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Review

Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae

1
Autonomous Department of Microbial Biology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland
2
Universidade do Vale do Taquari—UNIVATES, Rua Avelino Tallini, 171, 95900-000 Lajeado, RS, Brazil
3
Faculty of Agriculture and Life Sciences, Lincoln University, P.O. Box 84, Lincoln 7647, New Zealand
4
Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul. Av. Bento Gonçalves, 9500, Caixa Postal 15.053, 91501-970 Porto Alegre, RS, Brazil
*
Author to whom correspondence should be addressed.
Submission received: 31 January 2018 / Revised: 2 March 2018 / Accepted: 5 March 2018 / Published: 14 March 2018
(This article belongs to the Special Issue Genetics and Genomics of the Rhizobium-Legume Symbiosis)

Abstract

:
The legume tribe Genisteae comprises 618, predominantly temperate species, showing an amphi-Atlantic distribution that was caused by several long-distance dispersal events. Seven out of the 16 authenticated rhizobial genera can nodulate particular Genisteae species. Bradyrhizobium predominates among rhizobia nodulating Genisteae legumes. Bradyrhizobium strains that infect Genisteae species belong to both the Bradyrhizobium japonicum and Bradyrhizobium elkanii superclades. In symbiotic gene phylogenies, Genisteae bradyrhizobia are scattered among several distinct clades, comprising strains that originate from phylogenetically distant legumes. This indicates that the capacity for nodulation of Genisteae spp. has evolved independently in various symbiotic gene clades, and that it has not been a long-multi-step process. The exception is Bradyrhizobium Clade II, which unlike other clades comprises strains that are specialized in nodulation of Genisteae, but also Loteae spp. Presumably, Clade II represents an example of long-lasting co-evolution of bradyrhizobial symbionts with their legume hosts.

1. Introduction: Origin and Differentiation of the Tribe Genisteae

The Genisteae is one of the largest tribes within the legume family (Fabaceae) with ca. 618 species within 25 genera [1]. Most genera within the Genisteae show a preference for a temperate climate although several lupin (Lupinus spp.) species inhabit tropical areas in eastern Brazil [2,3,4]. These predominantly woody legumes thrive in a wide range of habitats, including coastal dunes, scrubland, sagebrush steppes, grasslands, mountain woodlands, and meadows. Genisteae (especially lupins) inhabit areas across a wide altitudinal range, extending from sea level to the upper elevation limit for plant growth, i.e., ca. 5,000 m [5]. Almost all of the Genisteae species tested can fix atmospheric nitrogen via symbiotic bacteria (general term ‘rhizobia’) in root nodules, and this gives them an advantage in low N soils if other factors are favourable for growth [6,7,8].
It has been estimated that the separation of the Genisteae and Crotalarieae took place in the Eocene ca. 41 million of years ago [9]. Evidence indicates that the formation of the two basal lineages, which later evolved into the extant genera Dichilus-Melolobium-Polhillia and Argyrolobium, occurred in southern Africa. Later, this tribe dispersed northward reaching the Mediterranean, where two other genera, Lupinus and Adenocarpus appeared. These events were followed by the emergence of the Cytisinae (nine genera) and Genistinae (eight genera) as predominant Genisteae groups in the Mediterranean [1,2,10]. Given that the time of separation of the genus Lupinus and the Cytisinae-Genistinae genera has been estimated at ca. 16 million years ago, the process of differentiation into the extant Genisteae genera may have been initiated in the Oligocene, albeit not later than in the early Miocene [11,12]. The environmental changes that are associated with the global climate cooling and growing aridification from the end of the Eocene may have played pivotal roles in the Genisteae speciation process [13,14]. Similarly, the mountain uplifts in the western parts of North and South America triggered replicate radiations in the genus Lupinus, resulting in the appearance of ca. 200 species with a great variety of morphological forms [12,15].
The amphi-Atlantic distribution of Genisteae species points to dispersal events having occurred across the Atlantic Ocean into the areas now comprising a distinct Fabaceae flora. The thesis of this review is that the complex evolutionary history of the Genisteae tribe is reflected by the diversity of rhizobium symbionts, with which it interacts. Indeed, seven out of the 16 authenticated rhizobial genera can nodulate particular Genisteae species (Figure 1). Thus, the objective of this work is to present a comprehensive phylogenetic and phylogeographic data concerning the rhizobia that nodulate this legume tribe.

2. The Genus Bradyrhizobium as a Predominant Group Infecting Genisteae Legumes

Bradyrhizobium strains were isolated from nodules of 30 out of the 33 lupin species listed in Table 1. Bradyrhizobium also occured in root nodules of 36 out of the 44 species of the remaining Genisteae genera (see Table 1). This indicates that Bradyrhizobium is a dominant rhizobium lineage nodulating this legume tribe although it is acknowledged that rhizobial symbionts have been characterized in only a fraction of Genisteae species [6,21], and nothing is known about rhizobial symbionts of 14, mostly monotypic genera.
The predominance of Bradyrhizobium strains among the rhizobia nodulating Genisteae spp. could be due to different factors, including their symbiotic potential that is responsible for their nodulation of a wide spectrum of Fabaceae spp. and their adaptability to various edaphic and climatic conditions, resulting in this genus having a broad geographical range [21,97]. Bradyrhizobia are common in soils in places where legumes are absent, which may explain the loss of nodulating ability by portions of rhizobial communities [98,99,100]. Indeed, Bradyrhizobium communities comprise both nodulating and non-nodulating bacteria, and the latter may even lack the capacity to fix nitrogen [101]. In phylogenetic trees, these non-nodulating, non-diazotrophic bradyrhizobia are often indistinguishable from symbiotic strains [100]. The lack of symbiotic properties may, however, be compensated by other attributes as revealed in bradyrhizobia inhabiting forest soil habitats that are rich in organic matter, whose genomes are enriched in loci involved in the catabolism of aromatic compounds [102].
The colonization of terrestrial environments by land plants had a profound impact on soil microbiota [103]. It is likely that Bradyrhizobium benefited from the expansion of land plants, developing a range of, mainly, mutualistic associations, which had been formed prior to the emergence of nitrogen-fixing symbiosis with Fabaceae. This explains the persistence of this genus in soils regardless of the presence of legumes [104,105,106]. Remarkably, members of this genus also play important roles in the nitrogen and sulphur cycles [64,107] and are also involved in a range of, mainly, mutualistic interactions with animals [108,109,110].

3. Bradyrhizobium japonicum and Related Species

Currently, the genus Bradyrhizobium comprises 50 species that have been proposed for strains originating from Europe, Northern Africa, South America, and Asia (see Supplementary Table S1). Despite recent efforts that were centred on the characterization of nonsymbiotic bradyrhizobia, type strains of 45 species are bacteria isolated directly from root or stem nodules of Fabaceae plants. Importantly, phylogenies of the 16S rRNA gene and several other core (nonsymbiotic) gene markers that are commonly used in MLSA (multiple locus sequence analysis) studies reveal two major branches in the genus Bradyrhizobium [111]. One of the branches, referred to as the B. japonicum supergroup or Bradyrhizobium group I, currently comprises 29 species, in addition to B. japonicum [112,113] (Figure 2 and Figures S1 and S2). The remaining B. elkanii supergroup or group II contains B. elkanii and 17 other species (Supplementary Table S1). Bradyrhizobium denitrificans and Bradyrhizobium oligotrophicum tend to group separately from the two supergroups. Apart from the 50 recognized species, Bradyrhizobium core gene phylogenies uncover many unnamed groups and single-strain lineages [28,114].
Earlier studies suggested that lupin bradyrhizobia are related to, or are often indistinguishable from, many soybean isolates in core gene phylogenetic trees [23,24,35,73,116]. Given that soybean and lupin bradyrhizobia belong to different cross-inoculation groups, two symbiovars (symbiovar genistearum for strains nodulating Genisteae and symbiovar glycinearum for microsymbionts of soybean) were proposed [35,117]. This division enabled the differentiation of related Bradyrhizobium strains by referring to their distinct symbiotic properties.
Studies that followed the publication of Barrera et al. [116] suggested that Bradyrhizobium isolates of Genisteae spp. showed phylogenetic affinity to B. japonicum, i.e., all of the isolates belonged to the Bradyrhizobium japonicum supergroup. This observation concerned the isolates originating from Genisteae plants growing in acidic or neutral soils in the Mediterranean and the Andes, the regions encompassing the principal centres of Genisteae differentiation [34,51,60,63,64,79,80]. Also, related Bradyrhizobium strains were detected among Genisteae isolates at the northern margin of this tribe’s geographical range in Belgium and Poland [48,58,65]. Likewise, B. japonicum-related strains were described in the western part of the United States among Bradyrhizobium isolates that were recovered from lupin and Acmispon spp. [70,118].
Although the prevalence of B. japonicum-related strains among Genisteae isolates was highlighted in earlier work, a closer examination revealed that a number of strains originating from more acid soils (pH <6) clustered separately with respect to B. japonicum species. Some strains infecting genistoid legumes in the Canary Islands were subsequently delineated as Bradyrhizobium canariense species [35]. It was then shown that B. canariense is widespread in the Mediterranean among Genisteae isolates, including several lupin species, Cytisus aeolicus, Genista aspalathoides, Retama sphaerocarpa, and Spartium junceum [25,34]. Further studies revealed that this species is also common in the western United States [118,119]. The western part of the United States constitutes a major centre of differentiation of the genus Lupinus, moreover, it is also inhabited by multiple Loteae species [12,120,121,122]. Also, B. canariense strains were reported in Poland and Iceland as well as in Western Australia in areas where lupin and serradella crops were cultivated [60,65,68]. The identification of B. canariense in areas located outside a Mediterranean climate appeared to be associated with acidic soils and suggested that soil pH is a primary factor determining the range of this species.
In the following years, Cytisus villosus was found to be infected by B. canariense and strains that belonged to two other species, which were broadly related to B. japonicum groups. These strains were formally described as Bradyrhizobium cytisi and Bradyrhizobium rifense [49,52]. This indicated that C. villosus, like most Genisteae so far studied, is nodulated by a broad range of Bradyrhizobium lineages. B. cytisi strains were also identified among both symbiotic and nonsymbiotic isolates which inhabit the rhizosphere of Acmispon strigosus (tribe Loteae) sampled across California [118].
Finally, a new species, B. lupini was proposed for strain USDA3051 that occupied a sister position with respect to B. canariense isolates in 16S rRNA and glnII-recA phylogenies [69]. This species seems to be common among Genisteae symbionts in the Mediterranean, which could be deduced from its presence together with B. canariense among recently recovered Bradyrhizobium symbionts of Lupinus micranthus and Lupinus luteus in Spain, Algeria, and Tunisia [78,79,80]. In addition to the dominant B. canariense–B. lupini group, the report of Msaddak et al. [79] unveiled two other, yet unnamed groups within the B. japonicum supergroup, one of which (Group II) showed an affinity to B. betae, a nonsymbiotic bacterium isolated from sugar beet root [123], while the other (Group V), depending on markers used (recA or glnII-recA-rrs) clustered with either B. rifense or Bradyrhizobium diazoefficiens spp.
It appears that B. canariense, B. cytisi, B. lupini, and B. rifense spp. prevail among the microsymbionts of Genisteae spp. in acidic and neutral soils. All of these species are probably adapted to poor, oligotrophic soils formed in a semi-arid-mediterranean climate. It is, thus, hardly surprising that these species were detected in regions that are known for a high diversity of Genisteae spp., i.e., in the Mediterranean, and in the western part of the United States. On the other hand, B. japonicum seems to be more common in temperate and subtropical climate, associating with legumes that are growing in more neutral soils [24,35,49,51,52,60,65,118,119].

4. Genisteae Isolates Related to Bradyrhizobium elkanii

Although most Bradyrhizobium isolates from Genisteae species belong to the B. japonicum supergroup, some cluster in the B. elkanii supergroup. Among Bradyrhizobium strains isolated from lupins native to Brazil, a strain originating from Lupinus paraguariensis aligned within the B. elkanii supergroup [60]. Related Bradyrhizobium strains were later described among root-nodule isolates that were recovered from Lupinus albescens plants [61]. L. albescens belongs to the same lupin group as L. paraguariensis, showing a similar range encompassing the northern part of Argentina, but also Uruguay, Paraguay, and southern Brazil [4,124]. Like other lupins, Lupinus albescens is adapted to poor, sandy soils, although it also inhabits more fertile soils. Out of the three major groups uncovered in core gene phylogenies, one group (Cluster III) [61], comprised strains from non-arenized-non-sandy soils that clustered in proximity to Bradyrhizobium pachyrhizi-B. elkanii spp. However, the remaining strains, referred to as Cluster I (contained strains from non-arenized soils) and Cluster II (contained strains from arenized-sandy soils) grouped separately within the B. japonicum superclade [61].
A considerable effort was centred on the investigation of rhizobial symbionts of Lupinus mariae-josephae. Unlike other lupins, most of which prefer acidic or neutral soils, L. mariae-josephae grows in alkaline, calcareous soils. This lupin species is also highly endemic—its geographic range is limited to small populations, scattered across the Valencia province in Eastern Spain [125]. The characterization of L. mariae-josephae rhizobium isolates originating from soil samples collected at a single location revealed a substantial level of diversity. All Bradyrhizobium strains isolated in this work grew very slowly, and clustered within the B. elkanii supergroup [64]. In a subsequent study, a much larger number of L. mariae-josephae isolates (103 strains) were characterized, from plants sampled at four principal locations of its natural occurrence. Phylogenies based on combined sequences of atpD, glnII, and recA genes uncovered six major groups (group I-VI), all were confined to the B. elkanii supergroup [75]. Three closely related L. mariae-josephae isolates (each belonging to group I) were then subjected to detailed molecular and phenotypic analyses, which resulted in the description of a new species, Bradyrhizobium valentinum [76]. The systematic status of isolates representing the remaining groups (groups II-VI) is unclear, however, these strains do not group together with known Bradyrhizobium species, and thus likely represent separate species within this genus.
Lupin is not the only Genisteae genus infected by strains within the B. elkanii supergroup. In fact, strains showing phylogenetic affinity to B. elkanii were previously reported in Sicily, among the isolates nodulating Calicotome spinosa and G. aspalathoides [34]. In addition, B. elkanii-related strains were detected in nodules of Retama raetam and R. sphaerocarpa, in seven distinct ecological-climatic areas of north-eastern Algeria [92]. In another study, all of the Bradyrhizobium strains isolated in Morocco and Spain from R. sphaerocarpa and Retama monosperma clustered in the B. elkanii supergroup. Here, isolates were classified as a new species, Bradyrhizobium retamae. In the phylogenetic tree based on concatenated sequences of recA, atpD, and glnII genes, B. retamae occupied a sister albeit distinct position with respect to Bradyrhizobium lablabi and Bradyrhizobium jicamae species [88]. Notably, B. retamae was the first Bradyrhizobium species nodulating Genisteae plants with an affinity to the B. elkanii supergroup. Later, for Bradyrhizobium isolates that were recovered from R. sphaerocarpa plants growing in different soil and climatic conditions in Spain, roughly one-third of the isolates clustered in the B. japonicum supergroup, whereas the remaining strains grouped in the B. elkanii cluster [93]. Strains belonging to these two major groups of Bradyrhizobium were also detected among the symbionts of Genista versicolor, which is endemic to the Sierra Nevada National Park in Spain [59]. It is emphasized that a significant proportion of the strains that were isolated in the studies described formed phylogenetic lines clearly distinct from the known Bradyrhizobium species, which indicates a very high level of diversity within Genisteae symbionts in the Mediterranean.

5. Phylogeny of Symbiotic Loci of Genisteae-Nodulating Bradyrhizobium Strains

The analysis of nodA, nodC, as well as nifD and nifH gene sequences revealed a high level of diversity within the genus Bradyrhizobium [21,60,70,82,114,126,127,128,129,130,131]. In recently published phylogenies of nodA and nifD symbiotic genes, Bradyrhizobium strains formed 16 major groups, referred to as Clade I–Clade XVI [28]. Following this classification scheme, Bradyrhizobium strains nodulating Genisteae spp. cluster in the nodA tree in Clade I, Clade II, Clade III, Clade IV, Clade VII, Clade XI, Clade XIII, Clade XV, and Clade XVI [60,61,65,76,114,132]. In the current work, in phylogenies that were based on sequences of nodA and nifD genes, Clade V is formed solely by strains originating from Australian native legumes [114]. Some South American strains that previously were assigned to Clade V were transferred to subclade III.4 of Clade III, which in symbiotic gene trees cluster separately with respect to the Australian strains (Figure 3 and Figure S3).
Clade II, also referred to as the lupin clade, was the first described symbiotic nodA gene group comprising Bradyrhizobium isolates from Genisteae spp. [132]. Further work revealed that Clade II is a dominant group among Genisteae bradyrhizobia in Europe and the Mediterranean [21,39,65,73,78,79,80]. Strains belonging to this group were also detected among Bradyrhizobium isolates that were recovered from Lupinus spp. endemic to the Andes, but not in lupin species that are native to the eastern part of Brazil [60,61]. Clade II strains also prevail among lupin isolates in North America, especially, in the western part of the United States [70,71,82,134].
The geographical range of Clade II overlaps with the distribution of Genisteae genera in the Mediterranean and the western part of the Americas. The exception is southern Africa where the four basal genera (Argyrolobium, Dichilus, Melolobium, and Polhillia) have their centres of divergence [2]. Presumably, these South-African genera are not nodulated by Clade II bradyrhizobia, as suggested by two recent studies [27,28]. However, this opinion should be taken with caution, given that only a limited number of Genisteae isolates from these four genera have so far been characterized in South Africa. Thus, we cannot exclude the possibility that early stages of Clade II differentiation took place in southern Africa, being connected to the divergence of the basal Genisteae genera [135]. In South Africa, Clade II bradyrhizobia have been detected as symbionts of Lupinus angustifolius which is exotic to this region. However, these strains were similar to European bradyrhizobia and it was assumed that they had been accidentally brought from Europe together with soil-contaminated lupin seeds [68].
Notably, the geographic range of Clade II to a large extent overlaps with the range of the Loteae tribe (Table S2). This legume tribe has its major centre of divergence in the Mediterranean, extending to western Asia, while the secondary centre of divergence is in the western part of the United States [120,121]. Although the Loteae plants are infected, primarily, by Mesorhizobium strains, at least some genera, e.g., the genus Acmispon in the western part of the United States, and the genus Ornithopus (serradella) in Europe show preference for Clade II bradyrhizobia [65,71,118,134]. Actually, Serradella species that are known to establish highly specific symbiosis with their rhizobial partners have, for a long time, been used as surrogate hosts for isolation of effective strains nodulating lupins and other Genisteae spp. [136,137]. Out of the five Ornithopus species, four are native to the Mediterranean and/or western and central Europe, whereas Ornithopus micranthus is endemic to south-eastern Brazil, north-eastern Argentina and Uruguay [121]. Evidently, Clade II bradyrhizobia are the preferred symbionts of pink (Ornithopus sativus) and yellow serradella (Ornithopus compressus) species [35,64,65,68]. Much less is known about rhizobia nodulating Ornithopus perpusillus and Ornithopus pinnatus, and the south American O. micranthus sp., although the two European species seem to be also nodulated by Clade II Bradyrhizobium symbionts [48,65,138]. Like the four European species, O. micranthus is infected by Bradyrhizobium strains, however, nothing is known about the phylogenetic affinities of symbiotic loci in these strains [139].
It has been assumed that Clade II Bradyrhizobium has evolved in the Mediterranean and that this process has been somehow connected to the diversification of Genisteae [60]. In fact, when considering the number of Genisteae genera, the Mediterranean is the major (although not primary) centre of divergence of this tribe [10,140,141]. The idea of coevolution of bradyrhizobia with Genisteae diversifying in the Mediterranean seems plausible as bradyrhizobia originating from this region occupy the outermost position within the nifD tree shown in Figure S4. However, the majority of Clade II nifD sequences form two internal branches, one of which comprises the “European” while the other the “American” isolates (Figure S4). It has to be mentioned that the “European” branch also includes bradyrhizobia that were recovered in the United States [44] and all American strains in this branch originate from Cytisus scoparius and are indistinguishable from European Clade II isolates. This is in line with a recent study [134], which revealed that European Genisteae legumes introduced to the United States show preference for “European” Clade II bradyrhizobia even in areas inhabited by native legumes nodulated by “American” Clade II strains.
Importantly, this branching pattern corroborates the assumption that the Mediterranean is the initial centre of Clade II divergence whereas the western part of the United States is a secondary centre of divergence (Figure 3 and Figure S4). The higher specificity of symbiosis with the Loteae and the fact that geographic ranges of these two tribes largely overlap indicate that the Loteae may have been a major driver in Clade II evolution. According to the “Jack-of-all-trades is master of none” hypothesis, one can assume that a specialist (in this case Clade II strains) shows much better ‘fitness’ with respect to a “generalist” group nodulating Genisteae [71]. Thus, the ability to form highly effective symbiosis with the two legume tribes (one of which is more restrictive) could explain the dissemination of Clade II bradyrhizobia across the Mediterranean and temperate parts of the Americas.
Clade III is the most heterogeneous and cosmopolitan group and it also shows the broadest host range amongst Bradyrhizobium major clades (see Table S2). In the nifD phylogenetic tree, this branch forms four, well supported inner branches referred to as III.1, III.2, III.3, and III.4 (see Figure 3 and Figure S3). Subclade III.1 comprises only two isolates from Senegal, while the remaining three subgroups are more numerous, containing bradyrhizobia originating from Genisteae (from American lupins) (Table S2). Unlike the cosmopolitan subclade III.3, Bradyrhizobium strains belonging to subclades III.2 and III.4 were detected solely in the Americas. Nevertheless, several independent reports indicate that these two groups are probably common among rhizobia infecting lupins that are native to South and North America [21,60,61,70,82]. In III.2 and III.4 subclades, bradyrhizobia originate from legumes belonging to 10 and 9 tribes, respectively, which implies that, although they have diversified in the Americas, there is a lack of evidence supporting a lasting co-evolution with Genisteae spp. (Table S2).
The largest and most cosmopolitan subclade III.3 comprises eight internal branches (III.3A-III.3H) (Figure 3). Bradyrhizobium strains originating from Genisteae are confined to branches III.3B, III.3C, and III.3G. The small branch III.3G contains identical nifD sequences from C. scoparius isolates originating from Spain and the United States, which suggests that this group may have a Mediterranean origin. In the predominantly Australian branch III.3B, four isolates originating from Spain (two strains from R. sphaerocarpa) and Portugal (two strains, one from introduced Acacia longifolia and one from native Cytisus grandiflorus) form an outer group. It cannot, however, be excluded that these strains, albeit originally from Australia, have extended their host range to the native Mediterranean genera [95]. On the other hand, the diverse branch III.C contains a single isolate from Argyrolobium rupestre (strain Arg105), originating from South Africa [28]. The branch III.C comprises the isolates from sub-Saharan Africa, southern Asia, Australia, as well as from Central and North Americas, therefore it can rightly be regarded as a cosmopolitan group.
Bradyrhizobium Clade IV strains nodulating Genisteae have been reported in the Mediterranean (in Algeria, Croatia, Italy, and Spain), among rhizobial symbionts of C. spinosa, G. aspalathoides, Laburnum anagyroides, L. mariae-josephae, R. monosperma, R. sphaerocarpa, and S. junceum [21,34,75,76]. Some of the isolates from L. mariae-josephae and Retama spp. belong to B. valentinum and B. retamae. Moreover, Clade IV bradyrhizobia were assigned to Bradyrhizobium icense, B. lablabi, Bradyrhizobium namibiense, Bradyrhizobium paxllaeri, and some as yet unnamed lineages (see Supplementary data Tables S1 and S2). This group shows a broad geographic range encompassing mainly arid and semi-arid parts of Africa, Asia, Australia, Europe, and the Americas [68,114,129,130,142].
Highly differentiated Clade VII comprises B. americanum, Bradyrhizobium ingae, B. iriomotense, B. manausense, and B. stylosanthis spp. (Supplementary data Table S1). The majority of Clade VII strains originate from North and South America, while some were isolated in south-east Asia (southern China, the Island of Okinawa, Thailand, and the Philippines) [143,144,145,146,147]. Given that Clade VII bradyrhizobia from south-east Asia occupy internal positions relative to the American strains, it can be assumed that this cluster has evolved in the Americas, possibly, in an area of hot and humid tropical climate. This can be deduced from the fact that this clade is common in tropical-humid (but not arid) parts of Central and South America, and the Caribbean [21,53,60,70,82]. Clade VII strains nodulate a broad range of, mainly, tropical legumes (Table S1), however, some strains originate from lupins that are endemic to south-eastern Brazil [60,61]. Like Clade VII, Clade XVI seems to be an American group. So far, Bradyrhizobium strains belonging to Clade XVI have been described among legume isolates from Costa Rica, Honduras, the Caribbean (the Island of Guadeloupe), and the United States [53,148,149,150]. Unlike Clade XVI strains that were isolated in Central America and the Caribbean which do not originate from Genisteae spp., all Clade XVI strains from the United States originate from Lupinus lepidus, Lupinus perennis, and A. strigosus [70].
In the nodA tree (Figure S3), Bradyrhizobium strains Arg62, Arg68, and Arg33 from the South African Argyrolobium sericeum cluster in Clade XV. This clade also comprises the isolates from Lotononis and Pearsonia spp.—the Crotalarieae genera endemic to southern Africa [1,28,151]. The grouping of these strains in the same cluster is not surprising considering the overlapping geographical ranges of the southern Genisteae genera and the Crotalarieae tribe in South Africa [27]. However, in the nifD tree (Figure 3), strain Arg62 groups within Clade III.3, while Arg33 has been included in Clade IV. This indicates that although nodA and nifD phylogenies are essentially congruent, there are some differences, most likely reflecting distinct evolutionary histories of these two symbiotic genes in particular clades.
Clade I has been described as a predominant group in temperate and tropical Australia, where this group of bradyrhizobia nodulate native legumes, primarily, members of the endemic Bossiaeeae-Mirbelieae tribes and the genus Acacia [68,114,132]. In addition, Clade I strains have been isolated outside this continent, usually from the introduced Australian Acacia species [95,152,153]. This implies that Clade I bradyrhizobia may have been co-introduced with Acacia spp. and that in their new habitats they out-competed the indigenous rhizobia in the process of nodulation of their native hosts. Importantly, Clade I bradyrhizobia were also reported in nodules of C. grandiflorus, L. micranthus, and Ulex europaeus (gorse), which can be regarded as an extension of Clade I strains’ range on native-Mediterranean hosts. This phenomenon of rapid adaptation to new legume hosts may be widespread in the genus Bradyrhizobium [80,95,154]. This can be concluded from the identification of other, presumably Australian groups, e.g. group III.3B (which has been mentioned above) as well as an enigmatic Clade XVIII (Figure 3). Clade XVIII is a phylogenetically distinct group, comprising nifD sequences (there is a lack of nod gene sequences for Clade XVIII in the GenBank database) which originate from Bradyrhizobium strains isolated from A. longifolia and A. saligna in Australia and A. saligna and Cytisus sp. in Portugal [155]. Although the Mediterranean origin of this group cannot be excluded, the association with Australian Acacia spp. in both Australia and in areas in Portugal that are infested by these mimosoid spp. strongly suggests that Clade XVIII has an Australian origin.

6. Fast-Growing Rhizobium Genera

In comparison to the genus Bradyrhizobium, much less is known about members of the fast-growing rhizobial genera that infect Genisteae plants. Nonetheless, work over the last 10 years has shown that Genisteae legumes are nodulated by both highly cosmopolitan genera as well as genera that occur rarely among rhizobial isolates.
The genera Mesorhizobium, Rhizobium, and Ensifer (=Sinorhizobium), along with Bradyrhizobium are regarded as the most cosmopolitan rhizobium groups due to their ability to nodulate a broad range of Fabaceae spp. [156]. However, available data indicate that these genera are not common symbionts of Genisteae species [156]. Mesorhizobium strains classified as M. loti nodulate with lupins, although they show a preference for Lotus spp., which, presumably, are their primary hosts. It seems, however, that M. loti is not the only Mesorhizobium species that is involved in root-nodule symbiosis with Genisteae. Recently, two Mesorhizobium strains isolated from North American lupins, one from Lupinus densiflorus, and the other from L. succulentus, were shown to have a phylogenetic affinity to Mesorhizobium ciceri—a species that until now has not been implicated in the symbiosis with genistoid legumes [157]. In the Mediterranean, Mesorhizobium strains nodulate with native Genisteae spp, including Genista saharae, R. raetam, Teline monspessulana, and three lupin species (see Table 1). However, only limited information is available about these strains especially their symbiotic loci [34,55,56,62]. Mesorhizobium strains were also recovered from root nodules of Argyrolobium lunare and A. velutinum in the Core Cape Subregion (the Fynbos) of South Africa. Interestingly, these isolates formed discrete branches on core gene and nodA phylogenetic trees, grouping together with strains nodulating Asphalathus spp. (tribe Crotalarieae), which indicates that these two genera are nodulated by closely related bacteria that may potentially form a single cross-inoculation group [27].
Although the isolation of Rhizobium strains from lupin nodules has been reported in a number of studies, to our knowledge the symbiotic effectiveness of these isolates on lupins has not been confirmed. Usually, strains described as Rhizobium, have not been sufficiently characterised at the molecular level or authentication tests on their original host have not been performed or proved negative [157,158,159]. For example, strain H 13-3 originally described as Rhizobium lupini, following more detailed analysis was reclassified as Agrobacterium sp. [160]. Also, two strains recently isolated from lupin species native to Morocco have been assigned to the genus Rhizobium based on the ARDRA analysis [161]. These strains require further characterization of selected core and symbiotic marker genes [111]. Nonetheless, there are reports indicating that members of the genus Rhizobium nodulate other Genisteae genera, including Adenocarpus spp., Argyrolobium uniflorum, C. spinosa, Cytisus spp. Genista spp., and R. raetam (see Table 1). However, as in the case of the lupin isolates, more detailed molecular characterization and authentication tests are needed to confirm their phylogenetic affinity and their symbiotic properties.
Ensifer (Sinorhizobium) strains have not been described in lupin nodules, which contrasts with several other Genisteae spp. that are nodulated by rhizobia belonging to this genus (see Table 1). For instance, Argyrolobium uniflorum and Genista saharae are infected exclusively by fast-growing rhizobium genera, in particular, Ensifer [29,30,31,55,56,91]. In the case of these two species, the predominance of Ensifer as symbiont may be caused by specific requirements of these particular Genisteae species, favouring this rhizobium genus. However, it may be related to the high salt and arid habitat of the legumes, which may favour Ensifer in comparison to other rhizobial genera [162].
In addition, to the four genera described above, Genisteae spp. are infected by three other fast-growing rhizobial genera. In 2005, Trujillo and co-workers described rhizobia classified as Ochrobactrum lupini, which were isolated in Argentina from native Lupinus honoratus [72]. Prior to this finding, this genus was assumed to comprise opportunistic pathogens and saprophytes living in soil and animal faeces [163]. Subsequently, Ochrobactrum strains were isolated in Spain from nodules of C. scoparius (Scotch broom) plants [47]. Also, Ochrobactrum rhizobia were described in root nodules of Acacia mangium in the Philippines and Thailand [164], as well as in nodules of Cicer arietinum in Pakistan [165].
The genus Microvirga which comprises soil and water saprophytes was included in the alpha-proteobacterial lineage of root-nodule bacteria only in 2012, although the first symbiotic strains were detected in nodules of Lupinus texensis in 2007 [87,166,167]. Recently, Microvirga strains were isolated from L. micranthus and L. luteus spp. in Tunisia, as well as from L. subcarnosus in the United States [79,80,157]. This indicates that Microvirga may be rather common among lupin isolates in both the Mediterranean and North America. It is unclear if Microvirga can nodulate Genisteae spp. other than lupins, however, aside from lupins, rhizobia belonging to this genus were also isolated from Listia angolensis in Zambia, Vigna sp. in Brazil, and from Vicia alpestris in the Caucasus, Russia [87,168,169].
The Phyllobacterium genus comprises bacteria that are well-known for their epiphytic and endophytic associations with plants [170]. Some phyllobacteria fix nitrogen, therefore, the occurrence of root-nodule bacteria in this genus is not unexpected [161]. Indeed, an isolate classified as Phyllobacterium trifolii was found nodulating white lupin (Lupinus albus) in addition to its original white clover (Trifolium repens) host. However, P. trifolii strains formed ineffective nodules on white lupins, which indicated that lupins are not their natural hosts [171]. Nonetheless, Phyllobacterium rhizobia were described in Tunisia, in the nodules of L. micranthus [79]. Prior to this finding, Phyllobacterium strains were identified as symbionts of Adenocarpus hispanicus, Genista saharae and G. tinctoria, R. sphaerocarpa, and S. junceum (see Table 1). This genus may be specialized in the nodulation of genistoid legumes, however, it cannot be excluded that some of the Phyllobacterium isolates are endophytic bacteria that are lacking the ability to form nodules [172].
The data discussed indicate that although members of the genera Microvirga, Ochrobactrum, and Phyllobacterium nodulate various legume-hosts (including some members of the tribe Genisteae), and show broad geographical range, they most likely prevail among root-nodule bacteria in only discrete environments [156]. While all the Genisteae isolates characterised so far are α–rhizobia, this may change if authentication tests confirm symbiotic-nitrogen-fixing properties of recently described lupin isolates belonging to the genus Burkholderia [157].

7. Summary

The high level of diversity shown by Genisteae microsymbionts most likely reflects the complex evolutionary history of this legume tribe, which can be linked to long-distance dispersal and radiation events in southern Africa, the Mediterranean, and the Americas. One can assume that following the dispersal, rhizobial communities which were encountered in newly colonized areas often differed from rhizobial symbionts in the areas of Genisteae primary occurrence. The lack of appropriate rhizobial symbionts is often perceived as an obstacle that is impeding the dispersal of particular Fabaceae spp. [173]. However, Fabaceae spp. may interact with indigenous rhizobia forming less efficient symbiosis [174,175]. This “opportunistic” strategy of the two symbiotic partners results in a broader range of rhizobial symbionts, and may explain why certain rhizobial genera cannot be regarded as optimal partners of their legume hosts. In the case of Genisteae spp., the necessity of adaptation to local rhizobia is manifested by the formation of symbiotic associations with members of at least seven rhizobial genera, out of the 16 genera that are known for their symbiotic nitrogen-fixation ability.
Despite the progress that has been made in the last ten years in research focused on the fast-growing genera nodulating Genisteae spp., the current knowledge concerning this diverse group of rhizobia lags significantly behind the understanding of the symbiosis that is established between Genisteae spp. and their Bradyrhizobium symbionts. Nonetheless, these efforts revealed three new genera, out which Microvirga appears to comprise effective symbionts of at least some lupin species in North America and the Old World [79,80,167].
Unlike the fast-growing rhizobia, the genus Bradyrhizobium appears to be a dominant group nodulating the majority of Genisteae species. Genisteae-nodulating bradyrhizobia cluster within both B. japonicum and B. elkanii superclades, belonging to seven distinct species, and a large number of partially characterized lineages. In symbiotic gene phylogenies, Bradyrhizobium symbionts are scattered in several distinct groups, each comprising strains originating from phylogenetically distinct legumes. This indicates that the capacity for nodulation of Genisteae spp. appeared independently in various symbiotic gene clades, and that the adaptation towards nodulation of this tribe was not a multi-step process. We assume that this process could be related to the loss of the noeI gene, which is involved in the methylation of the fucose moiety at the Nod factor reducing end [176], and which seems to be in a form of pseudogene in Bradyrhizobium strains nodulating Genisteae whose genomic sequences are available [60,73,86,177]. The exception could be Bradyrhizobium Clade II, which unlike other clusters comprises strains that appear to be specialized in the nodulation of Genisteae, but also Loteae species. It can be presumed that Clade II is an example of the long co-evolution process of Genisteae and their bradyrhizobial symbionts, although the tribe Loteae also may have played an important role.

Supplementary Materials

The following are available online at https://0-www-mdpi-com.brum.beds.ac.uk/2073-4425/9/3/163/s1. Figure S1: ML phylogeny of Bradzrhyiobium glnII gene; Figure S2: ML phylogeny of Bradzrhyiobium recA gene; Figure S3: ML phylogeny of Bradzrhyiobium nodA gene; Figure S4: The portion of nifD ML phylogenetic tree referring to Bradyrhizobium Clade II branch; Table S1: The list of Bradyrhizobium species; Table S2: The list of Legume genera belonging to nifD gene Clades that comprise Genisteae Bradyrhizobium symbionts.

Acknowledgments

This work was supported by a grant UMO-2014/15/B/NZ8/00259 (T.S.&J.B.) from The National Science Centre (NCN).

Author Contributions

T.S., J.B., M.A. and L.M.P.P. were responsible for the writting of the manuscript. J.B. and C.E.G. carried out phylogenetic analyses. J.B. was involved in text editing and submitting processes.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Cardoso, D.; Pennington, R.T.; de Queiroz, L.P.; Boatwright, J.S.; Van Wyk, B.-E.; Wojciechowski, M.F.; Lavin, M. Reconstructing the deep-branching relationships of the papilionoid legumes. S. Afr. J. Bot. 2013, 89, 58–75. [Google Scholar] [CrossRef]
  2. Polhill, R.M.; Van Wyk, B.E. Genisteae. In Legumes of the World; Lewis, G., Schrire, B., Mackinder, B., Lock, M., Eds.; Royal Botanic Gardens, Kew: Richmond, UK, 2005; pp. 283–297. ISBN 1-900-34780-6. [Google Scholar]
  3. Monteiro, R.; Gibbs, P.E. A taxonomic revision of the unifoliate species of Lupinus (Leguminosae) in Brazil. Notes Royal Bot. Gard. Edin. 1986, 44, 71–104. [Google Scholar]
  4. Iganci, J.R.V.; Miotto, S.T.S. Lupinus. In Lista de Espécies da Flora do Brasil; Jardim Botânico do Rio de Janeiro: Rio de Janeiro, Brazil, 2015. [Google Scholar]
  5. Nevado, B.; Atchison, G.W.; Hughes, C.E.; Filatov, D.A. Widespread adaptive evolution during repeated evolutionary radiations in New World lupins. Nat. Commun. 2016, 7, 1–9. [Google Scholar] [CrossRef] [PubMed]
  6. Sprent, J.I. Nodulation in a Taxonomic Context. In Legume Nodulation: A Global Perspective; Wiley-Blackwell Publisher: Oxford, UK, 2009; pp. 1–33. ISBN 9781405181754, 9781444316384. [Google Scholar]
  7. Andrews, M.; Raven, J.A.; Lea, P.J. Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann. Appl. Biol. 2013, 163, 174–199. [Google Scholar] [CrossRef]
  8. Raven, J.A.; Andrews, M. Evolution of tree nutrition. Tree Physiol. 2010, 30, 1050–1071. [Google Scholar] [CrossRef] [PubMed]
  9. Lavin, M.; Herendeen, P.S.; Wojciechowski, M.F. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst. Biol. 2005, 54, 575–594. [Google Scholar] [CrossRef] [PubMed]
  10. Ainouche, A.K.; Bayer, R.J.; Cubas, P.; Misset, M.T. Phylogenetic relationships within tribe Genisteae (Papilionaceae) with special reference to the genus Ulex. In Advances in Legume Systematics; Klitgaard, B.B., Bruneau, A., Eds.; Higher Level Systematics, Royal Botanic Gardens, Kew: London, UK, 2003; Part 10; pp. 239–252. [Google Scholar]
  11. Cubas, P.; Pardo, C.; Hikmat, T.; Castroviejo, S. Phylogeny and evolutionary diversification of Adenocarpus DC. (Leguminosae). Taxon 2010, 59, 720–732. [Google Scholar]
  12. Drummond, C.S.; Eastwood, R.J.; Miotto, S.T.S.; Hughes, C.E. Multiple Continental Radiations and Correlates of Diversification in Lupinus (Leguminosae): Testing for Key Innovation with Incomplete Taxon Sampling. Syst. Biol. 2012, 61, 443–460. [Google Scholar] [CrossRef] [PubMed]
  13. Zachos, J.; Pagani, M.; Sloan, L.; Thomas, E.; Billups, K. Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present. Science 2001, 292, 686–693. [Google Scholar] [CrossRef] [PubMed]
  14. Fiz-Palacios, O.; Valcárcel, V. From Messinian crisis to Mediterranean climate: A temporal gap of diversification recovered from multiple plant phylogenies. Persp. Plant Ecol. Evol. Syst. 2013, 15, 130–137. [Google Scholar] [CrossRef]
  15. Hughes, C.; Eastwood, R. Island radiation on a continental scale: Exceptional rates of plant diversification after uplift of the Andes. Proc. Natl. Acad. Sci. USA 2006, 103, 10334–10339. [Google Scholar] [CrossRef] [PubMed]
  16. Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res. 2004, 32, 1792–1797. [Google Scholar] [CrossRef] [PubMed]
  17. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 2013, 30, 2725–2729. [Google Scholar] [CrossRef] [PubMed]
  18. Drummond, A.J.; Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7, 214. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Darriba, D.; Taboada, G.L.; Doallo, R.; Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 2012, 9, 772. [Google Scholar] [CrossRef] [PubMed]
  20. Molecular Evolution, Phylogenetics and Epidemiology. FigTree. version 1.3.1. Available online: http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 30 January 2018).
  21. Parker, M.A. The Spread of Bradyrhizobium Lineages Across Host Legume Clades: from Abarema to Zygia. Microb. Ecol. 2015, 69, 630–640. [Google Scholar] [CrossRef] [PubMed]
  22. Abdelmoumen, H.; Filali-Maltouf, A.; Neyra, M.; Belabed, A.; Missbah El Idrissi, M. Effect of high salts concentrations on the growth of rhizobia and responses to added osmotica. J. Appl. Microbiol. 1999, 86, 889–898. [Google Scholar] [CrossRef]
  23. Jarabo-Lorenzo, A.; Pérez-Galdona, R.; Donate-Correa, J.; Rivas, R.; Velázquez, E.; Hernández, M.; Temprano, F.; Martínez-Molina, E.; Ruiz-Argüeso, T.; León-Barrios, M. Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst. Appl. Microbiol. 2003, 26, 611–623. [Google Scholar] [CrossRef] [PubMed]
  24. Vinuesa, P.; Silva, C.; Werner, D.; Martinez-Romero, E. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol. Phylogenet. Evol. 2005, 34, 29–54. [Google Scholar] [CrossRef] [PubMed]
  25. Ruiz-Díez, B.; Fajardo, S.; Puertas-Mejía, M.A.; del Rosario de Felipe, M.; Fernández-Pascual, M. Stress tolerance, genetic analysis and symbiotic properties of root-nodulating bacteria isolated from Mediterranean leguminous shrubs in Central Spain. Arch. Microbiol. 2009, 191, 35–46. [Google Scholar] [CrossRef] [PubMed]
  26. Ruiz-Díez, B.; Quiñones, M.A.; Fajardo, S.; López, M.A.; Higueras, P.; Fernández-Pascual, M. Mercury-resistant rhizobial bacteria isolated from nodules of leguminous plants growing in high Hg-contaminated soils. Appl. Microbiol. Biotechnol. 2012, 96, 543–554. [Google Scholar] [CrossRef] [PubMed]
  27. Lemaire, B.; Van Cauwenberghe, J.; Chimphango, S.; Stirton, C.; Honnay, O.; Smets, E.; Muasya, A.M. Recombination and horizontal transfer of nodulation and ACC deaminase (acdS) genes within Alpha- and Betaproteobacteria nodulating legumes of the Cape Fynbos biome. FEMS Microbiol. Ecol. 2015, 91, fiv118. [Google Scholar] [CrossRef] [PubMed]
  28. Beukes, C.W.; Stępkowski, T.; Venter, S.N.; Cłapa, T.; Phalane, F.L.; le Roux, M.M.; Steenkamp, E.T. Crotalarieae and Genisteae of the South African Great Escarpment are nodulated by novel Bradyrhizobium species with unique and diverse symbiotic loci. Mol. Phylogenet. Evol. 2016, 100, 206–218. [Google Scholar] [CrossRef] [PubMed]
  29. Zakhia, F.; Jeder, H.; Domergue, O.; Willems, A.; Cleyet-Marel, J.-C.; Gillis, M.; Dreyfus, B.; de Lajudie, P. Characterisation of Wild Legume Nodulating Bacteria (LNB) in the Infra-arid Zone of Tunisia. Syst. Appl. Microbiol. 2004, 27, 380–395. [Google Scholar] [CrossRef] [PubMed]
  30. Mahdhi, M.; de Lajudie, P.; Mars, M. Phylogenetic and symbiotic characterization of rhizobial bacteria nodulating Argyrolobium uniflorum in Tunisian arid soils. Can. J. Microbiol. 2008, 54, 209–217. [Google Scholar] [CrossRef] [PubMed]
  31. Mnasri, B.; Badri, Y.; Saidi, S.; de Lajudie, P.; Mhamdi, R. Symbiotic diversity of Ensifer meliloti strains recovered from various legume species in Tunisia. Syst. Appl. Microbiol. 2009, 32, 583–592. [Google Scholar] [CrossRef] [PubMed]
  32. Merabet, C.; Martens, M.; Mahdhi, M.; Zakhia, F.; Sy, A.; Le Roux, C.; Domergue, O.; Coopman, R.; Bekki, A.; Mars, M.; Willems, A.; de Lajudie, P. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal), Lotus creticus, Argyrolobium uniflorum and Medicago sativa (Tunisia) and description of Ensifer numidicus sp nov and Ensifer garamanticus sp nov. Int. J. Syst. Evol. Microbiol. 2010, 60, 664–674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Mousavi, S.A.; Österman, J.; Wahlberg, N.; Nesme, X.; Lavire, C.; Vial, L.; Paulin, L.; de Lajudie, P.; Lindström, K. Phylogeny of the Rhizobium–Allorhizobium–Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Syst. Appl. Microbiol. 2014, 37, 208–215. [Google Scholar] [CrossRef] [PubMed]
  34. Cardinale, M.; Lanza, A.; Bonnì, M.L.; Marsala, S.; Puglia, A.M.; Quatrini, P. Diversity of rhizobia nodulating wild shrubs of Sicily and some neighbouring islands. Arch. Microbiol. 2008, 190, 461–470. [Google Scholar] [CrossRef] [PubMed]
  35. Vinuesa, P.; Leon-Barrios, M.; Silva, C.; Willems, A.; Jarabo-Lorenzo, A.; Perez-Galdona, R.; Werner, D.; Martinez-Romero, E. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies α and Bradyrhizobium genospecies β. Int. J. Syst. Evol. Microbiol. 2005, 55, 569–575. [Google Scholar] [CrossRef] [PubMed]
  36. Vinuesa, P.; Rojas-Jiménez, K.; Contreras-Moreira, B.; Mahna, S.K.; Prasad, B.N.; Moe, H.; Selvaraju, S.B.; Thierfelder, H.; Werner, D. Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the asiatic continent. Appl. Environ. Microbiol. 2008, 74, 6987–6996. [Google Scholar] [CrossRef] [PubMed]
  37. Liu, W.Y.Y. Characterisation of rhizobia and studies on N2 fixation of common weed legumes in New Zealand. Ph.D. Thesis, Lincoln University, Lincoln, New Zealand, 2014. [Google Scholar]
  38. Weir, B.S.; Turner, S.J.; Silvester, W.B.; Park, D.C.; Young, J.M. Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Appl. Environ. Microbiol. 2004, 70, 5980–5987. [Google Scholar] [CrossRef] [PubMed]
  39. Kalita, M.; Małek, W. Molecular phylogeny of Bradyrhizobium bacteria isolated from root nodules of tribe Genisteae plants growing in southeast Poland. Syst. Appl. Microbiol. 2017, 40, 482–491. [Google Scholar] [CrossRef] [PubMed]
  40. Baimiev, A.K.; Ivanova, E.S.; Ptitsyn, K.G.; Belimov, A.A.; Safronova, V.I.; Baimiev, A.K. Genetic Characterization of Wild Leguminous Nodular Bacteria Living in the South Urals. Mol. Genet. Microbiol. Virol. 2012, 27, 33–39. [Google Scholar] [CrossRef]
  41. Rodríguez-Echeverría, S.; Pérez Fernández, M.A.; Vlaar, S.; Finan, T.M. Analysis of the legume-rhizobia symbiosis in shrubs from central western Spain. J. Appl. Microbiol. 2003, 95, 1367–1374. [Google Scholar] [CrossRef] [PubMed]
  42. Rodríguez-Echeverría, S.; Pérez-Fernández, M.A. Potential use of Iberian shrubby legumes and rhizobia inoculation in revegetation projects under acidic soil conditions. App. Soil Ecol. 2005, 29, 203–208. [Google Scholar] [CrossRef]
  43. Pérez-Fernández, M.A.; Hill, Y.J.; Calvo-Magro, E.; Valentine, A. Competing Bradyrhizobia strains determine niche occupancy by two native legumes in the Iberian Peninsula. Plant Ecol. 2015, 216, 1537–1549. [Google Scholar] [CrossRef]
  44. Horn, K.; Parker, I.M.; Malek, W.; Rodríguez-Echeverría, S.; Parker, M.A. Disparate origins of Bradyrhizobium symbionts for invasive populations of Cytisus scoparius (Leguminosae) in North America. FEMS Microbiol. Ecol. 2014, 89, 89–98. [Google Scholar] [CrossRef] [PubMed]
  45. Parker, M.A.; Malek, W.; Parker, I.M. Growth of an invasive legume is symbiont limited in newly occupied habitats. Divers. Distrib. 12, 563–571. [CrossRef]
  46. Lafay, B.; Burdon, J.J. Molecular diversity of rhizobia nodulating the invasive legume Cytisus scoparius in Australia. J. Appl. Microbiol. 2006, 100, 1228–1238. [Google Scholar] [CrossRef] [PubMed]
  47. Zurdo-Piñeiro, J.L.; Rivas, R.; Trujillo, M.E.; Vizcaíno, N.; Carrasco, J.A.; Chamber, M.; Palomares, A.; Mateos, P.F.; Martínez-Molina, E.; Velázquez, E. Ochrobactrum cytisi sp. nov., isolated from nodules of Cytisus scoparius in Spain. Int. J. Syst. Evol. Microbiol. 2007, 57, 784–788. [Google Scholar] [CrossRef] [PubMed]
  48. De Meyer, S.E.; Van Hoorde, K.; Vekeman, B.; Braeckman, T.; Willems, A. Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol. Biochem. 2011, 43, 2384–2396. [Google Scholar] [CrossRef]
  49. Chahboune, R.; Carro, L.; Peix, A.; Barrijal, S.; Velázquez, E.; Bedmar, E.J. Bradyrhizobium cytisi sp. nov. isolated from effective nodules of Cytisus villosus in Morocco. Int. J. Syst. Evol. Microbiol. 2011, 61, 2922–2927. [Google Scholar] [CrossRef] [PubMed]
  50. Ahnia, H.; Boulila, F.; Boulila, A.; Boucheffa, K.; Durán, D.; Bourebaba, Y.; Salmi, A.; Imperial, J.; Ruiz-Argüeso, T.; Rey, L. Cytisus villosus from Northeastern Algeria is nodulated by genetically diverse Bradyrhizobium strains. Antonie van Leeuwenhoek 2014, 105, 1121–1129. [Google Scholar] [CrossRef] [PubMed]
  51. Chahboune, R.; Barrijal, S.; Moreno, S.; Bedmar, E.J. Characterization of Bradyrhizobium species isolated from root nodules of Cytisus villosus grown in Morocco. Syst. Appl. Microbiol. 2011, 34, 440–445. [Google Scholar] [CrossRef] [PubMed]
  52. Chahboune, R.; Carro, L.; Peix, A.; Ramírez-Bahena, M.H.; Barrijal, S.; Velázquez, E.; Bedmar, E.J. Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Syst. Appl. Microbiol. 2012, 35, 302–305. [Google Scholar] [CrossRef] [PubMed]
  53. Parker, M.A.; Rousteau, A. Mosaic origins of Bradyrhizobium legume symbionts on the Caribbean island of Guadeloupe. Mol. Phylogenet. Evol. 2014, 77, 110–115. [Google Scholar] [CrossRef] [PubMed]
  54. Gonzalez-Andres, F.; Ortiz, J.M. Specificity of Rhizobia Nodulating Genista monspessulana and Genista linifolia In Vitro and in Field Situations. Arid Soil Res. Rehabil. 1999, 13, 223–237. [Google Scholar] [CrossRef]
  55. Mahdhi, M.; Nzoué, A.; Gueye, F.; Merabet, C.; de Lajudie, P.; Mars, M. Phenotypic and genotypic diversity of Genista saharae microsymbionts from the infra-arid region of Tunisia. Lett. Appl. Microbiol. 2007, 45, 604–609. [Google Scholar] [CrossRef] [PubMed]
  56. Chaïch, K.; Bekki, A.; Bouras, N.; Holtz, M.D.; Soussou, S.; Mauré, L.; Brunel, B.; de Lajudie, P.; Cleyet-Marel, J.-C. Rhizobial diversity associated with the spontaneous legume Genista saharae in the northeastern Algerian Sahara. Symbiosis 2017, 71, 111–120. [Google Scholar] [CrossRef]
  57. Kalita, M.; Stępkowski, T.; Łotocka, B.; Małek, W. Phylogeny of nodulation genes and symbiotic properties of Genista tinctoria bradyrhizobia. Arch. Microbiol. 2006, 186, 87–97. [Google Scholar] [CrossRef] [PubMed]
  58. Kalita, M.; Małek, W. Genista tinctoria microsymbionts from Poland are new members of Bradyrhizobium japonicum bv. genistearum. Syst. Appl. Microbiol. 2010, 33, 252–259. [Google Scholar] [CrossRef] [PubMed]
  59. Cobo-Díaz, J.F.; Martínez-Hidalgo, P.; Fernández-González, A.J.; Martínez-Molina, E.; Toro, N.; Velázquez, E.; Fernández-López, M. The endemic Genista versicolor from Sierra Nevada National Park in Spain is nodulated by putative new Bradyrhizobium species and a novel symbiovar (sierranevadense). Syst. Appl. Microbiol. 2014, 37, 177–185. [Google Scholar] [CrossRef] [PubMed]
  60. Stępkowski, T.; Hughes, C.E.; Law, I.J.; Markiewicz, Ł.; Gurda, D.; Chlebicka, A.; Moulin, L. Diversification of lupin Bradyrhizobium strains: evidence from nodulation gene trees. Appl. Environ. Microbiol. 2007, 73, 3254–3264. [Google Scholar] [CrossRef] [PubMed]
  61. Granada, C.E.; Beneduzi, A.; Lisboa, B.B.; Turchetto-Zolet, A.C.; Vargas, L.K.; Passaglia, L.M.P. Multilocus sequence analysis reveals taxonomic differences among Bradyrhizobium sp. symbionts of Lupinus albescens plants growing in arenized and non-arenized areas. Syst. Appl. Microbiol. 2015, 38, 323–329. [Google Scholar] [CrossRef] [PubMed]
  62. González-Sama, A.; Lucas, M.M.; De Felipe, M.R.; Pueyo, J.J. An unusual infection mechanism and nodule morphogenesis in white lupin (Lupinus albus). New Phytol. 2004, 163, 371–380. [Google Scholar] [CrossRef] [Green Version]
  63. Velázquez, E.; Valverde, A.; Rivas, R.; Gomism, V.; Peixm, A.; Gantois, I.; Igual, J.M.; León-Barrios, M.; Willems, A.; Mateos, P.F.; Martínez-Molina, E. Strains nodulating Lupinus albus on different continents belong to several new chromosomal and symbiotic lineages within Bradyrhizobium. Antonie Van Leeuwenhoek 2010, 97, 363–376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Sánchez-Cañizares, C.; Rey, L.; Durán, D.; Temprano, F.; Sánchez-Jiménez, P.; Navarro, A.; Polajnar, M.; Imperial, J.; Ruiz-Argüeso, T. Endosymbiotic bacteria nodulating a new endemic lupine Lupinus mariae-josephi from alkaline soils in Eastern Spain represent a new lineage within the Bradyrhizobium genus. Syst. Appl. Microbiol. 2011, 34, 207–215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Stępkowski, T.; Żak, M.; Moulin, L.; Króliczak, J.; Golińska, B.; Narożna, D.; Safronova, V.I.; Mądrzak, C.J. Bradyrhizobium canariense and Bradyrhizobium japonicum are the two dominant rhizobium species in root nodules of lupin and serradella plants growing in Europe. Syst. App. Microbiol. 2011, 34, 368–375. [Google Scholar] [CrossRef] [PubMed]
  66. Weisskopf, L.; Heller, S.; Eberl, L. Burkholderia species are major inhabitants of white lupin cluster roots. Appl. Environ. Microbiol. 2011, 77, 7715–7720. [Google Scholar] [CrossRef] [PubMed]
  67. Quiñones, M.A.; Ruiz-Díez, B.; Fajardo, S.; López-Berdonces, M.A.; Higueras, P.L.; Fernández-Pascual, M. Lupinus albus plants acquire mercury tolerance when inoculated with an Hg-resistant Bradyrhizobium strain. Plant Physiol. Biochem. 2013, 73, 168–175. [Google Scholar] [CrossRef] [PubMed]
  68. Stępkowski, T.; Moulin, L.; Krzyżańska, A.; McInnes, A.; Law, I.J.; Howieson, J. European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa. Appl. Environ. Microbiol. 2005, 71, 7041–7052. [Google Scholar] [CrossRef] [PubMed]
  69. Peix, A.; Ramírez-Bahena, M.H.; Flores-Félix, J.D.; de la Vega, P.A.; Rivas, R.; Mateos, P.F.; Igual, J.M.; Martínez-Molina, E.; Trujillo, M.E.; Velázquez, E. Revision of the taxonomic status of the species Rhizobium lupini and reclassification as Bradyrhizobium lupini comb. nov. Int. J. Syst. Evol. Microbiol. 2015, 65, 1213–1219. [Google Scholar] [CrossRef] [PubMed]
  70. Koppell, J.H.; Parker, M.A. Phylogenetic clustering of Bradyrhizobium symbionts on legumes indigenous to North America. Microbiology 2012, 158, 2050–2059. [Google Scholar] [CrossRef] [PubMed]
  71. Ehinger, M.; Mohr, T.J.; Starcevich, J.B.; Sachs, J.L.; Porter, S.S.; Simms, E.L. Specialization-generalization trade-off in a Bradyrhizobium symbiosis with wild legume hosts. BMC Ecol. 2014, 14, 8. [Google Scholar] [CrossRef] [PubMed]
  72. Trujillo, M.E.; Willems, A.; Abril, A.; Planchuelo, A.M.; Rivas, R.; Ludeña, D.; Mateos, P.F.; Martínez-Molina, E.; Velázquez, E. Nodulation of Lupinus albus by strains of Ochrobactrum lupini sp. nov. Appl. Environ. Microbiol. 2005, 71, 1318–1327. [Google Scholar] [CrossRef] [PubMed]
  73. Stępkowski, T.; Świderska, A.; Miedzinska, K.; Czaplinska, M.; Świderski, M.; Biesiadka, J.; Legocki, A.B. Low sequence similarity and gene content of symbiotic clusters of Bradyrhizobium sp. WM9 (Lupinus) indicate early divergence of “lupin” lineage in the genus Bradyrhizobium. Antonie Van Leeuwenhoek 2003, 84, 115–124. [Google Scholar] [CrossRef] [PubMed]
  74. Rey, L.; Sanchez-Canizares, C.; Durant, D.; Temprano, D.F.; Navarro, A.; Imperial, J.; Ruiz-Argueso, T. Lupinus marie-josephi, a new lupin endemic of soils with active lime and high pH in Eastern Spain, is nodulated by a new bacterial lineage within Bradyrhizobium genus. In Lupin crops—n Opportunity for Today, a Promise for the Future, Proceedings of the 13th International Lupin Conference, Poznań, Poland, 6–10 June 2011; Naganowska, B., Kachlicki, P., Wolko, B., Eds.; International Lupin Association: Canterbury, New Zealand; ISBN 978-83-61607-73-1.
  75. Durán, D.; Rey, L.; Sánchez-Cañizares, C.; Navarro, A.; Imperial, J.; Ruiz-Argueso, T. Genetic diversity of indigenous rhizobial symbionts of the Lupinus mariae-josephae endemism from alkaline-limed soils within its area of distribution in Eastern Spain. Syst. Appl. Microbiol. 2013, 36, 128–136. [Google Scholar] [CrossRef] [PubMed]
  76. Durán, D.; Rey, L.; Navarro, A.; Busquets, A.; Imperial, J.; Ruiz-Argüesoa, T. Bradyrhizobium valentinum sp. nov., isolated from effective nodules of Lupinus mariae-josephae, a lupine endemic of basic-lime soils in Eastern Spain. Syst. Appl. Microbiol. 2014, 37, 336–341. [Google Scholar] [CrossRef] [PubMed]
  77. Navarro, A.; Fos, S.; Laguna, E.; Durán, D.; Rey, L.; Rubio-Sanz, L.; Imperial, J.; Ruiz-Argüeso, T. Conservation of endangered Lupinus mariae-josephae in its natural habitat by inoculation with selected, native Bradyrhizobium strains. PLoS ONE 2014, 9, e102205. [Google Scholar] [CrossRef] [PubMed]
  78. Bourebaba, Y.; Durán, D.; Boulila, F.; Ahnia, H.; Boulila, A.; Temprano, F.; Palacios, J.M.; Imperial, J.; Ruiz-Argüeso, T.; Rey, L. Diversity of Bradyrhizobium strains nodulating Lupinus micranthus on both sides of the Western Mediterranean: Algeria and Spain. Syst. Appl. Microbiol. 2016, 39, 266–274. [Google Scholar] [CrossRef] [PubMed]
  79. Msaddak, A.; Durán, D.; Rejili, M.; Mars, M.; Ruiz-Argüeso, T.; Imperial, J.; Palacios, J.; Rey, L. Diverse bacteria affiliated with the genera Microvirga, Phyllobacterium and Bradyrhizobium nodulate Lupinus micranthus growing in soils of Northern Tunisia. Appl. Environ. Microbiol. 2017, 83, e02820-16. [Google Scholar] [CrossRef] [PubMed]
  80. Msaddak, A.; Rejili, M.; Durán, D.; Rey, L.; Imperial, J.; Palacios, J.M.; Ruiz-Argüeso, T.; Mars, M. Members of Microvirga and Bradyrhizobium genera are native endosymbiotic bacteria nodulating Lupinus luteus in Northern Tunisian soils. FEMS Microbiol. Ecol. 2017, 93. [Google Scholar] [CrossRef] [PubMed]
  81. Parker, M.A.; Kennedy, D.A. Diversity and relationships of bradyrhizobia from legumes native to eastern North America. Can. J. Microbiol. 2006, 52, 1148–1157. [Google Scholar] [CrossRef] [PubMed]
  82. Parker, M.A. Legumes select symbiosis island sequence variants in Bradyrhizobium. Mol. Ecol. 2012, 21, 1769–1778. [Google Scholar] [CrossRef] [PubMed]
  83. De Meyer, S.E.; Willems, A. Multilocus sequence analysis of Bosea species and description of Bosea lupini sp. nov., Bosea lathyri sp. nov. and Bosea robiniae sp. nov., isolated from legumes. Int. J. Syst. Evol. Microbiol. 2012, 62, 2505–2510. [Google Scholar] [CrossRef] [PubMed]
  84. Ryan-Salter, T.P.; Black, A.D.; Andrews, M.; Moot, D.J. Identification and effectiveness of rhizobial strains that nodulate Lupinus polyphyllus. Proc. N. Z. Grassl. Assoc. 2014, 76, 61–66. [Google Scholar]
  85. Black, A.D.; Ryan-Salter, T.P.; Liu, W.Y.Y.; Moot, D.J.; Hill, G.D.; Andrews, M. Bradyrhizobia with a distinct nodA gene nodulate Lupinus polyphyllus in New Zealand soils. In Proceedings of the XIV Lupin Conference, Milan, Italy, 24 June 2015. [Google Scholar]
  86. Stępkowski, T.; Czaplińska, M.; Miedzińska, K.; Moulin, L. The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst. Appl. Microbiol. 2003, 26, 483–494. [Google Scholar] [CrossRef] [PubMed]
  87. Ardley, J.K.; Parker, M.A.; De Meyer, S.E.; Trengove, R.D.; O'Hara, G.W.; Reeve, W.G.; Yates, R.J.; Dilworth, M.J.; Willems, A.; Howieson, J.G. Microvirga lupini sp. nov., Microvirga lotononidis sp. nov., and Microvirga zambiensis sp. nov. are Alphaproteobacterial root nodule bacteria that specifically nodulate and fix nitrogen with geographically and taxonomically separate legume hosts. Int. J. Syst. Evol. Microbiol. 2012, 62, 2579–2588. [Google Scholar] [CrossRef] [PubMed]
  88. Guerrouj, K.; Ruíz-Díez, B.; Chahboune, R.; Ramírez-Bahena, M.-H.; Abdelmoumenf, H.; Quinones, M.A.; Missbah El Idrissi, M.; Velázqueze, E.; Fernández-Pascual, M.; Bedmar, E.J.; et al. Definition of a novel symbiovar (sv. retamae) within Bradyrhizobium retamae sp. nov., nodulating Retama sphaerocarpa and Retama monosperma. Syst. Appl. Microbiol. 2013, 36, 218–223. [Google Scholar] [CrossRef] [PubMed]
  89. Hannane, F.Z.; Kacem, M.; Kaid-Harche, M. Preliminary characterization of slow growing rhizobial strains isolated from Retama monosperma (L.) Boiss. root nodules from Northwest coast of Algeria. Afr. J. Biotechnol. 2016, 15, 854–867. [Google Scholar] [CrossRef]
  90. Mahdhi, M.; Mars, M. Genotypic diversity of rhizobia isolated from Retama raetam in arid regions of Tunisia. Ann. Microbiol. 2006, 56, 305–311. [Google Scholar] [CrossRef]
  91. Mahdhi, M.; Nzoué, A.; de Lajudie, P.; Mars, M. Characterization of root-nodulating bacteria on Retama raetam in arid Tunisian soils. Prog. Nat. Sci. 2008, 18, 43–49. [Google Scholar] [CrossRef]
  92. Boulila, F.; Depret, G.; Boulila, A.; Belhadi, D.; Benallaoua, S.; Laguerre, G. Retama species growing in different ecological-climatic areas of northeastern Algeria have a narrow range of rhizobia that form a novel phylogenetic clade within the Bradyrhizobium genus. Syst. Appl. Microbiol. 2009, 32, 245–255. [Google Scholar] [CrossRef] [PubMed]
  93. Rodríguez-Echeverría, S.; Moreno, S.; Bedmar, E.J. Genetic diversity of root nodulating bacteria associated with Retama sphaerocarpa in sites with different soil and environmental conditions. Syst. Appl. Microbiol. 2014, 37, 305–310. [Google Scholar] [CrossRef] [PubMed]
  94. Quatrini, P.; Scaglione, G.; Cardinale, M.; Caradonna, F.; Puglia, A.M. Bradyrhizobium sp. nodulating the Mediterranean shrub Spanish broom (Spartium junceum L.). J. Appl. Microbiol. 2002, 92, 13–21. [Google Scholar] [CrossRef] [PubMed]
  95. Rodríguez-Echeverría, S. Rhizobial hitchhikers from Down Under: invasional meltdown in a plant–bacteria mutualism? J. Biogeogr. 2010, 37, 1611–1622. [Google Scholar] [CrossRef]
  96. Andrews, M.; Jack, D.; Dash, D.; Brown, S. Which rhizobia nodulate which legumes in New Zealand soils. J. N. Z. Grassl. 2015, 77, 281–286. [Google Scholar]
  97. Sprent, J.I.; Ardley, J.; James, E.K. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytologist. 2017, 215, 40–56. [Google Scholar] [CrossRef] [PubMed]
  98. Delmont, T.O.; Prestat, E.; Keegan, K.P.; Faubladier, M.; Robe, P.; Clark, I.M.; Pelletier, E.; Hirsch, P.R.; Meyer, F.; Gilbert, J.A.; et al. Structure, fluctuation and magnitude of a natural grassland soil metagenome. ISME J. 2012, 6, 1677–1687. [Google Scholar] [CrossRef] [PubMed]
  99. Okubo, T.; Tsukui, T.; Maita, H.; Okamoto, S.; Oshima, K.; Fujisawa, T.; Saito, A.; Futamata, H.; Hattori, R.; Shimomura, Y.; et al. Complete genome sequence of Bradyrhizobium sp. S23321: insights into symbiosis evolution in soil oligotrophs. Microbes Environ. 2012, 27, 306–315. [Google Scholar] [CrossRef] [PubMed]
  100. Guha, S.; Sarkar, M.; Ganguly, P.; Uddin, M.R.; Mandal, S.; DasGupta, M. Segregation of nod-containing and nod-deficient bradyrhizobia as endosymbionts of Arachis hypogaea and as endophytes of Oryza sativa in intercropped fields of Bengal Basin, India. Environ. Microbiol. 2016, 18, 2575–2590. [Google Scholar] [CrossRef] [PubMed]
  101. Jones, F.P.; Clark, I.M.; King, R.; Shaw, L.J.; Woodward, M.J.; Hirsch, P.R. Novel European free-living, non-diazotrophic Bradyrhizobium isolates from contrasting soils that lack nodulation and nitrogen fixation genes - a genome comparison. Sci. Rep. 2016, 6, 25858. [Google Scholar] [CrossRef] [PubMed]
  102. VanInsberghe, D.; Maas, K.R.; Cardenas, E.; Strachan, C.R.; Hallam, S.J.; Mohn, W.W. Non-symbiotic Bradyrhizobium ecotypes dominate North American forest soils. ISME J. 2015, 9, 2435–2441. [Google Scholar] [CrossRef] [PubMed]
  103. Rosenberg, E.; Zilber-Rosenberg, I. Microbes Drive Evolution of Animals and Plants: the Hologenome Concept. MBio 2016, 7, e01395. [Google Scholar] [CrossRef] [PubMed]
  104. Erlacher, A.; Cernava, T.; Cardinale, M.; Soh, J.; Sensen, C.W.; Grube, M.; Berg, G. Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol. 2015, 6, 53. [Google Scholar] [CrossRef] [PubMed]
  105. Tláskal, V.; Zrustová, P.; Vrška, T.; Baldrian, P. Bacteria associated with decomposing dead wood in a natural temperate forest. FEMS Microbiol. Ecol. 2017, 93, fix157. [Google Scholar] [CrossRef] [PubMed]
  106. 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 soilchronosequence. Nat. Commun. 2017, 8, 215. [Google Scholar] [CrossRef] [PubMed]
  107. Masuda, S.; Eda, S.; Ikeda, S.; Mitsui, H.; Minamisawa, K. Thiosulfate-dependent chemolithoautotrophic growth of Bradyrhizobium japonicum. Appl. Environ. Microbiol. 2010, 76, 2402–2409. [Google Scholar] [CrossRef] [PubMed]
  108. Lema, K.A.; Willis, B.L.; Bourne, D.G. Amplicon pyrosequencing reveals spatial and temporal consistency in diazotroph assemblages of the Acropora millepora microbiome. Environ. Microbiol. 2014, 16, 3345–3359. [Google Scholar] [CrossRef] [PubMed]
  109. Godoy-Vitorino, F.; Ruiz-Diaz, C.P.; Rivera-Seda, A.; Ramírez-Lugo, J.S.; Toledo-Hernández, C. The microbial biosphere of the coral Acropora cervicornis in Northeastern Puerto Rico. PeerJ. 2017, 5, e3717. [Google Scholar] [CrossRef] [PubMed]
  110. do Vale Pereira, G.; da Cunha, D.G.; Pedreira Mourino, J.L.; Rodiles, A.; Jaramillo-Torres, A.; Merrifield, D.L. Characterization of microbiota in Arapaima gigas intestine and isolation of potential probiotic bacteria. J. Appl. Microbiol. 2017, 123, 1298–1311. [Google Scholar] [CrossRef] [PubMed]
  111. Gevers, D.; Cohan, F.M.; Lawrence, J.G.; Spratt, B.G.; Coenye, T.; Feil, E.J.; Stackebrandt, E.; Van de Peer, Y.; Vandamme, P.; Thompson, F.L.; Swings, J. Opinion: Re-evaluating prokaryotic species. Nat. Rev. Microbiol. 2005, 3, 733–739. [Google Scholar] [CrossRef] [PubMed]
  112. Jordan, J.C. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow growing root nodule bacteria from leguminous plants. Int. J. Syst. Bacteriol. 1982, 32, 136–139. [Google Scholar] [CrossRef]
  113. Menna, P.; Barcellos, F.G.; Hungria, M. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int. J. Syst. Evol. Microbiol. 2009, 59, 2934–2950. [Google Scholar] [CrossRef] [PubMed]
  114. Stępkowski, T.; Watkin, E.; McInnes, A.; Gurda, D.; Gracz, J.; Steenkamp, E.T. Distinct Bradyrhizobium communities nodulate legumes native to temperate and tropical monsoon Australia. Mol. Phylogenet. Evol. 2012, 63, 265–277. [Google Scholar] [CrossRef] [PubMed]
  115. Posada, D. jModelTest: Phylogenetic Model Averaging. Mol. Biol. Evol. 2008, 27, 1253–1256. [Google Scholar] [CrossRef] [PubMed]
  116. Barrera, L.L.; Trujillo, M.E.; Goodfellow, M.; García, F.J.; Hernández-Lucas, I.; Dávila, G.; van Berkum, P.; Martínez-Romero, E. Biodiversity of bradyrhizobia nodulating Lupinus spp. Int. J. Syst. Bacteriol. 1997, 47, 1086–1091. [Google Scholar] [CrossRef] [PubMed]
  117. 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] [PubMed]
  118. Hollowell, A.C.; Regus, J.U.; Gano, K.A.; Bantay, R.; Centeno, D.; Pham, J.; Lyu, J.Y.; Moore, D.; Bernardo, A.; Lopez, G.; Patil, A.; Patel, S.; Lii, Y.; Sachs, J.L. Epidemic Spread of Symbiotic and Non-Symbiotic Bradyrhizobium Genotypes Across California. Microb. Ecol. 2016, 71, 700–710. [Google Scholar] [CrossRef] [PubMed]
  119. Hollowell, A.C.; Regus, J.U.; Turissini, D.; Gano-Cohen, K.A.; Bantay, R.; Bernardo, A.; Moore, D.; Pham, J.; Sachs, J.L. Metapopulation dominance and genomic-island acquisition of Bradyrhizobium with superior catabolic capabilities. Proc. Biol. Sci. 2016, 283, 20160496. [Google Scholar] [CrossRef] [PubMed]
  120. Sokoloff, D.D. Legumes of the World; Lewis, G., Schrire, B., Mackinder, B., Lock, M., Eds.; Royal Botanic Gardens, Kew: London, UK, 2005; pp. 454–465. ISBN 1-900-34780-6. [Google Scholar]
  121. Degtjareva, D.V.; Valiejo-Roman, C.M.; Kramina, T.E.; Mironov, E.M.; Samigullin, T.H.; Sokoloff, D.D. Taxonomic and phylogenetic relationships between Old World and New World members of the tribe Loteae (Leguminosae): new insights from molecular and morphological data, with special emphasis on Ornithopus. Wulfenia 2003, 10, 15–50. [Google Scholar]
  122. Drummond, C.S. Diversification of Lupinus (Leguminosae) in the western New World: derived evolution of perrennial life history and colonization of montane habitats. Mol. Phylogenet. Evol. 2008, 48, 408–421. [Google Scholar] [CrossRef] [PubMed]
  123. Rivas, R.; Willems, A.; Palomo, J.L.; García-Benavides, P.; Mateos, P.F.; Martínez-Molina, E.; Gillis, M.; Velázquez, E. Bradyrhizobium betae sp. nov., isolated from roots of Beta vulgaris affected by tumour-like deformations. Int. J. Syst. Evol. Microbiol. 2004, 54, 1271–1275. [Google Scholar] [CrossRef] [PubMed]
  124. Planchuelo, A.M.; Dunn, D.B. The simple leaved lupines and their relatives in Argentina. Ann. Mo. Bot. Gard. 1984, 71, 92–103. [Google Scholar] [CrossRef]
  125. Mahé, F.; Pascual, H.; Coriton, O.; Huteau, V.; Navarro-Perris, A.; Misset, M.T.; Ainouché, A.K. New data and phylogenetic placement of the enigmatic Old World lupin: Lupinus mariae-josephi H. Pascual. Genet. Resour. Crop Evol. 2011, 58, 101–114. [Google Scholar] [CrossRef]
  126. Menna, P.; Hungria, M. Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: Supporting evidences for the theory of monophyletic origin and spread and maintenance by both horizontal and vertical transfer. Int. J. Syst. Evol. Microbiol. 2011, 61, 3052–3067. [Google Scholar] [CrossRef] [PubMed]
  127. Aserse, A.A.; Räsänen, L.A.; Aseffa, F.; Hailemariam, A.; Lindström, K. Phylogenetically diverse groups of Bradyrhizobium isolated from nodules of Crotalaria spp., Indigofera spp., Erythrina brucei and Glycine max growing in Ethiopia. Mol. Phylogenet. Evol. 2012, 65, 595–609. [Google Scholar] [CrossRef] [PubMed]
  128. Chen, J.; Hu, M.; Ma, H.; Wang, Y.; Wang, E.T.; Zhou, Z.; Jun Gu, J. Genetic diversity and distribution of bradyrhizobia nodulating peanut in acid-neutral soils in Guangdong Province. Syst. Appl. Microbiol. 2016, 39, 418–427. [Google Scholar] [CrossRef] [PubMed]
  129. Degefu, T.; Wolde-Meskel, E.; Rasche, F. Genetic diversity and symbiotic effectiveness of Bradyrhizobium strains nodulating selected annual grain legumes growing in Ethiopia. Int. J. Syst. Evol. Microbiol. 2017, 68, 449–460. [Google Scholar] [CrossRef] [PubMed]
  130. Degefu, T.; Wolde-Meskel, E.; Woliy, K.; Frostegård, Å. Phylogenetically diverse groups of Bradyrhizobium isolated from nodules of tree and annual legume species growing in Ethiopia. Syst. Appl. Microbiol. 40, 205–214. [CrossRef] [PubMed]
  131. dos Santos, J.M.F.; Alves, P.A.C.; Silva, V.C.; Rhem, M.F.K.; James, E.K.; Gross, E. Diverse genotypes of Bradyrhizobium nodulate herbaceous Chamaecrista (Moench) (Fabaceae, Caesalpinioideae) species in Brazil. Syst. Appl. Microbiol. 2017, 40, 69–79. [Google Scholar] [CrossRef] [PubMed]
  132. Moulin, L.; Béna, G.; Boivin-Masson, C.; Stępkowski, T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol. Phyl. Evol. 2004, 30, 720–732. [Google Scholar] [CrossRef]
  133. Xia, X. DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. Mol. Biol. Evol. 2013, 30, 1720–1728. [Google Scholar] [CrossRef] [PubMed]
  134. Pierre, K.J.; Simms, E.L.; Tariq, M.; Zafar, M.; Porter, S.S. Invasive legumes can associate with many mutualists of native legumes, but usually do not. Ecol. Evol. 2017, 7, 8599–8611. [Google Scholar] [CrossRef] [PubMed]
  135. Martínez-Romero, E. Coevolution in Rhizobium-Legume Symbiosis? DNA Cell Biol. 2009, 28, 361–370. [Google Scholar] [CrossRef] [PubMed]
  136. Eckhardt, M.M.; Baldwin, I.R.; Fred, E.B. Studies on the root-nodule bacteria of Lupinus. J. Bacteriol. 1931, 21, 273–285. [Google Scholar] [PubMed]
  137. Perret, X.; Staehelin, C.; Broughton, W.J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 2000, 64, 180–201. [Google Scholar] [CrossRef] [PubMed]
  138. Tiwari, R.; Howieson, J.; Yates, R.; Tian, R.; Held, B.; Tapia, R.; Han, C.; Seshadri, R.; Reddy, T.B.; Huntemann, M.; Pati, A.; Woyke, T.; Markowitz, V.; Ivanova, N.; Kyrpides, N.; Reeve, W. Genome sequence of Bradyrhizobium sp. WSM1253; a microsymbiont of Ornithopus compressus from the Greek Island of Sifnos. Stand. Genomic Sci. 2015, 10, 113. [Google Scholar] [CrossRef] [PubMed]
  139. Goulart Machado, R.; Saccol De Sá, E.L.; Oldra, S.; Dalla Costa, M.; Dall´Agnol, G.; Da Silva Santos, N.; Rosa Da Silva, W. Rhizobia isolation and selection for serradella (Ornithopus micranthus) in Southern Brazil. Afr. J. Microbiol. Res. 2016, 10, 1894–1907. [Google Scholar] [CrossRef]
  140. Cubas, P.; Pardo, C.; Tahiri, H. Molecular approach to the phylogeny and systematics of Cytisus (Leguminosae) and related genera based on nucleotide sequence of nrDNA (ITS region) and cpDNA (trnL-trnF intergenic spacer). Plant Syst. Evol. 2002, 233, 223–242. [Google Scholar] [CrossRef]
  141. Pardo, C.; Cubas, P.; Tahiri, H. Molecular phylogeny and systematics of Genista (Leguminosae) and related genera based on nucleotide sequences of nrDNA (ITS region) and cpDNA (trnL-trnF intergenic spacer). Plant Syst. Evol. 2004, 244, 93–119. [Google Scholar] [CrossRef]
  142. Grönemeyer, J.L.; Bünger, W.; Reinhold-Hurek, B. Bradyrhizobium namibiense sp. nov., a symbiotic nitrogen-fixing bacterium from root nodules of Lablab purpureus, hyacinth bean, in Namibia. Int. J. Syst. Evol. Microbiol. 2017, 67, 4884–4891. [Google Scholar] [CrossRef] [PubMed]
  143. Islam, M.S.; Kawasaki, H.; Muramatsu, Y.; Nakagawa, Y.; Seki, T. Bradyrhizobium iriomotense sp. nov., isolated from a tumor-like root of the legume Entada koshunensis from Iriomote Island in Japan. Biosci. Biotechnol. Biochem. 2008, 72, 1416–1429. [Google Scholar] [CrossRef] [PubMed]
  144. da Silva, K.; De Meyer, S.E.; Rouws, L.F.M.; Farias, E.N.C.; dos Santos, M.A.O.; O'Hara, G.; Ardley, J.K.; Willems, A.; Pitard, R.M.; Zilli, J.E. Bradyrhizobium ingae sp. nov., isolated from effective nodules of Inga laurina grown in Cerrado soil. Int. J. Syst. Evol. Microbiol. 2014, 64, 3395–3401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Silva, F.V.; De Meyer, S.E.; Simões-Araújo, J.L.; Barbé Tda, C.; Xavier, G.R.; O'Hara, G.; Ardley, J.K.; Rumjanek, N.G.; Willems, A.; Zilli, J.E. Bradyrhizobium manausense sp. nov., isolated from effective nodules of Vigna unguiculata grown in Brazilian Amazonian rainforest soils. Int. J. Syst. Evol. Microbiol. 2014, 64, 2358–2363. [Google Scholar] [CrossRef] [PubMed]
  146. Delamuta, J.R.; Ribeiro, R.A.; Araújo, J.L.; Rouws, L.F.; Zilli, J.É.; Parma, M.M.; Melo, I.S.; Hungria, M. Bradyrhizobium stylosanthis sp. nov., comprising nitrogen-fixing symbionts isolated from nodules of the tropical forage legume Stylosanthes spp. Int. J. Syst. Evol. Microbiol. 2016, 66, 3078–3087. [Google Scholar] [CrossRef] [PubMed]
  147. Ramírez-Bahena, M.H.; Flores-Félix, J.D.; Chahboune, R.; Toro, M.; Velázquez, E.; Peix, A. Bradyrhizobium centrosemae (symbiovar centrosemae) sp. nov., Bradyrhizobium americanum (symbiovar phaseolarum) sp. nov. and a new symbiovar (tropici) of Bradyrhizobium viridifuturi establish symbiosis with Centrosema species native to America. Syst. Appl. Microbiol. 2016, 39, 378–383. [Google Scholar] [CrossRef] [PubMed]
  148. Qian, J.; Kwon, S.W.; Parker, M.A. rRNA and nifD phylogeny of Bradyrhizobium from sites across the Pacific Basin. FEMS Microbiol. Lett. 2003, 219, 159–165. [Google Scholar] [CrossRef]
  149. Ramírez-Bahena, M.H.; Peix, A.; Rivas, R.; Camacho, M.; Rodríguez-Navarro, D.N.; Mateos, P.F.; Martínez-Molina, E.; Willems, A.; Velázquez, E. Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov. isolated from effective nodules of Pachyrhizus erosus. Int. J. Syst. Evol. Microbiol. 2009, 59, 1929–1934. [Google Scholar] [CrossRef] [PubMed]
  150. Hollowell, A.C.; Gano, K.A.; Lopez, G.; Shahin, K.; Regus, J.U.; Gleason, N.; Graeter, S.; Pahua, V.; Sachs, J.L. Native California soils are selective reservoirs for multidrug-resistant bacteria. Environ. Microbiol. Rep. 2015, 7, 442–449. [Google Scholar] [CrossRef] [PubMed]
  151. Boatwright, J.S.; le Roux, M.M.; Wink, M.; Morozova, T.; Van Wyk, B.E. Phylogenetic relationships of tribe Crotalarieae (Fabaceae) inferred from DNA sequences and morphology. Syst. Bot. 2008, 33, 752–761. [Google Scholar] [CrossRef]
  152. Richardson, D.M.; Carruthers, J.; Hui, C.; Impson, F.A.C.; Miller, J.T.; Robertson, M.P.; Rouget, M.; Le Roux, J.J.; Wilson, J.R.U. Human-mediated introductions of Australian acacias—A global experiment in biogeography. Divers. Distrib. 2011, 17, 771–787. [Google Scholar] [CrossRef]
  153. Ndlovu, J.; Richardson, D.M.; Wilson, J.R.U.; Le Roux, J.J. Co-invasion of South African ecosystems by an Australian legume and its rhizobial symbionts. J. Biogeogr. 2013, 40, 1240–1251. [Google Scholar] [CrossRef]
  154. Rodríguez-Echeverría, S.; Le Roux, J.J.; Crisóstomo, J.A.; Ndlovu, J. Jack-of-all-trades and master of many? How does associated rhizobial diversity influence the colonization success of Australian Acacia species? Divers. Distrib. 2011, 17, 946–957. [Google Scholar] [CrossRef]
  155. Crisóstomo, J.A.; Rodríguez-Echeverría, S.; Freitas, H. Co-introduction of exotic rhizobia to the rhizosphere of the invasive legume Acacia saligna, an intercontinental study. Appl. Soil Ecol. 2013, 64, 118–126. [Google Scholar] [CrossRef]
  156. Andrews, M.; Andrews, M.E. Specificity in legume-rhizobia symbioses. Int. J. Mol. Sci. 2017, 18, 705. [Google Scholar] [CrossRef] [PubMed]
  157. Beligala, D.H.; Michaels, H.J.; Devries, M.; Phuntumart, V. Multilocus Sequence Analysis of Root Nodule Bacteria Associated with Lupinus spp. and Glycine max. Adv. Microbiol. 2017, 7, 790–812. [Google Scholar] [CrossRef]
  158. Pudełko, K. Diversity among field populations of bacterial strains nodulating lupins in Poland. Fragm. Agron. 2010, 27, 107–116. [Google Scholar]
  159. Pudełko, K.; Żarnicka, J. Diversity in symbiotic specificity of bacterial strains nodulating lupins in Poland. Pol. J. Agron. 2010, 2, 50–56. [Google Scholar]
  160. Wibberg, D.; Blom, J.; Jaenicke, S.; Kollin, F.; Rupp, O.; Scharf, B.; Schneiker-Bekel, S.; Sczcepanowski, R.; Goesmann, A.; Setubal, J.C.; Schmitt, R.; Pühler, A.; Schlüter, A. Complete genome sequencing of Agrobacterium sp. H13-3, the former Rhizobium lupini H13-3, reveals a tripartite genome consisting of a circular and a linear chromosome and an accessory plasmid but lacking a tumor-inducing Ti-plasmid. J. Biotechnol. 2011, 155, 50–62. [Google Scholar] [CrossRef] [PubMed]
  161. Gonzalez-Bashan, L.E.; Lebsky, V.K.; Hernandez, J.P.; Bustillos, J.J.; Bashan, Y. Changes in the metabolism of the microalga Chlorella vulgaris when coimmobilized in alginate with the nitrogen-fixing Phyllobacterium myrsinacearum. Can. J. Microbiol. 2000, 46, 653–659. [Google Scholar] [CrossRef] [PubMed]
  162. Mnasri, B.; Mrabet, M.; Laguerre, G.; Aouani, M.E.; Mhamdi, R. Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 2007, 187, 79–85. [Google Scholar] [CrossRef] [PubMed]
  163. Lebuhn, M.; Bathe, S.; Achouak, W.; Hartmann, A.; Heulin, T.; Schloter, M. Comparative sequence analysis of the internal transcribed spacer 1 of Ochrobactrum species. Syst. Appl. Microbiol. 2006, 29, 265–275. [Google Scholar] [CrossRef] [PubMed]
  164. Ngom, A.; Nakagawa, Y.; Sawada, H.; Tsukahara, J.; Wakabayashi, S.; Uchiumi, T.; Nuntagij, A.; Kotepong, S.; Suzuki, A.; Higashi, S.; Abe, M. A novel symbiotic nitrogen-fixing member of the Ochrobactrum clade isolated from root nodules of Acacia mangium. J. Gen. Appl. Microbiol. 2004, 50, 17–27. [Google Scholar] [CrossRef] [PubMed]
  165. Imran, A.; Hafeez, F.Y.; Frühling, A.; Schumann, P.; Malik, K.A.; Stackebrandt, E. Ochrobactrum ciceri sp. nov., isolated from nodules of Cicer arietinum. Int. J. Syst. Evol. Microbiol. 2010, 60, 1548–1553. [Google Scholar] [CrossRef] [PubMed]
  166. Andam, C.P.; Parker, M.A. Novel Alphaproteobacterial Root Nodule Symbiont Associated with Lupinus texensis. Appl. Environ. Microbiol. 2007, 73, 5687–5691. [Google Scholar] [CrossRef] [PubMed]
  167. Reeve, W.; Parker, M.; Tian, R.; Goodwin, L.; Teshima, H.; Tapia, R.; Han, C.; Han, J.; Liolios, K.; Huntemann, M.; Pati, A.; Woyke, T.; Mavromatis, K.; Markowitz, V.; Ivanova, N.; Kyrpides, N. Genome sequence of Microvirga lupini strain LUT6T, a novel Lupinus alphaproteobacterial microsymbiont from Texas. Stand. Genom. Sci. 2014, 9, 1159–1167. [Google Scholar] [CrossRef] [PubMed]
  168. Radl, V.; Simões-Araújo, J.L.; Leite, J.; Passos, S.R.; Martins, L.M.; Xavier, G.R.; Rumjanek, N.G.; Baldani, J.I.; Zilli, J.E. Microvirga vignae sp. nov., a root nodule symbiotic bacterium isolated from cowpea grown in semi-arid Brazil. Int. J. Syst. Evol. Microbiol. 2014, 64, 725–730. [Google Scholar] [CrossRef] [PubMed]
  169. Safronova, V.I.; Kuznetsova, I.G.; Sazanova, A.L.; Belimov, A.A.; Andronov, E.E.; Chirak, E.R.; Osledkin, Y.S.; Onishchuk, O.P.; Kurchak, O.N.; Shaposhnikov, A.I.; Willems, A.; Tikhonovich, I.A. Microvirga ossetica sp. nov., a species of rhizobia isolated from root nodules of the legume species Vicia alpestris Steven. Int. J. Syst. Evol. Microbiol. 2017, 67, 94–100. [Google Scholar] [CrossRef] [PubMed]
  170. Flores-Félix, J.D.; Carro, L.; Velázquez, E.; Valverde, Á.; Cerda-Castillo, E.; García-Fraile, P.; Rivas, R. Phyllobacterium endophyticum sp. nov., isolated from nodules of Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 2013, 63, 821–826. [Google Scholar] [CrossRef] [PubMed]
  171. Valverde, A.; Velázquez, E.; Fernández-Santos, F.; Vizcaino, N.; Rivas, R.; Mateos, P.F.; Martínez-Molina, E.; Igual, J.M.; Willems, A. Phyllobacterium trifolii sp nov., nodulating Trifolium and Lupinus in Spanish soils. Int. J. Syst. Evol. Microb. 2005, 55, 1985–1989. [Google Scholar] [CrossRef] [PubMed]
  172. Beghalem, H.; Aliliche, K.; Chriki, A.; Landoulsi, A. Molecular and phenotypic characterization of endophytic bacteria isolated from sulla nodules. Microb. Pathog. 2017, 111, 225–231. [Google Scholar] [CrossRef] [PubMed]
  173. Simonsen, A.K.; Dinnage, R.; Barrett, L.G.; Prober, S.M.; Thrall, P.H. Symbiosis limits establishment of legumes outside their native range at a global scale. Nat. Commun. 2017, 8, 14790. [Google Scholar] [CrossRef] [PubMed]
  174. Le Roux, J.J.; Hui, C.; Keet, J.H.; Ellis, A.G. Co-introduction vs ecological fitting as pathways to the establishment of effective mutualisms during biological invasions. New Phytol. 2017, 215, 1354–1360. [Google Scholar] [CrossRef] [PubMed]
  175. Pahua, V.J.; Stokes, P.J.N.; Hollowell, A.C.; Regus, J.U.; Gano-Cohen, K.A.; Wendlandt, C.E.; Quides, K.W.; Lyu, J.Y.; Sachs, J.L. Fitness variation among host species and the paradox of ineffective rhizobia. J. Evol. Biol. 2018. [Google Scholar] [CrossRef] [PubMed]
  176. Jabbouri, S.; Relić, B.; Hanin, M.; Kamalaprija, P.; Burger, U.; Promé, D.; Promé, J.C.; Broughton, W.J. nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. J. Biol. Chem. 1998, 273, 12047–12055. [Google Scholar] [CrossRef] [PubMed]
  177. Reeve, W.; Ardley, J.; Tian, R.; Eshragi, L.; Yoon, J.W.; Ngamwisetkun, P.; Seshadri, R.; Ivanova, N.N.; Kyrpides, N.C. A Genomic Encyclopedia of the Root Nodule Bacteria: assessing genetic diversity through a systematic biogeographic survey. Stand. Genom. Sci. 2015, 10, 14. [Google Scholar] [CrossRef] [PubMed]
Figure 1. A Bayesian posterior probability consensus tree based on 1408 bps of 16S rRNA derived from 16 rhizobial and 4 related genera (the genera nodulating Genisteae are in bold case-underlined). The strains used for this construction and the 16S rRNA Genbank accession numbers were: Rhizobium leguminosarum ATCC 10004 (U29386), Sinorhizobium fredii ATCC 35423 (X67231), Allorhizobium undicola ATCC 700741 (Y17047), Pararhizobium capsulatum ATCC 43294 (X73042), Neorhizobium galegae ATCC 43677 (D11343), Shinella zoogloeoides ATCC 19623 (AB238789), Ciceribacter lividus MSSRFBL1 (NR 135717), Mesorhizobium loti ATCC 700743 (X67229), Aminobacter anthyllidis STM 4645(FR869633), Phyllobacterium brassicacearum LMG 22836 (AY785319), Ochrobactrum lupini LMG 22726 (AY457038), Methylobacterium marchantiae DSM 21328 (FJ157976), Bradyrhizobium lupini USDA 3051 (KM114861), Bosea lupini LMG 26383 (FR774992), Azorhizobium oxalatiphilum DSM 18749 (FR799325), Labrys okinawensis DSM 18385 (AB236169), Devosia honganensis ACCC 19737 (KP339871), Paraburkholderia caribensis CCUG 42847 (Y17009), Cupriavidus alkaliphilus LMG 26294 (HQ438078), and Microvirga lupini LMG 26460 (EF191408). The 16S rRNA sequences were aligned in MUSCLE [16] and implemented in MEGA 6.0 [17]. The Bayesian analyses were performed using BEAST 1.7 software [18]. The model of nucleotide evolution used in all of the analyses was GTR + I + G, as selected by the jModel Test software [19]. The Yule process was selected as a tree prior to Bayesian analysis, 10,000,000 generations were performed and the tree was visualized and edited using FigTree version 1.3.1 software [20].
Figure 1. A Bayesian posterior probability consensus tree based on 1408 bps of 16S rRNA derived from 16 rhizobial and 4 related genera (the genera nodulating Genisteae are in bold case-underlined). The strains used for this construction and the 16S rRNA Genbank accession numbers were: Rhizobium leguminosarum ATCC 10004 (U29386), Sinorhizobium fredii ATCC 35423 (X67231), Allorhizobium undicola ATCC 700741 (Y17047), Pararhizobium capsulatum ATCC 43294 (X73042), Neorhizobium galegae ATCC 43677 (D11343), Shinella zoogloeoides ATCC 19623 (AB238789), Ciceribacter lividus MSSRFBL1 (NR 135717), Mesorhizobium loti ATCC 700743 (X67229), Aminobacter anthyllidis STM 4645(FR869633), Phyllobacterium brassicacearum LMG 22836 (AY785319), Ochrobactrum lupini LMG 22726 (AY457038), Methylobacterium marchantiae DSM 21328 (FJ157976), Bradyrhizobium lupini USDA 3051 (KM114861), Bosea lupini LMG 26383 (FR774992), Azorhizobium oxalatiphilum DSM 18749 (FR799325), Labrys okinawensis DSM 18385 (AB236169), Devosia honganensis ACCC 19737 (KP339871), Paraburkholderia caribensis CCUG 42847 (Y17009), Cupriavidus alkaliphilus LMG 26294 (HQ438078), and Microvirga lupini LMG 26460 (EF191408). The 16S rRNA sequences were aligned in MUSCLE [16] and implemented in MEGA 6.0 [17]. The Bayesian analyses were performed using BEAST 1.7 software [18]. The model of nucleotide evolution used in all of the analyses was GTR + I + G, as selected by the jModel Test software [19]. The Yule process was selected as a tree prior to Bayesian analysis, 10,000,000 generations were performed and the tree was visualized and edited using FigTree version 1.3.1 software [20].
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Figure 2. Maximum likelihood (ML) phylogeny of concatenated recA and glnII partial gene sequences (425 bp + 519 bp), comprising type strains of Bradyrhizobium species with the exception of species, in which recA sequences were missing: Bradyrhizobium betae LMG 21987, Bradyrhizobium guangdongense CCBAU 51649, Bradyrhizobium guangxiense CCBAU 53363, Bradyrhizobium icense LMTR 13 and Bradyrhizobium ingae BR 10250. The scale bar indicates the number of substitutions per site. Bootstrap values >70% (percentage of 500 replicates calculated under distance criteria) are given at the branching nodes. The sequences of Rhodopseudomonas boonkerdii NS23, M. loti NZP2213, Sinorhizobium meliloti 1021 and R. leguminosarum 3841 were used as outgroups. The sequences were aligned using ClustalW software and ML phylogenies were inferred with Mega 6 [17] using the best-fit nucleotide substitution models as indicated by jModelTest 2.1.4. [115]. The distances were calculated according to the GTR+I+G model. Arrows indicate Bradyrhizobium species that nodulate Genisteae plants. Asterisk denotes Bradyrhizobium algeriensis, which has not been formally recognized.
Figure 2. Maximum likelihood (ML) phylogeny of concatenated recA and glnII partial gene sequences (425 bp + 519 bp), comprising type strains of Bradyrhizobium species with the exception of species, in which recA sequences were missing: Bradyrhizobium betae LMG 21987, Bradyrhizobium guangdongense CCBAU 51649, Bradyrhizobium guangxiense CCBAU 53363, Bradyrhizobium icense LMTR 13 and Bradyrhizobium ingae BR 10250. The scale bar indicates the number of substitutions per site. Bootstrap values >70% (percentage of 500 replicates calculated under distance criteria) are given at the branching nodes. The sequences of Rhodopseudomonas boonkerdii NS23, M. loti NZP2213, Sinorhizobium meliloti 1021 and R. leguminosarum 3841 were used as outgroups. The sequences were aligned using ClustalW software and ML phylogenies were inferred with Mega 6 [17] using the best-fit nucleotide substitution models as indicated by jModelTest 2.1.4. [115]. The distances were calculated according to the GTR+I+G model. Arrows indicate Bradyrhizobium species that nodulate Genisteae plants. Asterisk denotes Bradyrhizobium algeriensis, which has not been formally recognized.
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Figure 3. Maximum likelihood (ML) tree based on bradyrhizobial nifD gene sequences (759 bp). The significance of each branch is indicated by the bootstrap percentage calculated for 500 bootstraps. The bootstrap values greater than 70% are indicated at nodes. The sequences were aligned using ClustalW software and ML phylogenies were inferred with Mega 6 [17] using the best-fit nucleotide substitution models, as indicated by jModelTest 2.1.4. [115]. The distances were calculated according to the HKY+I+G model. Because of the substitution saturation that is associated with the third codon position in the nifD dataset, as estimated using DAMBE 5 [133] these positions were excluded from further analysis. The number of sequences used in the construction of this phylogenetic tree is given in brackets: Bradyrhizobium: (640); Rhodopseudomonas (29); Paraburkholderia/Burkholderia (19); Mesorhizobium (22); Microvirga (3); Azorhizobium (2). The number of Bradyrhizobium sequences included in a particular clade or branch is also shown in brackets: Clade I (54), Clade II (106), Clade III(III.1) (2), Clade III(III.2) (33), Clade III(III.3A) (31), Clade III(III.3B) (22), Clade III(III.3C) (87), Clade III(III.3D) (54), Clade III(III.3E) (9), Clade III(III.3F) (8), Clade III(III.3G) (3), Clade III(III.3H) (12), Clade III(III.4) (33), Clade IV (41), Clade V (14), Clade VI (7), Clade VII (64), Clade X (9), Clade XI (2), Clade XVI (10), Clade XVIII (6), Clade XIX (7), Clade XX (15). Black arrows indicate Bradyrhizobium species nodulating Genisteae plants.
Figure 3. Maximum likelihood (ML) tree based on bradyrhizobial nifD gene sequences (759 bp). The significance of each branch is indicated by the bootstrap percentage calculated for 500 bootstraps. The bootstrap values greater than 70% are indicated at nodes. The sequences were aligned using ClustalW software and ML phylogenies were inferred with Mega 6 [17] using the best-fit nucleotide substitution models, as indicated by jModelTest 2.1.4. [115]. The distances were calculated according to the HKY+I+G model. Because of the substitution saturation that is associated with the third codon position in the nifD dataset, as estimated using DAMBE 5 [133] these positions were excluded from further analysis. The number of sequences used in the construction of this phylogenetic tree is given in brackets: Bradyrhizobium: (640); Rhodopseudomonas (29); Paraburkholderia/Burkholderia (19); Mesorhizobium (22); Microvirga (3); Azorhizobium (2). The number of Bradyrhizobium sequences included in a particular clade or branch is also shown in brackets: Clade I (54), Clade II (106), Clade III(III.1) (2), Clade III(III.2) (33), Clade III(III.3A) (31), Clade III(III.3B) (22), Clade III(III.3C) (87), Clade III(III.3D) (54), Clade III(III.3E) (9), Clade III(III.3F) (8), Clade III(III.3G) (3), Clade III(III.3H) (12), Clade III(III.4) (33), Clade IV (41), Clade V (14), Clade VI (7), Clade VII (64), Clade X (9), Clade XI (2), Clade XVI (10), Clade XVIII (6), Clade XIX (7), Clade XX (15). Black arrows indicate Bradyrhizobium species nodulating Genisteae plants.
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Table 1. Genisteae species and their rhizobium symbionts.
Table 1. Genisteae species and their rhizobium symbionts.
Tribes and GeneraGeographical OriginRhizobium Symbionts and Sources
Genisteae
Adenocarpus
Adenocarpus decorticansMoroccoRhizobium [22]
Adenocarpus foliolosusSpain-Canary IslandsBradyrhizobium [23,24]
Adenocarpus hispanicusSpainPhyllobacterium [25]; Bradyrhizobium [26]
Argyrolobium
Argyrolobium lunareSouth AfricaMesorhizobium [27]
Argyrolobium rupestreSouth AfricaBradyrhizobium [28]
Argyrolobium sericeumSouth AfricaBradyrhizobium [28]
Argyrolobium velutinumSouth AfricaMesorhizobium [27]
Argyrolobium uniflorumSenegal, TunisiaRhizobium, Sinorhizobium (=Ensifer) [29,30]; Sinorhizobium [31,32]; Rhizobium [33]
Calicotome
Calicotome infestaItalyBradyrhizobium [34]
Calicotome spinosaItalyBradyrhizobium, Rhizobium [34]
Chamaecytisus
Chamaecytisus proliferusMorocco, Spain-Canary Islands, New ZealandBradyrhizobium [23,24,35,36,37,38]
Chamaecytisus ratisbonensisPolandBradyrhizobium [39]
Chamaecytisus ruthenicusRussiaBradyrhizobium [40]
Cytisus
Cytisus aeolicusItalyBradyrhizobium [34]
Cytisus arboreusMoroccoRhizobium [22]
Cytisus balansaeSpainBradyrhizobium [41,42,43]
Cytisus grandiflorusPortugalBradyrhizobium [21,44]
Cytisus laburnumSpainBradyrhizobium [25]
Cytisus multiflorusSpainBradyrhizobium [41,42,43]
Cytisus proliferusSpain-Canary IslandsBradyrhizobium [21,44]
Cytisus purgansSpainAgrobacterium, Rhizobium [25]
Cytisus scopariusBelgium, Ireland, Poland, Spain, UK, USA; Australia, New ZealandBradyrhizobium [21,37,38,39,41,44,45]; Bradyrhizobium, Mesorhizobium, Rhizobium [46]; Ochrobactrum cytisi [47]; Bradyrhizobium, Ensifer, Rhizobium, Phyllobacterium [48]
Cytisus striatusSpainBradyrhizobium [39,42]
Cytisus triflorusAlgeria, MoroccoBradyrhizobium [49,50]
Cytisus villosusAlgeria, MoroccoBradyrhizobium [49,50,51,52,53]
Genista
Genista aspalathoidesItalyBradyrhizobium Clade II and Clade IV [34]
Genista germanicaPolandBradyrhizobium [39]
Genista hystrixSpainBradyrhizobium [41,42]
Genista linifoliaSpainBradyrhizobium [54]
Genista monspessulanaSpainBradyrhizobium [54]
Genista saharaeAlgeria, TunisiaEnsifer, Phyllobacterium, Mesorhizobium, Rhizobium [55]; Ensifer [31]; Ensifer, Mesorhizobium, Neorhizobium [56]
Genista stenopetalaSpain-Canary IslandsBradyrhizobium [21,44]
Genista sylvestrisCroatiaBradyrhizobium [21]
Genista tinctoriaPoland, Russia, SloveniaBradyrhizobium [21,57,58]; Phyllobacterium, Rhizobium, Bradyrhizobium [40]
Genista versicolorSpainBradyrhizobium [59]
Laburnum
Laburnum anagyroidesBelgium, CroatiaBradyrhizobium [21,25]; Bradyrhizobium [48]
Lupinus
Lupinus albescensBrazilBradyrhizobium [60,61]
Lupinus albusPoland, SpainMesorhizobium [62,63]; Bradyrhizobium [44,60,64,65,66,67]
Lupinus angustifoliusAustralia, Poland, South Africa, SpainBradyrhizobium [60,64,65,68,69]
Lupinus arboreusUSA-California, New ZealandBradyrhizobium [37,70,71]
Lupinus bandelieraeBoliviaBradyrhizobium [60]
Lupinus bicolorUSA-CaliforniaBradyrhizobium [71]
Lupinus bracteolarisBrazilBradyrhizobium [60]
Lupinus breviscapusBoliviaBradyrhizobium [60]
Lupinus campestrisMexicoBradyrhizobium [60]
Lupinus cosentiniiAustralia, SpainBradyrhizobium [64,68]
Lupinus hispanicusSpainBradyrhizobium [64]
Lupinus honoratusArgentinaOchrobactrum [72]
Lupinus lepidusUSA-WashingtonBradyrhizobium [53,70]
Lupinus leucophyllusUSA-WashingtonBradyrhizobium [70]
Lupinus luteusPoland, Spain, USABradyrhizobium, Mesorhizobium [73]; Bradyrhizobium [64,65,69]
Lupinus mariae-josephaeSpainBradyrhizobium [64,74,75,76,77]
Lupinus micranthusAlgeria, Spain, TunisiaBradyrhizobium [64,78]; Bradyrhizobium, Microvirga, Phyllobacterium [79,80]
Lupinus misticolaPeruBradyrhizobium [60]
Lupinus montanusMexico-MorelosBradyrhizobium [24]
Lupinus mutabilisEcuadorBradyrhizobium [60]
Lupinus nootkatensisUSA-AlaskaBradyrhizobium [60,70]
Lupinus paraguariensisBrazilBradyrhizobium [60]
Lupinus paranensisBrazilBradyrhizobium [60]
Lupinus perennisUSABradyrhizobium [81,82]
Lupinus polyphyllusBelgium, Germany, New Zealand, PolandBosea [83]; Bradyrhizobium [24,60,84,85]; Bradyrhizobium, Rhizobium [48]
Lupinus pycnostachysBoliviaBradyrhizobium [60]
Lupinus rubriflorusBrazil,Bradyrhizobium [60]
Lupinus sericeusUSA-WashingtonBradyrhizobium [70]
Lupinus simulansMexico-OaxacaBradyrhizobium [53,70]; Bradyrhizobium [53]
Lupinus succulentusUSA-CaliforniaMesorhizobium [86]
Lupinus texensisUSA-TexasMicrovirga [87]
Lupinus tominensisBoliviaBradyrhizobium [60]
Lupinus uleanusBrazilBradyrhizobium [60]
Retama
Retama monospermaAlgeria, Morocco, SpainBradyrhizobium [88,89]
Retama raetamAlgeria, TunisiaAgrobacterium, Mesorhizobium, Rhizobium, Sinorhizobium (Ensifer) [90,91]; Bradyrhizobium [92]; Sinorhizobium [31]
Retama sphaerocarpaAlgeria, Morocco, SpainBradyrhizobium [21,41,88,92,93]; Bradyrhizobium, Phyllobacterium [25]
Spartium
Spartium junceumCroatia, Italy, Slovenia, SpainBradyrhizobium [21,34,50,94]; Bradyrhizobium, Phyllobacterium [25]
Teline
Teline canarienseSpainBradyrhizobium [23,24,35]
Teline monspessulanaItalyMesorhizobium [34]
Teline stenopetalaSpainBradyrhizobium [34]
Ulex
Ulex europaeusNew Zealand, PortugalBradyrhizobium [38,44,48,95,96]

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MDPI and ACS Style

Stępkowski, T.; Banasiewicz, J.; Granada, C.E.; Andrews, M.; Passaglia, L.M.P. Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae. Genes 2018, 9, 163. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9030163

AMA Style

Stępkowski T, Banasiewicz J, Granada CE, Andrews M, Passaglia LMP. Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae. Genes. 2018; 9(3):163. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9030163

Chicago/Turabian Style

Stępkowski, Tomasz, Joanna Banasiewicz, Camille E. Granada, Mitchell Andrews, and Luciane M. P. Passaglia. 2018. "Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae" Genes 9, no. 3: 163. https://0-doi-org.brum.beds.ac.uk/10.3390/genes9030163

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