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Rhizobia Isolated from the Relict Legume Vavilovia Formosa Represent a Genetically Specific Group Within Rhizobium Leguminosarum Biovar Viciae

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Rhizobia Isolated from the Relict Legume Vavilovia Formosa Represent a Genetically Specific Group Within Rhizobium Leguminosarum Biovar Viciae G C A T T A C G G C A T genes Article Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae Anastasiia K. Kimeklis 1,2,* , Elizaveta R. Chirak 1, Irina G. Kuznetsova 1 , Anna L. Sazanova 1, Vera I. Safronova 1, Andrey A. Belimov 1 , Olga P. Onishchuk 1, Oksana N. Kurchak 1, Tatyana S. Aksenova 1, Alexander G. Pinaev 1, Evgeny E. Andronov 1,2,3 and Nikolay A. Provorov 1 1 All-Russian Research Institute of Agricultural Microbiology, 196608 Saint Petersburg, Russia; [email protected] (E.R.C.); [email protected] (I.G.K.); [email protected] (A.L.S.); [email protected] (V.I.S.); [email protected] (A.A.B.); [email protected] (O.P.O.); [email protected] (O.N.K.); [email protected] (T.S.A.); [email protected] (A.G.P.); [email protected] (E.E.A.); [email protected] (N.A.P.) 2 Saint-Petersburg State University, 199034 Saint Petersburg, Russia 3 V.V. Dokuchaev Soil Science Institute of Russian Academy of Science, 119017 Moscow, Russia * Correspondence: [email protected]; Tel.: +7-(921)-350-22-02 Received: 23 October 2019; Accepted: 27 November 2019; Published: 1 December 2019 Abstract: Twenty-two rhizobia strains isolated from three distinct populations (North Ossetia, Dagestan, and Armenia) of a relict legume Vavilovia formosa were analysed to determine their position within Rhizobium leguminosarum biovar viciae (Rlv). These bacteria are described as symbionts of four plant genera Pisum, Vicia, Lathyrus, and Lens from the Fabeae tribe, of which Vavilovia is considered to be closest to its last common ancestor (LCA). In contrast to biovar viciae, bacteria from Rhizobium leguminosarum biovar trifolii (Rlt) inoculate plants from the Trifolieae tribe. Comparison of house-keeping (hkg: 16S rRNA, glnII, gltA, and dnaK) and symbiotic (sym: nodA, nodC, nodD, and nif H) genes of the symbionts of V. formosa with those of other Rlv and Rlt strains reveals a significant group separation, which was most pronounced for sym genes. A remarkable feature of the strains isolated from V. formosa was the presence of the nodX gene, which was commonly found in Rlv strains isolated from Afghanistan pea genotypes. Tube testing of different strains on nine plant species, including all genera from the Fabeae tribe, demonstrated that the strains from V. formosa nodulated the same cross inoculation group as the other Rlv strains. Comparison of nucleotide similarity in sym genes suggested that their diversification within sym-biotypes of Rlv was elicited by host plants. Contrariwise, that of hkg genes could be caused by either local adaptation to soil niches or by genetic drift. Long-term ecological isolation, genetic separation, and the ancestral position of V. formosa suggested that symbionts of V. formosa could be responsible for preserving ancestral genotypes of the Rlv biovar. Keywords: Rhizobium leguminosarum bv. viciae; Vavilovia formosa (Stev.) Fed.; tribe Fabeae; evolution of symbiosis; housekeeping genes (hkg); symbiotic (sym) genes; group separation 1. Introduction Root nodule bacteria (rhizobia) represent a useful model for studying the molecular and ecological mechanisms of evolution of symbiotic bacteria. Divergent evolution (intra-species radiation and formation of new species) by these bacteria is promoted by host plants, which elicit the selection pressures responsible for the genetic and ecological diversification of rhizobia [1–3]. This evolution Genes 2019, 10, 991; doi:10.3390/genes10120991 www.mdpi.com/journal/genes Genes 2019, 10, 991 2 of 17 may be traced using specialised symbiotic (sym) genes representing the accessory parts of bacterial genomes,Genes 2019 which, 10, x diFORffer PEER in theirREVIEW natural histories from housekeeping genes (hkg) representing2 of the 18 core partsevolution of genomes may [ 4be]. traced As a resultusing specialised of co-evolutionary symbiotic processes,(sym) genes symbiosisrepresenting is the formed accessory between parts of tightly co-adaptedbacterial cross-inoculation genomes, which differ groups in their of rhizobia natural andhistories legumes, from housekeeping and their coevolution genes (hkg is) representing directed by a set of symbiosis-specificthe core parts of genomes genes from [4]. As each a result partner of co [5-evolutionary–7]. In some processes, rhizobia, symbiosissym genes is areformed more between susceptible to autonomoustightly co-adapted horizontal cross gene-inoculation transfer thangroupshkg ofgenes, rhizobia because and theylegumes, are locatedand their on coevolution plasmids—mobile is elementsdirected of the by genomea set of symbiosis [3]. This- resultsspecific ingenes an intensive from each recombination partner [5–7]. In of some host rhizobia, specific andsym chromosomalgenes are markersmore [8 susceptible]. For example, to autonomousRhizobium horizontal leguminosarum gene transferis composed than hkg of genes, two because biovars, they which are havelocated diverged on basedplasmids on their—mobile plasmid-encoded elements of the host genom rangese [3]. [9 ].This Biovar resultsviciae in an (intensiveRlv) nodulates recombination legumes of fromhost the specific and chromosomal markers [8]. For example, Rhizobium leguminosarum is composed of two Fabeae tribe, while biovar trifolii (Rlt) nodulates clovers from the Trifolieae tribe; however, they show a biovars, which have diverged based on their plasmid-encoded host ranges [9]. Biovar viciae (Rlv) conservative chromosomal arrangement of hkg markers (Figure1). nodulates legumes from the Fabeae tribe, while biovar trifolii (Rlt) nodulates clovers from the EvenTrifolieae so, divergenttribe; however, evolution they show of rhizobia a conservative is not restrictedchromosomal to sym arrangementgenes. Application of hkg markers of (Figure the average nucleotide1). identity (ANI) method has demonstrated that a local R. leguminosarum population could be separatedEven into so, five divergent genomic evolution species, of di rhizobiaffering inis not their restrictedhkg genes, to sym representing genes. Application their core of the genomes average [10]. However,nucleotide this speciationidentity (ANI) does method not correlate has demonstrated with the diversificationthat a local R. leguminosarum of R. leguminosarum populationinto could biovars viciaebeand separatedtrifolii, suggestinginto five genomic that hkg species,and sym differinggene in evolution their hkgis genes, controlled representing by diff theirerent core mechanisms. genomes We decided[10]. to However, probe this this hypothesis speciationusing does not the correlate model of withRlv, the a symbiont diversification of the of legume R. leguminosarum tribe Fabeae, into which includesbiovars five viciae genera: andLens trifolii, Lathyrus, suggesting, Pisum that, Vicia hkg, andand Vaviloviasym gene[ 11evolution]. The latter is controlled genus consists by different of a single mechanisms. We decided to probe this hypothesis using the model of Rlv, a symbiont of the legume species, Vavilovia formosa (Stev.) Fed., a relict and endangered legume plant, which grows mostly in tribe Fabeae, which includes five genera: Lens, Lathyrus, Pisum, Vicia, and Vavilovia [11]. The latter high-mountain regions of the Caucasus and Middle East [12–15]. Based on genetic and morphological genus consists of a single species, Vavilovia formosa (Stev.) Fed., a relict and endangered legume plant, markers,whichVavilovia grows mostlyis closely in high related-mountain to Pisum regions, such of thatthe Caucasus it is still sometimesand Middle attribute East [12– to15]. this Based genus on [16]. Basedgenetic on a number and morphological of phenotypic markers, traits, VaviloviaV. formosa is closelyis considered related to Pisum to be, thesuch closest that it is living still sometimes relative to the last commonattribute ancestorto this genus (LCA) [16]. of Based the Fabeaeon a number tribe of [17 phenotypic]. Due to hard-to-reachtraits, V. formosa niches, is considered scarce to populations, be the and theclosest deeply living growing relativeroots to the of lastV. formosacommon, itancestor is challenging (LCA) of to the obtain Fabeae a representativetribe [17]. Due collectionto hard-to- of its symbionts.reach niches, Nevertheless, scarce populations, symbionts and representing the deeply growing a local populationroots of V. formosa in North, it is challenging Ossetia were to obtain previously describeda representative [18]. Most collection of the isolates of its symbionts. were identified Nevertheless, as Rlv, symbionts with some representing isolates belonging a local population to the genera Bosea,inTardiphaga North Ossetia, and werePhyllobacterium previously. described A remarkable [18]. Most feature of ofthe these isolatesRlv wereisolates identified was that as theRlv,nod withX gene some isolates belonging to the genera Bosea, Tardiphaga, and Phyllobacterium. A remarkable feature of was found in all strains [18]. This gene enables rhizobia to nodulate the highly selective Afghanistan these Rlv isolates was that the nodX gene was found in all strains [18]. This gene enables rhizobia to pea lines, which have a specific allele of the sym2 gene, sym2A, which restricts nodulation by Rlv strains nodulate the highly selective Afghanistan pea lines, which have a specific allele of the sym2 gene, devoidsym of2A,nod whichX[19 restricts]. nodulation by Rlv strains devoid of nodX [19]. FigureFigure 1. Plant 1. Plant hosts hosts of Rlv of Rlvand andRlt Rlton on the the scheme scheme of of Fabeae Fabeae
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