrossRef] [Green Version]
  84. Zhao, R.; Liu, L.X.; Zhang, Y.Z.; Jiao, J.; Cui, W.J.; Zhang, B.; Wang, X.L.; Li, M.L.; Chen, Y.; Xiong, Z.Q.; et al. Adaptive Evolution of Rhizobial Symbiotic Compatibility Mediated by Co-Evolved Insertion Sequences. ISME J. 2018, 12, 101–111. [Google Scholar] [CrossRef] [Green Version]
  85. Sugawara, M.; Takahashi, S.; Umehara, Y.; Iwano, H.; Tsurumaru, H.; Odake, H.; Suzuki, Y.; Kondo, H.; Konno, Y.; Yamakawa, T.; et al. Variation in Bradyrhizobial NopP Effector Determines Symbiotic Incompatibility with Rj2-Soybeans via Effector-Triggered Immunity. Nat. Commun. 2018, 9, 3139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Zhang, B.; Wang, M.; Sun, Y.; Zhao, P.; Liu, C.; Qing, K.; Hu, X.; Zhong, Z.; Cheng, J.; Wang, H.; et al. Glycine max NNL1 Restricts Symbiotic Compatibility with Widely Distributed Bradyrhizobia via Root Hair Infection. Nat. Plants 2021, 7, 73–86. [Google Scholar] [CrossRef] [PubMed]
  87. Hubber, A.; Vergunst, A.C.; Sullivan, J.T.; Hooykaas, P.J.J.; Ronson, C.W. Symbiotic Phenotypes and Translocated Effector Proteins of the Mesorhizobium loti Strain R7A VirB/D4 Type IV Secretion System. Mol. Microbiol. 2004, 54, 561–574. [Google Scholar] [CrossRef] [PubMed]
  88. Paço, A.; Da-Silva, J.R.; Eliziário, F.; Brígido, C.; Oliveira, S.; Alexandre, A. traG Gene Is Conserved across Mesorhizobium spp. Able to Nodulate the Same Host Plant and Expressed in Response to Root Exudates. Biomed Res. Int. 2019, 2019, 3715271. [Google Scholar] [CrossRef]
  89. Sullivan, J.T.; Trzebiatowski, J.R.; Cruickshank, R.W.; Gouzy, J.; Brown, S.D.; Elliot, R.M.; Fleetwood, D.J.; McCallum, N.G.; Rossbach, U.; Stuart, G.S.; et al. Comparative Sequence Analysis of the Symbiosis Island of Mesorhizobium loti Strain R7A. J. Bacteriol. 2002, 184, 3086–3095. [Google Scholar] [CrossRef] [Green Version]
  90. Hubber, A.M.; Sullivan, J.T.; Ronson, C.W. Symbiosis-Induced Cascade Regulation of the Mesorhizobium loti R7A VirB/D4 Type IV Secretion System. Mol. Plant-Microbe Interact. 2007, 20, 255–261. [Google Scholar] [CrossRef] [Green Version]
  91. Yang, L.L.; Jiang, Z.; Li, Y.; Wang, E.T.; Zhi, X.Y. Plasmids Related to the Symbiotic Nitrogen Fixation Are Not Only Cooperated Functionally but Also May Have Evolved over a Time Span in Family Rhizobiaceae. Genome. Biol. Evol. 2020, 12, 2002–2014. [Google Scholar] [CrossRef]
  92. Nelson, M.; Guhlin, J.; Epstein, B.; Tiffin, P.; Sadowsky, M.J. The Complete Replicons of 16 Ensifer meliloti Strains Offer Insights into Intra-and Inter-Replicon Gene Transfer, Transposon-Associated Loci, and Repeat Elements. Microb. Genom. 2018, 4, e000174. [Google Scholar] [CrossRef] [Green Version]
  93. Jozefkowicz, C.; Brambilla, S.; Frare, R.; Stritzler, M.; Piccinetti, C.; Puente, M.; Berini, C.A.; Pérez, P.R.; Soto, G.; Ayub, N. Stable Symbiotic Nitrogen Fixation under Water-Deficit Field Conditions by a Stress-Tolerant Alfalfa Microsymbiont and Its Complete Genome Sequence. J. Biotechnol. 2017, 263, 52–54. [Google Scholar] [CrossRef]
  94. Zhang, P.; Zhang, B.; Jiao, J.; Dai, S.-Q.; Chen, W.-X.; Tian, C.-F. Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery. mBio 2020, 11, e03193-19. [Google Scholar] [CrossRef] [Green Version]
  95. Price, P.A.; Tanner, H.R.; Dillon, B.A.; Shabab, M.; Walker, G.C.; Griffitts, J.S. Rhizobial Peptidase HrrP Cleaves Host-Encoded Signaling Peptides and Mediates Symbiotic Compatibility. Proc. Natl. Acad. Sci. USA 2015, 112, 15244–15249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Crook, M.B.; Lindsay, D.P.; Biggs, M.B.; Bentley, J.S.; Price, J.C.; Clement, S.C.; Clement, M.J.; Long, S.R.; Griffitts, J.S. Rhizobial Plasmids That Cause Impaired Symbiotic Nitrogen Fixation and Enhanced Host Invasion. Mol. Plant-Microbe Interact. 2012, 25, 1026–1033. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  97. Arashida, H.; Odake, H.; Sugawara, M.; Noda, R.; Kakizaki, K.; Ohkubo, S.; Mitsui, H.; Sato, S.; Minamisawa, K. Evolution of Rhizobial Symbiosis Islands through Insertion Sequence-Mediated Deletion and Duplication. ISME J. 2022, 16, 112–121. [Google Scholar] [CrossRef]
  98. Remigi, P.; Capela, D.; Clerissi, C.; Tasse, L.; Torchet, R.; Bouchez, O.; Batut, J.; Cruveiller, S.; Rocha, E.P.C.; Masson-Boivin, C. Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts Following Horizontal Gene Transfer. PLoS Biol. 2014, 12, e1001942. [Google Scholar] [CrossRef] [Green Version]
  99. Tang, M.; Bouchez, O.; Masson-boivin, C.; Capela, D. Modulation of Quorum Sensing as an Adaptation to Nodule Cell Infection during Experimental Evolution of Legume. mBio 2020, 11, e03129-19. [Google Scholar] [CrossRef] [Green Version]
  100. Doin de Moura, G.G.; Remigi, P.; Masson-boivin, C.; Capela, D. Experimental Evolution of Legume Symbionts: What Have We Learnt? Genes 2020, 11, 339. [Google Scholar] [CrossRef] [Green Version]
  101. Biemont, C. A Brief History of the Status of Transposable Elements: From Junk DNA to Major Players in Evolution. Genetics 2010, 1093, 1085–1093. [Google Scholar] [CrossRef]
  102. Niu, X.M.; Xu, Y.C.; Li, Z.W.; Bian, Y.T.; Hou, X.H.; Chen, J.F.; Zou, Y.P.; Jiang, J.; Wu, Q.; Ge, S.; et al. Transposable Elements Drive Rapid Phenotypic Variation in Capsella rubella. Proc. Natl. Acad. Sci. USA 2019, 116, 6908–6913. [Google Scholar] [CrossRef] [Green Version]
  103. Vandecraen, J.; Chandler, M.; Aertsen, A.; Van Houdt, R. The Impact of Insertion Sequences on Bacterial Genome Plasticity and Adaptability. Crit. Rev. Microbiol. 2017, 43, 709–730. [Google Scholar] [CrossRef] [Green Version]
  104. Siguier, P.; Gourbeyre, E.; Chandler, M. Bacterial Insertion Sequences: Their Genomic Impact and Diversity. FEMS Microbiol. Rev. 2014, 38, 865–891. [Google Scholar] [CrossRef] [Green Version]
  105. Freiberg, C.; Fellay, R.; Bairoch, A.; Broughton, W.J.; Rosenthal, A.; Perret, X. Molecular Basis of Symbiosis between Rhizobium and Legumes. Nature 1997, 387, 394–401. [Google Scholar] [CrossRef] [PubMed]
  106. Barnett, M.J.; Fisher, R.F.; Jones, T.; Komp, C.; Abola, A.P.; Barloy-Hubler, F.; Bowser, L.; Capela, D.; Galibert, F.; Gouzy, J.; et al. Nucleotide Sequence and Predicted Functions of the Entire Sinorhizobium meliloti pSymA Megaplasmid. Proc. Natl. Acad. Sci. USA 2001, 98, 9883–9888. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Kaneko, T.; Nakamura, Y.; Sato, S.; Asamizu, E.; Kato, T.; Sasamoto, S.; Watanabe, A.; Idesawa, K.; Ishikawa, A.; Kawashima, K.; et al. Complete Genome Structure of the Nitrogen-Fixing Symbiotic Bacterium Mesorhizobium loti. DNA Res. 2000, 7, 331–338. [Google Scholar] [CrossRef] [Green Version]
  108. Barros-Carvalho, G.A.; Hungria, M.; Lopes, F.M.; Van Sluys, M.A. Brazilian-Adapted Soybean Bradyrhizobium Strains Uncover IS Elements with Potential Impact on Biological Nitrogen Fixation. FEMS Microbiol. Lett. 2019, 366, fnz046. [Google Scholar] [CrossRef] [PubMed]
  109. Tao, J.; Wang, S.; Liao, T.; Luo, H. Evolutionary Origin and Ecological Implication of a Unique nif Island in Free-Living Bradyrhizobium Lineages. ISME J. 2021, 15, 3195–3206. [Google Scholar] [CrossRef] [PubMed]
  110. Guo, H.; Shi, W.; Zhang, B.; Xu, Y.; Jiao, J. Intracellular Common Gardens Reveal Niche Differentiation in Transposable Element Community during Bacterial Adaptive Evolution. ISME J. 2022. [Google Scholar] [CrossRef]
  111. Jiao, J.; Zhang, B.; Li, M.-L.; Zhang, Z.; Tian, C.-F. The Zinc-Finger Bearing Xenogeneic Silencer MucR in α-Proteobacteria Balances Adaptation and Regulatory Integrity. ISME J. 2022, 16, 738–749. [Google Scholar] [CrossRef]
  112. Shi, W.-T.; Zhang, B.; Li, M.-L.; Liu, K.-H.; Jiao, J.; Tian, C.-F. The Convergent Xenogeneic Silencer MucR Predisposes α-Proteobacteria to Integrate AT-Rich Symbiosis Genes. Nucleic Acids Res. 2022, 50, 8580–8598. [Google Scholar] [CrossRef]
  113. Jiao, J.; Tian, C.-F. Ancestral Zinc-Finger Bearing Protein MucR in Alpha-Proteobacteria: A Novel Xenogeneic Silencer? Comput. Struct. Biotechnol. J. 2020, 18, 3623–3631. [Google Scholar] [CrossRef]
  114. Jiao, J.; Ni, M.; Zhang, B.; Zhang, Z.; Young, J.P.W.; Chan, T.-F.; Chen, W.X.; Lam, H.-M.; Tian, C.F. Coordinated Regulation of Core and Accessory Genes in the Multipartite Genome of Sinorhizobium fredii. PLoS Genet. 2018, 14, e1007428. [Google Scholar] [CrossRef] [Green Version]
  115. Wheatley, R.M.; Ford, B.L.; Li, L.; Aroney, S.T.N.; Knights, H.E.; Ledermann, R.; East, A.K.; Ramachandran, V.K.; Poole, P.S. Lifestyle Adaptations of Rhizobium from Rhizosphere to Symbiosis. Proc. Natl. Acad. Sci. USA 2020, 117, 23823–23834. [Google Scholar] [CrossRef] [PubMed]
  116. DiCenzo, G.C.; Checcucci, A.; Bazzicalupo, M.; Mengoni, A.; Viti, C.; Dziewit, L.; Finan, T.M.; Galardini, M.; Fondi, M. Metabolic Modelling Reveals the Specialization of Secondary Replicons for Niche Adaptation in Sinorhizobium meliloti. Nat. Commun. 2016, 7, 12219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  117. Galardini, M.; Pini, F.; Bazzicalupo, M.; Biondi, E.G.; Mengoni, A. Replicon-Dependent Bacterial Genome Evolution: The Case of Sinorhizobium meliloti. Genome Biol. Evol. 2013, 5, 542–558. [Google Scholar] [CrossRef]
  118. Ramachandran, V.K.; East, A.K.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Adaptation of Rhizobium leguminosarum to Pea, Alfalfa and Sugar Beet Rhizospheres Investigated by Comparative Transcriptomics. Genome Biol. 2011, 12, R106. [Google Scholar] [CrossRef] [Green Version]
  119. Vercruysse, M.; Fauvart, M.; Beullens, S.; Braeken, K.; Cloots, L.; Engelen, K.; Marchal, K.; Michiels, J. A Comparative Transcriptome Analysis of Rhizobium etli Bacteroids: Specific Gene Expression During Symbiotic Nongrowth. Mol. Plant Microbe Interact. 2011, 24, 1553–1561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  120. Capela, D.; Filipe, C.; Bobilk, C.; Batut, J.; Bruand, C.; Bobik, C.; Plantes-microorganismes, L.I.; Inra-cnrs, U.M.R. Sinorhizobium meliloti Differentiation during Symbiosis with Alfalfa: A Transcriptomic Dissection. Mol. Plant Microbe Interact. 2006, 19, 363–372. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  121. Li, Y.; Tian, C.F.; Chen, W.F.; Wang, L.; Sui, X.H.; Chen, W.X. High-Resolution Transcriptomic Analyses of Sinorhizobium sp. NGR234 Bacteroids in Determinate Nodules of Vigna unguiculata and Indeterminate Nodules of Leucaena leucocephala. PLoS ONE 2013, 8, e70531. [Google Scholar] [CrossRef]
  122. Green, R.T.; East, A.K.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Transcriptomic Analysis of Rhizobium leguminosarum Bacteroids in Determinate and Indeterminate Nodules. Microb. Genom. 2019, 5, e000254. [Google Scholar] [CrossRef]
  123. Schulte, C.C.M.; Borah, K.; Wheatley, R.M.; Terpolilli, J.J.; Saalbach, G.; Crang, N.; de Groot, D.H.; Ratcliffe, R.G.; Kruger, N.J.; Papachristodoulou, A.; et al. Metabolic Control of Nitrogen Fixation in Rhizobium-Legume Symbioses. Sci. Adv. 2021, 7, eabh2433. [Google Scholar] [CrossRef]
  124. Aroney, S.T.N.; Poole, P.S.; Sánchez-Cañizares, C. Rhizobial Chemotaxis and Motility Systems at Work in the Soil. Front. Plant Sci. 2021, 12, 1856. [Google Scholar] [CrossRef]
  125. Acosta-jurado, S.; Fuentes-romero, F.; Ruiz-sainz, J.E.; Janczarek, M.; Vinardell, J.M. Rhizobial Exopolysaccharides: Genetic Regulation of Their Synthesis and Relevance in Symbiosis with Legumes. Int. J. Mol. Sci. 2021, 22, 6233. [Google Scholar] [CrossRef] [PubMed]
  126. Janczarek, M.; Rachwał, K.; Marzec, A.; Grzadziel, J.; Palusińska-Szysz, M. Signal Molecules and Cell-Surface Components Involved in Early Stages of the Legume-Rhizobium Interactions. Appl. Soil Ecol. 2015, 85, 94–113. [Google Scholar] [CrossRef]
  127. Kawaharada, Y.; Kelly, S.; Nielsen, M.W.; Hjuler, C.T.; Gysel, K.; Muszyński, A.; Carlson, R.W.; Thygesen, M.B.; Sandal, N.; Asmussen, M.H.; et al. Receptor-Mediated Exopolysaccharide Perception Controls Bacterial Infection. Nature 2015, 523, 308–312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  128. Kawaharada, Y.; Nielsen, M.W.; Kelly, S.; James, E.K.; Andersen, K.R.; Madsen, L.H.; Heckmann, A.B.; Radutoiu, S.; Rasmussen, S.R.; Fu, W.; et al. Differential Regulation of the Epr3 Receptor Coordinates Membrane-Restricted Rhizobial Colonization of Root Nodule Primordia. Nat. Commun. 2017, 8, 14534. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  129. Arnold, M.F.F.; Penterman, J.; Shabab, M.; Chen, E.J.; Walker, C. Important Late-Stage Symbiotic Role of the Sinorhizobium meliloti Exopolysaccharide Succinoglycan. J. Bacteriol. 2018, 200, e00665-17. [Google Scholar] [CrossRef] [Green Version]
  130. Li, D.; Li, Z.; Wu, J.; Tang, Z.; Xie, F.; Chen, D.; Lin, H.; Li, Y. Analysis of Outer Membrane Vesicles Indicates That Glycerophospholipid Metabolism Contributes to Early Symbiosis Between Sinorhizobium fredii HH103 and Soybean. Mol. Plant-Microbe Interact. 2022, 35, 311–322. [Google Scholar] [CrossRef]
  131. Yang, M.H.; Sun, K.J.; Zhou, L.; Yang, R.F.; Zhong, Z.T.; Zhu, J. Functional Analysis of Three AHL Autoinducer Synthase Genes in Mesorhizobium loti Reveals the Important Role of Quorum Sensing in Symbiotic Nodulation. Can. J. Microbiol. 2009, 55, 210–214. [Google Scholar] [CrossRef]
  132. Marketon, M.M.; Gronquist, M.R.; Eberhard, A.; Gonza, J.E. Characterization of the Sinorhizobium meliloti sinR/sinI Locus and the Production of Novel N-Acyl Homoserine Lactones. J. Bacteriol. 2002, 184, 5686–5695. [Google Scholar] [CrossRef] [Green Version]
  133. Gurich, N.; Gonzalez, J.E. Role of Quorum Sensing in Sinorhizobium meliloti-Alfalfa Symbiosis. J. Bacteriol. 2009, 191, 4372–4382. [Google Scholar] [CrossRef] [Green Version]
  134. Acosta-Jurado, S.; Alías-Villegas, C.; Almozara, A.; Espuny, M.R.; Vinardell, J.M.; Pérez-Montaño, F. Deciphering the Symbiotic Significance of Quorum Sensing Systems of Sinorhizobium fredii HH103. Microorganisms 2020, 8, 68. [Google Scholar] [CrossRef] [Green Version]
  135. Calatrava-Morales, N.; McIntosh, M.; Soto, M.J. Regulation Mediated by N-Acyl Homoserine Lactone Quorum Sensing Signals in the Rhizobium-Legume Symbiosis. Genes 2018, 9, 263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  136. Jiménez-Guerrero, I.; Medina, C.; Vinardell, J.M.; Ollero, F.J.; López-Baena, F.J. The Rhizobial Type 3 Secretion System: The Dr. Jekyll and Mr. Hyde in the Rhizobium–Legume Symbiosis. Int. J. Mol. Sci. 2022, 23, 11089. [Google Scholar] [CrossRef] [PubMed]
  137. Ratu, S.T.N.; Amelia, L.; Okazaki, S. Type III Effector Provides a Novel Symbiotic Pathway in Legume-Rhizobia Symbiosis. Biosci. Biotechnol. Biochem. 2023, 87, 28–37. [Google Scholar] [CrossRef] [PubMed]
  138. De Sousa, B.F.S.; Castellane, T.C.L.; Tighilt, L.; Lemos, E.G. de M.; Rey, L. Rhizobial Exopolysaccharides and Type VI Secretion Systems: A Promising Way to Improve Nitrogen Acquisition by Legumes. Front. Agron. 2021, 3, e661468. [Google Scholar] [CrossRef]
  139. Salinero-Lanzarote, A.; Pacheco-Moreno, A.; Domingo-Serrano, L.; Durán, D.; Ormeño-Orrillo, E.; Martínez-Romero, E.; Albareda, M.; Palacios, J.M.; Rey, L. The Type VI Secretion System of Rhizobium etli Mim1 Has a Positive Effect in Symbiosis. FEMS Microbiol. Ecol. 2019, 95, efiz054. [Google Scholar] [CrossRef]
  140. Fauvart, M.; Michiels, J. Rhizobial Secreted Proteins as Determinants of Host Specificity in the Rhizobium-Legume Symbiosis. FEMS Microbiol. Lett. 2008, 285, 1–9. [Google Scholar] [CrossRef] [Green Version]
  141. Finnie, C.; Hartley, N.M.; Findlay, K.C.; Downie, J.A. The Rhizobium leguminosarum prsDE Genes Are Required for Secretion of Several Proteins, Some of Which Influence Nodulation, Symbiotic Nitrogen Fixation and Exopolysaccharide Modification. Mol. Microbiol. 1997, 25, 135–146. [Google Scholar] [CrossRef]
  142. Liu, J.; Wang, T.; Qin, Q.; Yu, X.; Yang, S.; Dinkins, R.D.; Kuczmog, A.; Putnoky, P.; Muszyński, A.; Griffitts, J.S.; et al. Paired Medicago Receptors Mediate Broad-Spectrum Resistance to Nodulation by Sinorhizobium meliloti Carrying a Species-Specific Gene. Proc. Natl. Acad. Sci. USA 2022, 119, e2214703119. [Google Scholar] [CrossRef]
  143. Yurgel, S.N.; Kahn, M.L. Dicarboxylate Transport by Rhizobia. FEMS Microbiol. Rev. 2004, 28, 489–501. [Google Scholar] [CrossRef] [Green Version]
  144. Wang, C.; Saldanha, M.; Sheng, X.; Shelswell, K.J.; Walsh, K.T.; Sobral, B.W.S.; Charles, T.C. Roles of Poly-3-Hydroxybutyrate (PHB) and Glycogen in Symbiosis of Sinorhizobium meliloti with Medicago sp. Microbiology 2007, 153, 388–398. [Google Scholar] [CrossRef] [Green Version]
  145. Mandon, K.; Michel-reydellet, N.; Encarnacio, S.; Kaminski, P.A.; Leija, A.; Cevallos, M.A.; Elmerich, C.; Mora, J. Poly-β-Hydroxybutyrate Turnover in Azorhizobium caulinodans Is Required for Growth and Affects nifA Expression. J. Bacteriol. 1998, 180, 5070–5076. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  146. Sun, Y.-W.; Li, Y.; Hu, Y.; Chen, W.-X.; Tian, C.-F. Coordinated Regulation of the Size and Number of Polyhydroxybutyrate Granules by Core and Accessory Phasins in the Facultative Microsymbiont Sinorhizobium fredii NGR234. Appl. Environ. Microbiol. 2019, 85, e00717-19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  147. Lodwig, E.M.; Hosie, A.H.; Bourdes, A.; Findlay, K.; Allaway, D.; Karunakaran, R.; Downie, J.A.; Poole, P.S. Amino-Acid Cycling Drives Nitrogen Fixation in the Legume-Rhizobium Symbiosis. Nature 2003, 422, 722–726. [Google Scholar] [CrossRef]
  148. Prell, J.; White, J.P.; Bourdes, A.; Bunnewell, S.; Bongaerts, R.J.; Poole, P.S. Legumes Regulate Rhizobium Bacteroid Development and Persistence by the Supply of Branched-Chain Amino Acids. Proc. Natl. Acad. Sci. USA 2009, 106, 12477–12482. [Google Scholar] [CrossRef] [Green Version]
  149. Prell, J.; Bourdes, A.; Kumar, S.; Lodwig, E.; Hosie, A.; Kinghorn, S.; White, J.; Poole, P. Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses. PLoS ONE 2010, 5, e13933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  150. Hu, Y.; Jiao, J.; Liu, L.X.; Sun, Y.W.; Chen, W.; Sui, X.; Chen, W.; Tian, C.F. Evidence for Phosphate Starvation of Rhizobia without Terminal Differentiation in Legume Nodules. Mol. Plant-Microbe Interact. 2018, 31, 1060–1068. [Google Scholar] [CrossRef] [Green Version]
  151. Bardin, S.D.; Finan, T.M. Regulation of Phosphate Assimilation in Rhizobium (Sinorhizobium) meliloti. Genetics 1998, 148, 1689–1700. [Google Scholar] [CrossRef]
  152. Yuan, Z.C.; Zaheer, R.; Finan, T.M. Regulation and Properties of PstSCAB, a High-Affinity, High-Velocity Phosphate Transport System of Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 1089–1102. [Google Scholar] [CrossRef] [Green Version]
  153. Feng, X.-Y.; Tian, Y.; Cui, W.-J.; Li, Y.-Z.; Wang, D.; Liu, Y.; Jiao, J.; Chen, W.-X.; Tian, C.-F. The PTSNtr-KdpDE-KdpFABC Pathway Contributes to Low Potassium Stress Adaptation and Competitive Nodulation of Sinorhizobium fredii. mBio 2022, 13, e03721-21. [Google Scholar] [CrossRef]
  154. Dominguez-Ferreras, A.; Munoz, S.; Olivares, J.; Soto, M.J.; Sanjuan, J.; Domínguez-ferreras, A.; Mun, S.; Sanjua, J. Role of Potassium Uptake Systems in Sinorhizobium meliloti Osmoadaptation and Symbiotic Performance. J. Bacteriol. 2009, 191, 2133–2143. [Google Scholar] [CrossRef] [Green Version]
  155. Cheng, G.; Karunakaran, R.; East, A.K.; Poole, P.S. Multiplicity of Sulfate and Molybdate Transporters and Their Role in Nitrogen Fixation in Rhizobium leguminosarum bv. viciae Rlv3841. Mol. Plant-Microbe Interact. 2016, 29, 143–152. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  156. Liu, K.-H.; Zhang, B.; Yang, B.-S.; Shi, W.-T.; Li, Y.-F.; Wang, Y.; Zhang, P.; Jiao, J.; Tian, C.-F. Rhizobiales-Specific RirA Represses a Naturally “Synthetic” Foreign Siderophore Gene Cluster to Maintain Sinorhizobium-Legume Mutualism. mBio 2022, 13, e02900-21. [Google Scholar] [CrossRef] [PubMed]
  157. Sankari, S.; Babu, V.M.P.; Bian, K.; Alhhazmi, A.; Andorfer, M.C.; Avalos, D.M.; Smith, T.A.; Yoon, K.; Drennan, C.L.; Yaffe, M.B.; et al. A Haem-Sequestering Plant Peptide Promotes Iron Uptake in Symbiotic Bacteria. Nat. Microbiol. 2022, 7, 1453–1465. [Google Scholar] [CrossRef] [PubMed]
  158. Hood, G.; Ramachandran, V.K.; East, A.; Downie, J.A.; Poole, P.S. Manganese Transport Is Essential for N2-Fixation by Rhizobium leguminosarum in Bacteroids from Galegoid but Not Phaseoloid Nodules. Environ. Microbiol. 2017, 19, 2715–2726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  159. Ruiz, B.; Le Scornet, A.; Sauviac, L.; Rémy, A.; Bruand, C.; Meilhoc, E. The Nitrate Assimilatory Pathway in Sinorhizobium meliloti: Contribution to NO Production. Front. Microbiol. 2019, 10, 1526. [Google Scholar] [CrossRef] [PubMed]
  160. Cam, Y.; Pierre, O.; Boncompagni, E.; Herouart, D.; Meilhoc, E.; Bruand, C. Nitric Oxide (NO) a Key Player in the Senescence of Medicago truncatula Root Nodules. New Phytol. 2012, 196, 548–560. [Google Scholar] [CrossRef]
  161. Bobik, C.; Meilhoc, E.; Batut, J. FixJ: A Major Regulator of the Oxygen Limitation Response and Late Symbiotic Functions of Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 4890–4902. [Google Scholar] [CrossRef]
  162. Bauer, E.; Kaspar, T.; Fischer, H.M.; Hennecke, H. Expression of the fixR-nifA Operon in Bradyrhizobium japonicum Depends on a New Response Regulator, RegR. J. Bacteriol. 1998, 180, 3853–3863. [Google Scholar] [CrossRef] [Green Version]
  163. Rutten, P.J.; Steel, H.; Hood, G.A.; Ramachandran, V.K.; McMurtry, L.; Geddes, B.; Papachristodoulou, A.; Poole, P.S. Multiple Sensors Provide Spatiotemporal Oxygen Regulation of Gene Expression in a Rhizobium-Legume Symbiosis. PLoS Genet. 2021, 17, e1009099. [Google Scholar] [CrossRef]
  164. De Nisco, N.J.; Abo, R.P.; Wu, C.M.; Penterman, J.; Walker, G.C. Global Analysis of Cell Cycle Gene Expression of the Legume Symbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 2014, 111, 3217–3224. [Google Scholar] [CrossRef] [Green Version]
  165. Gibson, K.E.; Campbell, G.R.; Lloret, J.; Walker, G.C. CbrA Is a Stationary-Phase Regulator of Cell Surface Physiology and Legume Symbiosis in Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 4508–4521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Kobayashi, H.; De Nisco, N.J.; Chien, P.; Simmons, L.A.; Walker, G.C. Sinorhizobium meliloti CpdR1 Is Critical for Co-Ordinating Cell Cycle Progression and the Symbiotic Chronic Infection. Mol. Microbiol. 2009, 73, 586–600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  167. diCenzo, G.C.; Zamani, M.; Ludwig, H.N.; Finan, T.M. Heterologous Complementation Reveals a Specialized Activity for BacA in the Medicago-Sinorhizobium meliloti Symbiosis. Mol. Plant-Microbe Interact. 2017, 30, 312–324. [Google Scholar] [CrossRef] [Green Version]
  168. Marlow, V.L.; Haag, A.F.; Kobayashi, H.; Fletcher, V.; Scocchi, M.; Walker, G.C.; Ferguson, G.P. Essential Role for the BacA Protein in the Uptake of a Truncated Eukaryotic Peptide in Sinorhizobium meliloti. J. Bacteriol. 2009, 191, 1519–1527. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  169. Karunakaran, R.; Haag, A.F.; East, A.K.; Ramachandran, V.K.; Prell, J.; James, E.K.; Scocchi, M.; Ferguson, G.P.; Poole, P.S. BacA Is Essential for Bacteroid Development in Nodules of Galegoid, but Not Phaseoloid, Legumes. J. Bacteriol. 2010, 192, 2920–2928. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  170. Haag, A.F.; Baloban, M.; Sani, M.; Kerscher, B.; Pierre, O.; Farkas, A.; Longhi, R.; Boncompagni, E.; Hérouart, D.; Dall’Angelo, S.; et al. Protection of Sinorhizobium against Host Cysteine-Rich Antimicrobial Peptides Is Critical for Symbiosis. PLoS Biol. 2011, 9, e1001169. [Google Scholar] [CrossRef]
  171. Nicoud, Q.; Barrière, Q.; Busset, N.; Dendene, S.; Travin, D.; Bourge, M.; Le Bars, R.; Boulogne, C.; Lecroël, M.; Jenei, S.; et al. Sinorhizobium meliloti Functions Required for Resistance to Antimicrobial NCR Peptides and Bacteroid Differentiation. mBio 2021, 12, e00895-21. [Google Scholar] [CrossRef]
  172. Ren, B.; Wang, X.; Duan, J.; Ma, J. Rhizobial tRNA-Derived Small RNAs Are Signal Molecules Regulating Plant Nodulation. Science 2019, 365, 919–922. [Google Scholar] [CrossRef]
  173. García-Tomsig, N.I.; Robledo, M.; diCenzo, G.C.; Mengoni, A.; Millán, V.; Peregrina, A.; Uceta, A.; Jiménez-Zurdo, J.I. Pervasive RNA Regulation of Metabolism Enhances the Root Colonization Ability of Nitrogen-Fixing Symbiotic α-Rhizobia. mBio 2022, 13, e03576-21. [Google Scholar] [CrossRef] [PubMed]
  174. Sánchez-Cañizares, C.; Prell, J.; Pini, F.; Rutten, P.; Kraxner, K.; Wynands, B.; Karunakaran, R.; Poole, P.S. Global Control of Bacterial Nitrogen and Carbon Metabolism by a PTSNtr-Regulated Switch. Proc. Natl. Acad. Sci. USA 2020, 117, 10234–10245. [Google Scholar] [CrossRef]
  175. Li, Y.Z.; Wang, D.; Feng, X.Y.; Jiao, J.; Chen, W.X.; Tian, C.F. Genetic Analysis Reveals the Essential Role of Nitrogen Phosphotransferase System Components in Sinorhizobium fredii CCBAU 45436 Symbioses with Soybean and Pigeonpea Plants. Appl. Environ. Microbiol. 2016, 82, 1305–1315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  176. David, M.; Daveran, M.L.; Batut, J.; Dedieu, A.; Domergue, O.; Ghai, J.; Hertig, C.; Boistard, P.; Kahn, D. Cascade Regulation of nif Gene Expression in Rhizobium meliloti. Cell 1988, 54, 671–683. [Google Scholar] [CrossRef] [PubMed]
  177. Kaminski, P.A.; Elmerich, C. Involvement of fixLJ in the Regulation of Nitrogen Fixation in Azorhizobium caulinodans. Mol. Microbiol. 1991, 5, 665–673. [Google Scholar] [CrossRef] [PubMed]
  178. Kaminski, P.A.; Mandon, K.; Arigoni, F.; Desnoues, N.; Elmerich, C. Regulation of Nitrogen Fixation in Azorhizobium caulinodans: Identification of a fixK-like Gene, a Positive Regulator of nifA. Mol. Microbiol. 1991, 5, 1983–1991. [Google Scholar] [CrossRef]
  179. Emmerich, R.; Hennecke, H.; Fischer, H.M. Evidence for a Functional Similarity between the Two-Component Regulatory Systems RegSR, ActSR, and RegBA (PrrBA) in α-Proteobacteria. Arch. Microbiol. 2000, 174, 307–313. [Google Scholar] [CrossRef]
  180. Lindemann, A.; Moser, A.; Pessi, G.; Hauser, F.; Friberg, M.; Hennecke, H.; Fischer, H.M. New Target Genes Controlled by the Bradyrhizobium japonicum Two-Component Regulatory System RegSR. J. Bacteriol. 2007, 189, 8928–8943. [Google Scholar] [CrossRef] [Green Version]
  181. Anthamatten, D.; Scherb, B.; Hennecke, H. Characterization of a fixLJ-Regulated Bradyrhizobium japonicum Gene Sharing Similarity with the Escherichia coli fnr and Rhizobium meliloti fixK Genes. J. Bacteriol. 1992, 174, 2111–2120. [Google Scholar] [CrossRef]
  182. Cabrera, J.J.; Jiménez-Leiva, A.; Tomás-Gallardo, L.; Parejo, S.; Casado, S.; Torres, M.J.; Bedmar, E.J.; Delgado, M.J.; Mesa, S. Dissection of FixK2 Protein–DNA Interaction Unveils New Insights into Bradyrhizobium diazoefficiens Lifestyles Control. Environ. Microbiol. 2021, 23, 6194–6209. [Google Scholar] [CrossRef]
  183. Galinier, A.; Garnerone, A.M.; Reyrat, J.M.; Kahn, D.; Batut, J.; Boistard, P. Phosphorylation of the Rhizobium meliloti FixJ Protein Induces Its Binding to a Compound Regulatory Region at the fixK Promoter. J. Biol. Chem. 1994, 269, 23784–23789. [Google Scholar] [CrossRef]
  184. Lopez, O.; Morera, C.; Miranda-Rios, J.; Girard, L.; Romero, D.; Soberon, M. Regulation of Gene Expression in Response to Oxygen in Rhizobium etli: Role of FnrN in fixNOQP Expression and in Symbiotic Nitrogen Fixation. J. Bacteriol. 2001, 183, 6999–7006. [Google Scholar] [CrossRef] [Green Version]
  185. Ledbetter, R.N.; Garcia Costas, A.M.; Lubner, C.E.; Mulder, D.W.; Tokmina-Lukaszewska, M.; Artz, J.H.; Patterson, A.; Magnuson, T.S.; Jay, Z.J.; Duan, H.D.; et al. The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii: Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis. Biochemistry 2017, 56, 4177–4190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  186. Kim, C.H.; Helinski, D.R.; Ditta, G. Overlapping Transcription of the nifA Regulatory Gene in Rhizobium meliloti. Gene 1986, 50, 141–148. [Google Scholar] [CrossRef] [PubMed]
  187. Martínez, M.; Palacios, J.M.; Imperial, J.; Ruiz-Argüeso, T. Symbiotic Autoregulation of nifA Expression in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 2004, 186, 6586–6594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  188. Webb, I.U.C.; Xu, J.; Sanchez-Cañizares, C.; Karunakaran, R.; Ramachandran, V.K.; Rutten, P.J.; East, A.K.; Huang, W.E.; Watmough, N.J.; Poole, P.S. Regulation and Characterization of Mutants of fixABCX in Rhizobium leguminosarum. Mol. Plant-Microbe Interact. 2021, 34, 1167–1180. [Google Scholar] [CrossRef] [PubMed]
  189. Salazar, E.; Javier Díaz-Mejía, J.; Moreno-Hagelsieb, G.; Martínez-Batallar, G.; Mora, Y.; Mora, J.; Encarnación, S. Characterization of the NifA-RpoN Regulon in Rhizobium etli in Free Life and in Symbiosis with Phaseolus vulgaris. Appl. Environ. Microbiol. 2010, 76, 4510–4520. [Google Scholar] [CrossRef] [Green Version]
  190. Hauser, F.; Pessi, G.; Friberg, M.; Weber, C.; Rusca, N.; Lindemann, A.; Fischer, H.M.; Hennecke, H. Dissection of the Bradyrhizobium japonicum NifA+σ54 Regulon, and Identification of a Ferredoxin Gene (fdxN) for Symbiotic Nitrogen Fixation. Mol. Genet. Genomics 2007, 278, 255–271. [Google Scholar] [CrossRef]
  191. Klipp, W.; Reiländer, H.; Schlüter, A.; Krey, R.; Pühler, A. The Rhizobium meliloti fdxN Gene Encoding a Ferredoxin-like Protein Is Necessary for Nitrogen Fixation and Is Cotranscribed with nifA and nifB. Mol. Gen. Genet. 1989, 216, 293–302. [Google Scholar] [CrossRef]
  192. del Cerro, P.; Rolla-Santos, A.A.P.; Gomes, D.F.; Marks, B.B.; Pérez-Montaño, F.; Rodríguez-Carvajal, M.Á.; Nakatani, A.S.; Gil-Serrano, A.; Megías, M.; Ollero, F.J.; et al. Regulatory nodD1 and nodD2 Genes of Rhizobium tropici Strain CIAT 899 and Their Roles in the Early Stages of Molecular Signaling and Host-Legume Nodulation. BMC Genom. 2015, 16, 251. [Google Scholar] [CrossRef] [Green Version]
  193. Machado, D.; Pueppke, S.G.; Vinardel, J.M.; Ruiz-Sainz, J.E.; Krishnan, H.B. Expression of nodD1 and nodD2 in Sinorhizobium fredii, a Nitrogen-Fixing Symbiont of Soybean and Other Legumes. Mol. Plant-Microbe Interact. 1998, 11, 375–382. [Google Scholar] [CrossRef] [Green Version]
  194. Chen, X.C.; Feng, J.; Hou, B.H.; Li, F.Q.; Li, Q.; Hong, G.F. Modulating DNA Bending Affects NodD-Mediated Transcriptional Control in Rhizobium leguminosarum. Nucleic Acids Res. 2005, 33, 2540–2548. [Google Scholar] [CrossRef] [Green Version]
  195. Peck, M.C.; Fisher, R.F.; Long, S.R. Diverse Flavonoids Stimulate NodD1 Binding to nod Gene Promoters in Sinorhizobium meliloti. J. Bacteriol. 2006, 188, 5417–5427. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  196. Rossen, L.; Shearman, C.A.; Johnston, A.W.B.; Downie, J.A. The nodD Gene of Rhizobium leguminosarum Is Autoregulatory and in the Presence of Plant Exudate Induces the nodA,B,C Genes. EMBO J. 1985, 4, 3369–3373. [Google Scholar] [CrossRef] [PubMed]
  197. McIver, J.; Djordjevic, M.A.; Weinman, J.J.; Bender, G.L.; Rolfe, B.G. Extension of Host Range of Rhizobium leguminosarum bv. trifolii Caused by Point Mutations in nodD That Result in Alterations in Regulatory Function and Recognition of Inducer Molecules. Mol. Plant. Microbe. Interact. 1989, 2, 97–106. [Google Scholar] [CrossRef] [PubMed]
  198. Ferguson, S.; Major, A.S.; Sullivan, J.T.; Bourke, S.D.; Kelly, S.J.; Perry, B.J.; Ronson, C.W. Rhizobium leguminosarum bv. trifolii NodD2 Enhances Competitive Nodule Colonization in the Clover-Rhizobium Symbiosis. Appl. Environ. Microbiol. 2020, 86, e01268-20. [Google Scholar] [CrossRef]
  199. Honma, M.A.; Asomaning, M.; Ausubel, F.M. Rhizobium meliloti nodD Genes Mediate Host-Specific Activation of nodABC. J. Bacteriol. 1990, 172, 901–911. [Google Scholar] [CrossRef] [Green Version]
  200. Ayala-García, P.; Jiménez-Guerrero, I.; Jacott, C.N.; López-Baena, F.J.; Ollero, F.J.; del Cerro, P.; Pérez-Montaño, F. The Rhizobium tropici CIAT 899 NodD2 Protein Promotes Symbiosis and Extends Rhizobial Nodulation Range by Constitutive Nodulation Factor Synthesis. J. Exp. Bot. 2022, 73, 6931–6941. [Google Scholar] [CrossRef]
  201. Rodpothong, P.; Sullivan, J.T.; Songsrirote, K.; Sumpton, D.; Cheung, K.W.J.T.; Thomas-Oates, J.; Radutoiu, S.; Stougaard, J.; Ronson, C.W. Nodulation Gene Mutants of Mesorhizobium loti R7A-nodZ and nolL Mutants Have Host-Specific Phenotypes on Lotus spp. Mol. Plant-Microbe Interact. 2009, 22, 1546–1554. [Google Scholar] [CrossRef]
  202. Kelly, S.; Sullivan, J.T.; Kawaharada, Y.; Radutoiu, S.; Ronson, C.W.; Stougaard, J. Regulation of Nod Factor Biosynthesis by Alternative NodD Proteins at Distinct Stages of Symbiosis Provides Additional Compatibility Scrutiny. Environ. Microbiol. 2018, 20, 97–110. [Google Scholar] [CrossRef]
  203. Fellay, R.; Hanin, M.; Montorzi, G.; Frey, J.; Freiberg, C.; Golinowski, W.; Staehelin, C.; Broughton, W.J.; Jabbouri, S. nodD2 of Rhizobium sp. NGR234 Is Involved in the Repression of the nodABC Operon. Mol. Microbiol. 1998, 27, 1039–1050. [Google Scholar] [CrossRef] [Green Version]
  204. Loh, J.; Stacey, G. Nodulation Gene Regulation in Bradyrhizobium japonicum: A Unique Integration of Global Regulatory Circuits. Appl. Environ. Microbiol. 2003, 69, 10–17. [Google Scholar] [CrossRef] [Green Version]
  205. Acosta-Jurado, S.; Rodríguez-Navarro, D.-N.; Kawaharada, Y.; Rodríguez-Carvajal, M.A.; Gil-Serrano, A.; Soria-Díaz, M.E.; Pérez-Montaño, F.; Fernández-Perea, J.; Yanbo, N.; Alias-Villegas, C.; et al. Sinorhizobium fredii HH103 nolR and nodD2 Mutants Gain Capacity for Infection Thread Invasion of Lotus japonicus Gifu and Lotus Burttii. Environ. Microbiol. 2019, 21, 1718–1739. [Google Scholar] [CrossRef] [PubMed]
  206. Fujishige, N.A.; Lum, M.R.; De Hoff, P.L.; Whitelegge, J.P.; Faull, K.F.; Hirsch, A.M. Rhizobium Common nod Genes Are Required for Biofilm Formation. Mol. Microbiol. 2008, 67, 504–515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  207. Pérez-Montaño, F.; Jiménez-Guerrero, I.; Del Cerro, P.; Baena-Ropero, I.; López-Baena, F.J.; Ollero, F.J.; Bellogín, R.; Lloret, J.; Espuny, R. The Symbiotic Biofilm of Sinorhizobium fredii SMH12, Necessary for Successful Colonization and Symbiosis of Glycine max cv Osumi, Is Regulated by Quorum Sensing Systems and Inducing Flavonoids via NodD1. PLoS ONE 2014, 9, e0105901. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  208. Rumbaugh, K.P.; Sauer, K. Biofilm Dispersion. Nat. Rev. Microbiol. 2020, 18, 571–586. [Google Scholar] [CrossRef]
  209. Crespo-rivas, J.C.; Cuesta-berrio, L.; Ruiz-sainz, J.E. Exopolysaccharide Production by Sinorhizobium fredii HH103 Is Repressed by Genistein in a NodD1-Dependent Manner. PLoS ONE 2016, 11, e0160499. [Google Scholar] [CrossRef] [Green Version]
  210. Barnett, M.J.; Long, S.R. The Sinorhizobium meliloti SyrM Regulon: Effects on Global Gene Expression Are Mediated by syrA and nodD3. J. Bacteriol. 2015, 197, 1792–1806. [Google Scholar] [CrossRef] [Green Version]
  211. Cheng, H.P.; Walker, G.C. Succinoglycan Is Required for Initiation and Elongation of Infection Threads during Nodulation of Alfalfa by Rhizobium meliloti. J. Bacteriol. 1998, 180, 5183–5191. [Google Scholar] [CrossRef]
  212. Rodríguez-Navarro, D.N.; Rodríguez-Carvajal, M.A.; Acosta-Jurado, S.; Soto, M.J.; Margaret, I.; Crespo-Rivas, J.C.; Sanjuan, J.; Temprano, F.; Gil-Serrano, A.; Ruiz-Sainz, J.E.; et al. Structure and Biological Roles of Sinorhizobium fredii HH103 Exopolysaccharide. PLoS ONE 2014, 9, e115391. [Google Scholar] [CrossRef] [Green Version]
  213. Theunis, M.; Kobayashi, H.; Broughton, W.J.; Prinsen, E. Flavonoids, NodD1, NodD2, and Nod-Box NB15 Modulate Expression of the Y4wEFG Locus That Is Required for Indole-3-Acetic Acid Synthesis in Rhizobium sp. Strain NGR234. Mol. Plant-Microbe Interact. 2004, 17, 1153–1161. [Google Scholar] [CrossRef] [Green Version]
  214. Deakin, W.J.; Broughton, W.J. Symbiotic Use of Pathogenic Strategies: Rhizobial Protein Secretion Systems. Nat. Rev. Microbiol. 2009, 7, 312–320. [Google Scholar] [CrossRef]
  215. Barnett, M.J.; Toman, C.J.; Fisher, R.F.; Long, S.R. A Dual-Genome Symbiosis Chip for Coordinate Study of Signal Exchange and Development in a Prokaryote-Host Interaction. Proc. Natl. Acad. Sci. USA 2004, 101, 16636–16641. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  216. Acosta-Jurado, S.; Alias-Villegas, C.; Navarro-Gómez, P.; Almozara, A.; Rodríguez-Carvajal, M.A.; Medina, C.; Vinardell, J.M. Sinorhizobium fredii HH103 syrM Inactivation Affects the Expression of a Large Number of Genes, Impairs Nodulation with Soybean and Extends the Host-Range to Lotus japonicus. Environ. Microbiol. 2020, 22, 1104–1124. [Google Scholar] [CrossRef] [PubMed]
  217. Mulligan, J.T.; Long, S.R. A Family of Activator Genes Regulates Expression of Rhizobium meliloti Nodulation Genes. Genetics 1989, 122, 7–18. [Google Scholar] [CrossRef]
  218. Kiss, E.; Mergaert, P.; Olah, B.; Kereszt, A.; Staehelin, C.; Davies, A.E.; Downie, J.A.; Kondorosi, A.; Kondorosi, E. Conservation of nolR in the Sinorhizobium and Rhizobium Genera of the Rhizobiaceae Family. Mol. Plant-Microbe Interact. 1998, 11, 1186–1195. [Google Scholar] [CrossRef] [Green Version]
  219. Lee, S.G.; Krishnan, H.B.; Jez, J.M. Structural Basis for Regulation of Rhizobial Nodulation and Symbiosis Gene Expression by the Regulatory Protein NolR. Proc. Natl. Acad. Sci. USA 2014, 111, 6509–6514. [Google Scholar] [CrossRef] [Green Version]
  220. Cren, M.; Kondorosi, A.; Kondorosi, E. NolR Controls Expression of the Rhizobium meliloti Nodulation Genes Involved in the Core Nod Factor Synthesis. Mol. Microbiol. 1995, 15, 733–747. [Google Scholar] [CrossRef]
  221. del Cerro, P.; Rolla-Santos, A.A.P.; Valderrama-Fernández, R.; Gil-Serrano, A.; Bellogín, R.A.; Gomes, D.F.; Pérez-Montaño, F.; Megías, M.; Hungría, M.; Ollero, F.J. NrcR, a New Transcriptional Regulator of Rhizobium tropici CIAT 899 Involved in the Legume Root-Nodule Symbiosis. PLoS ONE 2016, 11, e0154029. [Google Scholar] [CrossRef]
  222. Vinardell, J.M.; Ollero, F.J.; Hidalgo, A.; Lopez-Baena, F.J.; Medina, C.; Ivanov-Vangelov, K.; Parada, M.; Madinabeitia, N.; Espuny Mdel, R.; Bellogin, R.A.; et al. NoIR Regulates Diverse Symbiotic Signals of Sinorhizobium fredii HH103. Mol. Plant-Microbe Interact. 2004, 17, 676–685. [Google Scholar] [CrossRef] [Green Version]
  223. Göttfert, M.; Grob, P.; Hennecke, H. Proposed Regulatory Pathway Encoded by the nodV and nodW Genes, Determinants of Host Specificity in Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 1990, 87, 2680–2684. [Google Scholar] [CrossRef] [Green Version]
  224. Loh, J.; Lohar, D.P.; Andersen, B.; Stacey, G. A Two-Component Regulator Mediates Population-Density-Dependent Expression of the Bradyrhizobium japonicum Nodulation Genes. J. Bacteriol. 2002, 184, 1759–1766. [Google Scholar] [CrossRef] [Green Version]
  225. Garcia, M.; Dunlap, J.; Loh, J.; Stacey, G. Phenotypic Characterization and Regulation of the nolA Gene of Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 1996, 9, 625–635. [Google Scholar] [CrossRef] [PubMed]
  226. Kondorosi, E.; Pierre, M.; Cren, M.; Haumann, U.; Buiré, M.; Hoffmann, B.; Schell, J.; Kondorosi, A. Identification of NoIR, a Negative Transacting Factor Controlling the nod Regulon in Rhizobium meliloti. J. Mol. Biol. 1991, 222, 885–896. [Google Scholar] [CrossRef] [PubMed]
  227. Kondorosi, E.; Gyuris, J.; Schmidt, J.; John, M.; Duda, E.; Hoffmann, B.; Schell, J.; Kondorosi, A. Positive and Negative Control of nod Gene Expression in Rhizobium meliloti Is Required for Optimal Nodulation. EMBO J. 1989, 8, 1331–1340. [Google Scholar] [CrossRef] [PubMed]
  228. Mueller, K.; Gonzalez, J.E. Complex Regulation of Symbiotic Functions Is Coordinated by MucR and Quorum Sensing in Sinorhizobium meliloti. J. Bacteriol. 2011, 193, 485–496. [Google Scholar] [CrossRef] [Green Version]
  229. Bittinger, M.A.; Milner, J.L.; Saville, B.J.; Handelsman, J. rosR, a Determinant of Nodulation Competitiveness in Rhizobium etli. Mol. Plant-Microbe Interact. 1997, 10, 180–186. [Google Scholar] [CrossRef] [Green Version]
  230. Janczarek, M.; Kutkowska, J.; Piersiak, T.; Skorupska, A. Rhizobium leguminosarum bv. trifolii RosR Is Required for Interaction with Clover, Biofilm Formation and Adaptation to the Environment. BMC Microbiol. 2010, 10, 284. [Google Scholar] [CrossRef] [Green Version]
  231. Jiao, J.; Wu, L.J.; Zhang, B.; Hu, Y.; Li, Y.; Zhang, X.X.; Guo, H.J.; Liu, L.X.; Chen, W.X.; Zhang, Z.; et al. MucR Is Required for Transcriptional Activation of Conserved Ion Transporters to Support Nitrogen Fixation of Sinorhizobium fredii in Soybean Nodules. Mol. Plant-Microbe Interact. 2016, 29, 352–361. [Google Scholar] [CrossRef]
  232. Acosta-Jurado, S.; Alias-Villegas, C.; Navarro-Gomez, P.; Zehner, S.; Del Socorro Murdoch, P.; Rodríguez-Carvajal, M.A.; Soto, M.J.; Ollero, F.J.; Ruiz-Sainz, J.E.; Göttfert, M.; et al. The Sinorhizobium fredii HH103 MucR1 Global Regulator Is Connected with the nod Regulon and Is Required for Efficient Symbiosis with Lotus burttii and Glycine max cv. Williams. Mol. Plant-Microbe Interact. 2016, 29, 700–712. [Google Scholar] [CrossRef] [Green Version]
  233. Janczarek, M. The Ros/MucR Zinc-Finger Protein Family in Bacteria: Structure and Functions. Int. J. Mol. Sci. 2022, 23, 15536. [Google Scholar] [CrossRef]
  234. Rachwał, K.; Matczyńska, E.; Janczarek, M. Transcriptome Profiling of a Rhizobium leguminosarum bv. trifolii rosR Mutant Reveals the Role of the Transcriptional Regulator RosR in Motility, Synthesis of Cell-Surface Components, and Other Cellular Processes. BMC Genom. 2015, 16, 1111. [Google Scholar] [CrossRef] [Green Version]
  235. Barnett, M.J.; Long, S.R. Identification and Characterization of a Gene on Rhizobium meliloti pSymA, syrB, That Negatively Affects syrM Expression. Mol. Plant Microbe Interact. 1997, 10, 550–559. [Google Scholar] [CrossRef] [Green Version]
  236. Li, M.-L.; Jiao, J.; Zhang, B.; Shi, W.-T.; Yu, W.-H.; Tian, C.-F. Global Transcriptional Repression of Diguanylate Cyclases by MucR1 Is Essential for Sinorhizobium-Soybean Symbiosis. mBio 2021, 12, e01192-21. [Google Scholar] [CrossRef] [PubMed]
  237. Sauviac, L.; Philippe, H.; Phok, K.; Bruand, C. An Extracytoplasmic Function Sigma Factor Acts as a General Stress Response Regulator in Sinorhizobium meliloti. J. Bacteriol. 2007, 189, 4204–4216. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  238. Bertram-Drogatz, P.A.; Quester, I.; Becker, A.; Puhler, A. The Sinorhizobium meliloti MucR Protein, Which Is Essential for the Production of High-Molecular-Weight Succinoglycan Exopolysaccharide, Binds to Short DNA Regions Upstream of exoH and exoY. Mol. Gen. Genet. 1998, 257, 433–441. [Google Scholar] [CrossRef] [PubMed]
  239. Schäper, S.; Wendt, H.; Bamberger, J.; Sieber, V.; Schmid, J.; Becker, A. A Bifunctional UDP-Sugar 4-Epimerase Supports Biosynthesis of Multiple Cell Surface Polysaccharides in Sinorhizobium meliloti. J. Bacteriol. 2019, 201, e00801-18. [Google Scholar] [CrossRef]
Genes 14 00274 g001 550
Figure 1. Adaptive evolution of rhizobium symbiosis. After acquiring the key symbiosis genes (nod and nif) by horizontal gene transfer (HGT), bacteria recipients confront ever-fluctuating environmental conditions and resources, and interactions with other soil microorganisms and plants. During the process of adaptive evolution, those bacteria, with the key symbiosis genes effectively integrated with the genomic background, survive the saprophytic life, colonize the host rhizoplane, communicate and establish a mutualistic symbiosis relationship with the host plant. In a strain–host-dependent manner, the nitrogen-fixing rhizobia, named bacteroids, are at either non-terminal or terminal differentiation status within symbiosome. nod, nodulation; nif, nitrogen fixation; NFR, nodulation factor receptor.
Figure 1. Adaptive evolution of rhizobium symbiosis. After acquiring the key symbiosis genes (nod and nif) by horizontal gene transfer (HGT), bacteria recipients confront ever-fluctuating environmental conditions and resources, and interactions with other soil microorganisms and plants. During the process of adaptive evolution, those bacteria, with the key symbiosis genes effectively integrated with the genomic background, survive the saprophytic life, colonize the host rhizoplane, communicate and establish a mutualistic symbiosis relationship with the host plant. In a strain–host-dependent manner, the nitrogen-fixing rhizobia, named bacteroids, are at either non-terminal or terminal differentiation status within symbiosome. nod, nodulation; nif, nitrogen fixation; NFR, nodulation factor receptor.
Genes 14 00274 g001
Genes 14 00274 g002 550
Figure 2. Genome innovations after receiving key symbiosis genes. The main patterns of rhizobial genome innovation in adaptive evolution include gene acquisition, loss, duplication, inactivation and variation, mediated by transposable elements and transient hyper-mutagenesis. Red star indicates a point mutation.
Figure 2. Genome innovations after receiving key symbiosis genes. The main patterns of rhizobial genome innovation in adaptive evolution include gene acquisition, loss, duplication, inactivation and variation, mediated by transposable elements and transient hyper-mutagenesis. Red star indicates a point mutation.
Genes 14 00274 g002
Genes 14 00274 g003 550
Figure 3. Working model for transcriptional integration of key symbiosis genes. Red arrow, positive regulation; green line, negative regulation. Solid lines indicate cases with molecular evidence. EPS, exopolysaccharide; APS, arabinose-containing polysaccharide; NO, nitric oxide. Sf, S. fredii; Sm, S. meliloti. For simplicity, functional genes in broad-host-range S. fredii are shown. The negative regulation of syrM by SyrB and positive regulation of nifA by FixJ are demonstrated in S. meliloti.
Figure 3. Working model for transcriptional integration of key symbiosis genes. Red arrow, positive regulation; green line, negative regulation. Solid lines indicate cases with molecular evidence. EPS, exopolysaccharide; APS, arabinose-containing polysaccharide; NO, nitric oxide. Sf, S. fredii; Sm, S. meliloti. For simplicity, functional genes in broad-host-range S. fredii are shown. The negative regulation of syrM by SyrB and positive regulation of nifA by FixJ are demonstrated in S. meliloti.
Genes 14 00274 g003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Liu, S.; Jiao, J.; Tian, C.-F. Adaptive Evolution of Rhizobial Symbiosis beyond Horizontal Gene Transfer: From Genome Innovation to Regulation Reconstruction. Genes 2023, 14, 274. https://doi.org/10.3390/genes14020274

AMA Style

Liu S, Jiao J, Tian C-F. Adaptive Evolution of Rhizobial Symbiosis beyond Horizontal Gene Transfer: From Genome Innovation to Regulation Reconstruction. Genes. 2023; 14(2):274. https://doi.org/10.3390/genes14020274

Chicago/Turabian Style

Liu, Sheng, Jian Jiao, and Chang-Fu Tian. 2023. "Adaptive Evolution of Rhizobial Symbiosis beyond Horizontal Gene Transfer: From Genome Innovation to Regulation Reconstruction" Genes 14, no. 2: 274. https://doi.org/10.3390/genes14020274

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop