Recapitulative results of root nodule symbionts from Northwestern African wild legumes.
Abstract
The present review discusses the phylogenomic diversity of root nitrogen-fixing bacteria associated to wild legumes under North African soils. The genus Ensifer is a dominant rhizobium lineage nodulating the majority of the wild legumes, followed by the genus Rhizobium and Mesorhizobium. In addition, to the known rhizobial genera, two new Microvirga and Phyllobacterium genera were described as real nodulating and nitrogen-fixing microsymbiotes from Lupinus spp. The promising rhizobia related to nitrogen fixation efficiency in association with some legumes are shared. Phylogenetic studies are contributing greatly to our knowledge of relationships on both sides of the plant-bacteria nodulation symbiosis. Multiple origins of nodulation (perhaps even within the legume family) appear likely. However, all nodulating flowering plants are more closely related than previously suspected, suggesting that the predisposition to nodulate might have arisen only once. The origins of nodulation, and the extent to which developmental programs are conserved in nodules, remain unclear, but an improved understanding of the relationships between nodulin genes is providing some clues.
Keywords
- rhizobia
- North Africa
- symbiosis
- legumes
- phylogenomic
1. Introduction
Africa has a vast array of indigenous legumes, ranging from large rain forest trees to small annual herbs [1]. However, in recent years, there has been a tendency in agriculture and forestry to use exotic species for crops and wood. As has been pointed out several times over nearly 30 years, most recently [2], by the US National Academy of Sciences, this ignores the potential of the native species, which are arguably better adapted to their environment. For this review, the nodulated indigenous legume genera in Northwestern Africa with known uses have been selected to illustrate the problems and potential for their better exploitation.
The wild legume flora in Northwestern Africa is rich, with great specific and infraspecific diversity [3]. The overgrazing and expansion of agriculture has gradually led to the regression and extinction of many pastoral and forage species. In addition, desertification causes disturbance of plant-microbe symbioses, which are a critical ecological factor in helping further plant growth in degraded ecosystems [4]. In this context, the establishment of indigenous pastoral legume species associated with their appropriate symbiotic bacterial partners may be of increased value for success in soil fertility restoration. Biological N2 fixation (BNF) is the major way for N input into desert ecosystems. Rhizobium-legume symbioses represent the major mechanism of BNF in arid lands, compared with the N2-fixing heterotrophs and associative bacteria [5, 6] and actinorhizal plants [7, 8]. Deficiency in mineral N often limits plant growth, and so symbiotic relationships have evolved between plants and a variety of N2-fixing organisms [9]. The symbiotically fixed N2 by the association between rhizobium species and the legumes represents a renewable source of N for agriculture. Values estimated for various legume crops and pasture species are often impressive [10]. In addition to crop legumes, the nodulated wild (herb and tree) legumes have potential for nitrogen fixation and reforestation and to control soil erosion [11]. It has been reported that a novel, suitable wild legume-rhizobia associations are useful in providing a vegetational cover in degraded lands [12].
Considering the major ecological importance of many wild legumes such as
Therefore, understanding the nature of indigenous populations of rhizobia-nodulating wild legumes is of considerable agricultural significance. It is also of interest to identify a wider variety of bacterial strains in a bid to define new strains for the production of inoculants for smallholder farms.
2. Genetics and functional genomics of legume nodulation
The interaction between rhizobia and legumes in root nodules is an essential element in sustainable agriculture, as this symbiotic association is able to enhance biological fixation of atmospheric nitrogen (N2) and is also a paradigm in plant-microbe signaling [14, 15, 16]. The knowledge of the whole genome would allow the specific features of each rhizobium to be identified. The prominent feature of this group of bacteria is their molecular dialog with plant hosts, an interaction that is enabled by the presence of a series of symbiotic genes encoding for the synthesis and export of signals triggering organogenetic and physiological responses in the plant [17, 18]. In recent years, significant progress has been made in resolving the complex exchange of signals responsible for nodulation through genome assembly, mutational and expression analysis, and proteome characterization of legumes [14, 19, 20] and rhizobia [15, 21, 22, 23].
3. Phylogenomic of wild legume root nitrogen-fixing symbionts
The known diversity of rhizobia increases annually and is the subject of several reviews, the most recent and comprehensive being that of [24]. It is not our intention to revisit this subject nor the genetic basis of nodulation [25, 26], the horizontal transfer of symbiosis-related genes [23], or the symbiovar concept [27] but instead to attempt to link, where possible, rhizobial genotypes with their geographical locations and/or legume tribes/genera. At the time of writing, rhizobia consist of a diverse range of genera in the Alphaproteobacterial and Betaproteobacterial classes and are termed “alpha-rhizobia” and “beta-rhizobia,” respectively (Figure 1).
3.1 The genus Bradyrhizobium (Bradyrhizobiaceae )
The
For the
3.2 The genus Mesorhizobium (Phyllobactericeae )
The genus
For subtribe
3.3 The genus Rhizobium (Rhizobiaceae )
The genus
For
3.4 The genus Ensifer (Sinorhizobium) (Rhizobiaceae)
The genera
Bacteria belonging to
3.5 The genus Neorhizobium (Rhizobiaceae )
The genus
3.6 The genus Phyllobacterium (Phyllobactericeae )
The
3.7 The genus Microvirga (Methylobacteriaceae )
The genus
Table 1 shows the root nodule symbionts from Northwestern African wild legumes.
Subfamily tribe | Genus | Species | Symbiont | Geographic origin |
---|---|---|---|---|
Acacieae | Tunisia, Morocco | |||
Tunisia, Morocco | ||||
Tunisia, Morocco | ||||
Tunisia, Morocco | ||||
Algeria, Morocco | ||||
Algeria | ||||
Algeria | ||||
Algeria | ||||
Algeria | ||||
Algeria | ||||
Mimosae | Tunisia | |||
Galegae | Tunisia | |||
Tunisia | ||||
Tunisia | ||||
Morocco, Tunisia | ||||
Morocco | ||||
Morocco | ||||
Genisteae | Tunisia | |||
Morocco | ||||
Morocco | ||||
Morocco | ||||
Morocco | ||||
Algeria, Morocco | ||||
Algeria, Tunisia | ||||
Algeria, Tunisia | ||||
Tunisia | ||||
Algeria | ||||
Algeria, Morocco | ||||
Algeria, Tunisia, Morocco | ||||
Algeria, Morocco | ||||
Hedysareae | Tunisia | |||
Morocco | ||||
Tunisia | ||||
Tunisia | ||||
Tunisia | ||||
Loteae | Tunisia | |||
Tunisia | ||||
Tunisia | ||||
Tunisia | ||||
Tunisia | ||||
Tunisia | ||||
Algeria, Tunisia | ||||
Algeria | ||||
Algeria | ||||
Algeria | ||||
Tunisia | ||||
Tunisia | ||||
Algeria | ||||
Trifolieae | Morocco | |||
Morocco | ||||
Algeria | ||||
Algeria, Tunisia | ||||
Tunisia | ||||
Tunisia | ||||
Tunisia, Algeria, Morocco | ||||
Tunisia, Algeria, Morocco | ||||
Tunisia, Algeria, Morocco | ||||
Algeria, Tunisia | ||||
Tunisia, Algeria, Morocco | ||||
Algeria | ||||
Tunisia | ||||
Tunisia | ||||
Vicieae | Tunisia | |||
Tunisia |
4. Promising nitrogen-fixing rhizobia
The root nodule symbiosis established between legumes and rhizobia is an exquisite biological interaction responsible for fixing a significant amount of nitrogen in terrestrial ecosystems. The success of this interaction depends on the recognition of the right partner by the plant within the richest microbial ecosystems on Earth, the soil. Recent metagenomic studies of the soil biome have revealed its complexity, which includes microorganisms that affect plant fitness and growth in a beneficial, harmful, or neutral manner. In this complex scenario, understanding the molecular mechanisms by which legumes recognize and discriminate rhizobia from pathogens, but also between distinct rhizobia species and strains that differ in their symbiotic performance, is a considerable challenge.
By symbiotic efficiency and properties, strains isolated from wild legumes varied in their symbiosis effectiveness with their host plant of origin. A great diversity among and within isolates was reported by many authors. This symbiotic diversity within and between isolates growing in diverse geographical areas was also defined by Tinick and Hadobas [85] for other legume plants. All strains were capable of nodulation. Mahdhi et al. [55, 86] reported that two
5. Conclusion
The Mediterranean basin is a hotspot place of legume diversity and the center of diversification of many of them. Our review contributes to enlarge our knowledge on the LNB-legume symbioses. We evidenced the biodiversity among bacteria-nodulating wild legumes in Northwestern Africa and unknown associations were found. Several groups may represent new genospecies to be further characterized to assess their taxonomical status. This work thus opens further interesting perspectives and makes new models available for evolutionary studies and for understanding mechanisms involved in nitrogen-fixing symbiosis.
References
- 1.
Lock JM. Legumes of Africa: A Check List. Kew, England, Royal Botanic Gardens; 1989 - 2.
Anon. Lost Crops of Africa. Washington: National Academy Press; 2006 - 3.
Le Houerou HN. La végétation de la Tunisie steppique (1) (Structure, écologie, sociologie, répartition, évolution, utilisation, biomasse, productivité) (avec référence aux végétations analogues d’Algérie, de Libye et du Maroc). Annales de l’Institut National de la Recherche Agronomique de la Tunisie. 1969; 42 :622 - 4.
Requena N, Pérez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM. Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Applied and Environmental Microbiology. 2001; 67 :495-498 - 5.
Abdel-Ghaffar AS. Aspects of microbial activities and nitrogen fixation in Egyptian desert soils. Arid Soil Research and Rehabilitation. 1989; 3 :281-294 - 6.
Wullstein LH. Evaluation and significance of associative dinitrogen fixation for arid soil rehabilitation. Arid Soil Research and Rehabilitation. 1989; 3 :259-265 - 7.
Caucas V, Abril A. Frankia sp. infectsAtriplex cordobensis -cross-inoculation assay and symbiotic efficiency. Phyton. 1996;59 :103-110 - 8.
Sayed WF, Wheeler CT, Zahran HH, Shoreit AAM. Effect of temperature and moisture on the survival and symbiotic effectiveness of Frankia spp. Biology and Fertility of Soils. 1997;25 :349-353 - 9.
Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X. Molecular basis of symbiosis between rhizobium and legumes. Nature. 1997; 387 :394-401 - 10.
Peoples MB, Ladha JK, Herridge DF. Enhancing legume N2 fixation through plant and soil management. Plant and Soil. 1995; 174 :83-101 - 11.
Ahmad MH, Rafique MU, McLaughlin W. Characterization of indigenous rhizobia from wild legumes. FEMS Microbiology Letters. 1984; 24 :197-203 - 12.
Jha PK, Nair S, Gopinathan MC, Babu CR. Suitability of rhizobia-inoculated wild legumes Argyrolobium flaccidum ,Astragalus graveolens ,Indigofera gangetica andLespedeza stenocarpa in providing a vegetational cover in an unreclaimed lime stone quarry. Plant and Soil. 1995;177 :139-149 - 13.
Sprent JI. Legume Nodulation: A Global Perspective. Oxford, UK: Wiley-Blackwell; 2009 - 14.
Young ND, Debellé F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature. 2011;480 :520-524. DOI: 10.1038/nature10625 - 15.
Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, et al. Legumes symbioses: Absence of nod genes in photosynthetic bradyrhizobia. Science. 2007; 316 :1307-1312. DOI: 10.1126/science.1139548 - 16.
Wang D, Yang SM, Tang F, Zhu HY. Symbiosis specificity in the legume—Rhizobial mutualism. Cellular Microbiology. 2012; 14 :334-342. DOI: 10.1111/j.1462-5822.2011.01736 - 17.
Spaink HP, Wijffelman CA, Pees E, Okker RJH, Lugtenberg BJJ. Rhizobium nodulation gene nod D as a determinant of host specificity. Nature. 1987;328 :337-340. DOI: 10.1038/328337a0 - 18.
Long SR. Genes and signals in the rhizobium-legume symbiosis. Plant Physiology. 2001; 125 :69-72. DOI: 10.1104/pp.125.1.69 - 19.
Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, et al. Genome structure of the legume, Lotus japonicus . DNA Research. 2008;15 :227-239. DOI: 10.1093/dnares/dsn008 - 20.
Marx H, Minogue CE, Jayaraman D, Richards AL, Kwiecien NW, Sihapirani AF, et al. A proteomic atlas of the legume Medicago truncatula and its nitrogen-fixing endosymbiontSinorhizobium meliloti . Nature Biotechnology. 2016;34 :1198-1205. DOI: 10.1038/nbt.3681 - 21.
Tolin S, Arrigoni G, Moscatiello R, Masi A, Navazio L, Sablok G, et al. Quantitative analysis of the naringenin-inducible proteome in Rhizobium leguminosarum by isobaric tagging and mass spectrometry. Proteomics. 2013; 13 :1961-1972. DOI: 10.1002/pmic.201200472 - 22.
Čuklina J, Hahn J, Imakaev M, Omasits U, Förstner KU, Ljubimov N, et al. Genome-wide transcription start site mapping of Bradyrhizobium japonicum grown free-living or in symbiosis—A rich resource to identify new transcripts, proteins and to study gene regulation. BMC Genomics. 2016;17 :302. DOI: 10.1186/s12864-016-2602-9 - 23.
Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends in Microbiology. 2016; 24 :63-75. DOI: 10.1016/j.tim.2015.10.007 - 24.
Peix A, Ramırez-Bahena MH, Velazquez E, Bedmar EJ. Bacterial associations with legumes. Critical Reviews in Plant Sciences. 2015; 34 :17-42 - 25.
Pueppke SG, Broughton WJ. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Molecular Plant-Microbe Interactions. 1999;12 :293-318 - 26.
Perret X, Staehelin C, Broughton WJ. Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews. 2000; 64 :180-201 - 27.
Rogel MA, Ormeno-Orrillo E, Martinez-Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Systematic and Applied Microbiology. 2011; 34 :96-104 - 28.
Sprent JI, Ardley J, James EK. Tansley review: Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytologist. 2017; 215 :40-56. DOI: 10.1111/nph.14474 - 29.
Jordan DC. NOTES: Transfer of Rhizobium japonicum Buchanan 1980 toBradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. International Journal of Systematic and Evolutionary Microbiology. 1982;32 :136-139. DOI: 10.1099/00207713-32-1-136 - 30.
Djouadi S, Amrani S, Bouherama A, Nazhat-Ezzaman N, Aïd F. Nature des rhizobia associés à 15 espèces du genre Lotus en Algérie. Botany. 2017;95 :879-888. DOI: 10.1139/cjb-2017-0020 - 31.
Zakhia F, Jeder H, Domergue O, Willems A, Cleyet-Marel JC, Gillis M, et al. Characterization of wild legume nodulating bacteria (LNB) in the infra-arid zone of Tunisia. Systematic and Applied Microbiology. 2004; 27 :380-395. DOI: 10.1078/0723-2020-00273 - 32.
Amrani S, Nazhat-Ezzaman N, Bhatnagar T. Caractéristiques symbiotiques et génotypiques des Rhizobia associes a Acacia saligna (Labill.) Wendl. dans quelques pépinières en Algérie. Acta Botanica Gallica. 2009;156 :501-513 - 33.
Boukhatem ZF, Domergue O, Bekki A, Merabet C, Sekkour S, Bouazza F, et al. Symbiotic characterization and diversity of rhizobia associated with native and introduced acacias in arid and semi-arid regions in Algeria. FEMS Microbiology Ecology. 2012; 80 :534-547 - 34.
Fikri-Benbrahim K, Chraibi M, Lebrazi S, Moumni M, Ismaili M. Phenotypic and genotypic diversity and symbiotic effectiveness of rhizobia isolated from Acacia sp. grown in Morocco. Journal of Agricultural Science and Technology. 2017;19 :201-216 - 35.
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 theBradyrhizobium genus. Systematic and Applied Microbiology. 2009;32 :245-255. DOI: 10.1016/j.syapm.2009.01.005 - 36.
Hannane FZ, 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. African Journal of Biotechnology. 2016;15 :854-867 - 37.
Guerrouj K, Perez-Valera E, Chahboune R, Abdelmoumen H, Bedmar EJ, El Idrissi MM. Identification of the rhizobial symbiont of Astragalus glombiformis in eastern Morocco asMesorhizobium camelthorni . Antonie Van Leeuwenhoek. 2013;104 :187-198 - 38.
Menna P, Barcellos FG, Hungria M. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region andgln II,rec A,atp D anddna K genes. International Journal of Systematic and Evolutionary Microbiology. 2009;59 :2934-2950 - 39.
Chahboune R, Carro L, Peix A, Barrijal S, Velázquez E, Bedmar EJ. Bradyrhizobium cytisi sp. nov., isolated from effective nodules ofCytisus villosus . International Journal of Systematic and Evolutionary Microbiology. 2011;61 :2922-2927 - 40.
Chahboune R, Carro L, Peix A, Ramirez-Bahena MH, Barrijal S, Velaszquez E, et al. Bradyrhizobium rifense sp. nov. isolated from effective nodules ofCytisus villosus grown in the Moroccan Rif. Systematic and Applied Microbiology. 2012;35 :302-305 - 41.
Ahnia H, Boulila F, Boulila A, Boucheffa K, Durán D, Bourebaba Y, et al. Cytisus villosus from northeastern Algeria is nodulated by genetically diverseBradyrhizobium strains. Antonie Van Leeuwenhoek. 2014;105 :1121-1129. DOI: 10.1007/s10482-014-0173-9 - 42.
Chahboune R, El Akhal MR, Arakrak A, Bakkal M, Laglaoui A, Pueyo JJ, et al. Characterization of bradyrhizobia isolated from root nodules of Cytisus triflorus in the rif occidental of morocco. In: Proceedings of the 15th International Nitrogen Fixation Congress and the 12th International Conference of the African Association for Biological Nitrogen Fixation. 2008. p. 155 - 43.
Bourebaba Y, Durán D, Boulila F, Ahnia H, Boulila A, Temprano F, et al. Diversity of Bradyrhizobium strains nodulatingLupinus micranthus on both sides of the Western Mediterranean: Algeria and Spain. Systematic and Applied Microbiology. 2016;39 :266-274. DOI: 10.1016/j.syapm.2016.04.006 - 44.
Msaddak A, Durán D, Rejili M, Mars M, et al. Diverse bacteria affiliated with the genera Microvirga ,Phyllobacterium andBradyrhizobium nodulateLupinus micranthus growing in soils of Northern Tunisia. Applied and Environmental Microbiology. 2017;83 (6). pii: e02820-16. DOI: 10.1128/AEM.02820-16 - 45.
Msaddak A, Rejili M, Durán D, Rey L, Palacios JM, Imperial J, et al. Definition of two new symbiovars, sv. lupini and sv.mediterranense , within the generaBradyrhizobium and Phyllobacterium efficiently nodulatingLupinus mkicranthus in Tunisia. Systematic and Applied Microbiology. 2018;41 :487-493 - 46.
Jarvis BDW, van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, et al. Transfer of Rhizobium loti ,Rhizobium huakuii ,Rhizobium ciceri ,Rhizobium mediterraneum , andRhizobium tianshanense toMesorhizobium gen. nov. International Journal of Systematic Bacteriology. 1997;47 :895-898 - 47.
Mahdhi M, Houidheg N, Mahmoudi N, Msaadek A, Rejili M, Mars M. Characterization of rhizobial bacteria nodulating Astragalus corrugatus andHippocrepis areolata in Tunisian arid soils. Polish Journal of Microbiology. 2016;65 :331-339 - 48.
Ourarhi M, Abdelmoumen H, Guerrouj K, Benata H, Muresu R, Squartini A, et al. Colutea arborescens is nodulated by diverse rhizobia in Eastern Morocco. Archives of Microbiology. 2011;193 :115-124. DOI: 10.1007/s00203-010-0650-0 - 49.
Rejili M, Lorite MJ, Mahdhi M, Pinilla JS, Ferchichi A, Mars M. Genetic diversity of rhizobial populations recovered from three Lotus species cultivated in the infra-arid Tunisian soils. Progress in Natural Science. 2009; 19 :1079-1087 - 50.
Rejili M, Mahdhi M, Fterich A, Dhaoui S, Guefrachi I, Abdeddayem R, et al. Symbiotic nitrogen fixation of wild legumes in Tunisia: Soil fertility dynamics, field nodulation and nodules effectiveness. Agriculture, Ecosystems and Environment. 2012; 157 :60-69. DOI: 10.1016/j.pnsc.2009.02.003 - 51.
Rejii M, Mahdhi M, Domínguez-Núñez JA, Mars M. The phenotypic, phylogenetic and symbiotic characterization of rhizobia nodulating Lotus sp. in Tunisian arid soils. Annales de Microbiologie. 2013;64 :355-362 - 52.
Roba M, Willems A, Le Quéré A, Maynaud G, Pervent M, et al. Mesorhizobium delmotii andMesorhizobium prunaredense are two new species containing rhizobial strains within the symbiovaranthyllidis . Systematic and Applied Microbiology. 2017;40 :135-143 - 53.
Chaich K, Bekki A, Bouras N, Holtz MD, Soussou S, Maure L, et al. Rhizobial diversity associated with the spontaneous legume Genista saharae in the northeastern Algerian Sahara. Symbiosis. 2017;71 (2):111-120 - 54.
Fterich A, Mahdhi M, Caviedes MA, Pajuelo E, Rivas R, Rodriguez-Llorente ID, et al. Characterization of root-nodulating bacteria associated to Prosopis farcta growing in the arid regions of Tunisia. Archives of Microbiology. 2011;193 :385-397 - 55.
Young JM. Renaming of Agrobacterium larrymoorei Bouzar and Jones 2001 asRhizobium larrymoorei (Bouzar and Jones 2001) comb. nov. International Journal of Systematic and Evolutionary Microbiology. 2004;54 :149 - 56.
Mahdhi M, Mars M. Genotypic diversity of rhizobia isolated from Retama raetam in arid regions of Tunisia. Annales de Microbiologie. 2006;56 :305-311 - 57.
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. Letters in Applied Microbiology. 2007;54 :604-609 - 58.
Mahdhi M, de Lajudie P, Mars M. Phylogenetic and symbiotic characterization of rhizobial bacteria nodulating Argyrolobium uniflorum in Tunisian arid soils. Canadian Journal of Microbiology. 2008;54 :209-217 - 59.
Abdelmoumen H, Filali Maltout A, Neyra M, Belabed A, El Idrissi MM. Effects of high salts concentrations on the growth of rhizobia and responses to added osmotica. Journal of Applied Microbiology. 1999; 86 :889-898 - 60.
Bouchiba Z, Boukhatem ZF, Ighilhariz Z, Derkaoui N, Bekki A. Diversity of nodular bacteria of Scorpiurus muricatus in western Algeria and their impact on plant growth. Canadian Journal of Microbiology. 2017;63 :450-463. DOI: 10.1139/cjm-2016-0493 - 61.
Merabet C, Bekki A, Benrabah N, Bey M, Bouchentouf L, Ameziane H, et al. Distribution of Medicago species and their microsymbionts in a saline region of Algeria. Arid Land Research and Management. 2006;20 :219-231 - 62.
Sebbane N, Sahnoune M, Zakhia F, Willems A, Benallaoua S, de Lajudie P. Phenotypical and genotypical characteristics of root-nodulating bacteria isolated from annual Medicago spp. in Soummam Valley (Algeria). Letters in Applied Microbiology. 2006;42 :235-241 - 63.
Mahdhi M, Fterich A, Rejili M, Rodriguez-Llorente ID, Mars M. Legume-Nodulating bacteria (LNB) from three pasture legumes ( Vicia sativa ,Trigonella maritima andHedysarum spinosissimum ) in Tunisia. Annales de Microbiologie. 2012;62 :61-68 - 64.
Fitouri SD, Trabelsi D, Saïdi S, Zribi K, Ben Jeddi F, Mhamdi R. Diversity of rhizobia nodulating sulla ( Hedysarum coronarium L.) and selection of inoculant strains for semi-arid Tunisia. Annales de Microbiologie. 2012;62 :77-84. DOI: 10.1007/s13213-011-0229-22012 - 65.
Ezzakkioui F, El Mourabit N, Chahboune R, Castellano-Hinojosa A, Bedmar EJ, Barrijal S. Phenotypic and genetic characterization of rhizobia isolated from Hedysarum flexuosum in northwest region of Morocco. Journal of Basic Microbiology. 2015;55 :830-837. DOI: 10.1002/jobm.2014007 - 66.
Balkwill DL. Ensifer. In: Bergey’s Manual of Systematics of Archaea and Bacteria. Hoboken, New Jersey-USA: John Wiley & Sons, Ltd; 2005 - 67.
Willems A, Fernandez-Lopez M, Munoz-Adelantado E, Goris J, et al. Description of new Ensifer strains from nodules and proposal to transferEnsifer adhaerens Casida 1982 toSinorhizobium asSinorhizobium adhaerens comb. nov. request for an opinion. International Journal of Systematic and Evolutionary Microbiology. 2003;53 :1207-1217 - 68.
Judicial Commission. Opinion 84 – The genus name Sinorhizobium Chen et al. 1988 is a later synonym of Ensifer Casida 1982 and is not conserved over the latter genus name, and the species name ‘Sinorhizobium adhaerens ’ is not validly published. International Journal of Systematic and Evolutionary Microbiology. 2008;58 :1973 - 69.
Merabet C, Martens M, Mahdhi M, Zakhia F, et al. Multilocus sequence analysis of root nodule isolates from Lotus arabicus (Senegal) ,Lotus creticus ,Argyrolobium uniflorum andMedicago sativa (Tunisia) and description ofEnsifer numidicus sp. nov. andEnsifer garamanticus sp. nov. International Journal of Systematic and Evolutionary Microbiology. 2010;60 :664-674 - 70.
Khbaya B, Neyra M, Normand P, Zerhari K, Filali-Maltouf A. Genetic diversity and phylogeny of rhizobia that nodulate Acacia spp. in Morocco assessed by analysis of rRNA genes. Applied and Environmental Microbiology. 1998;64 :4912-4917 - 71.
Fterich A, Mahdhi M, Mars M. Impact of grazing on soil microbial communities along a chronosequence of Acacia tortilis subsp.raddiana in arid soils in Tunisia. European Journal of Soil Biology. 2012;50 :56-63 - 72.
Sakrouhi I, Belfquih M, Sbabou L, Moulin P, Bena G, Filali-Maltouf A, et al. Recovery of symbiotic nitrogen fixing acacia rhizobia from Merzouga Desert sand dunes in south East Morocco—Identification of a probable new species of Ensifer adapted to stressed environments. Systematic and Applied Microbiology. 2016;39 :22-31 - 73.
Ben Romdhane S, Nasr H, Samba-Mbaye R, Neyra M, Ghorbal MH. Diversity of Acacia tortilis rhizobia revealed by PCR/RFLP on crushed root nodules in Tunisia. Annals of Microbiology. 2005; 55 :249-258 - 74.
Jebara M, Drevon JJ, Aouani ME. Effects of hydroponic culture system and NaCl on interactions between common bean lines and native rhizobia from Tunisian soils. Agronomie. 2001; 21 :601-605 - 75.
Zribi K, Mhamdi R, Huguet T, Aouani ME. Distribution and genetic diversity of rhizobia nodulating natural populations of Medicago truncatula in Tunisian soils. Soil Biology and Biochemistry. 2004;36 :903-908. DOI: 10.1016/j.soilbio.2004.02.003 - 76.
Badri M, Ilahi H, Huguet T, Aouani ME. Quantitative and molecular genetic variation in sympatric populations of Medicago laciniata andM. truncatula (Fabaceae): Relationships with eco-geographical geographical factors. Genetical Research. 2007;89 :107-122 - 77.
Elboutahiri N, Thami-Alami I, Udupa SM. Phenotypic and genetic diversity in Sinorhizobium meliloti andS. medicae from drought and salt affected regions of Morocco. BMC Microbiology. 2015;10 :15. DOI: 10.1186/1471-2180-10-15 - 78.
Baba Arbi S, Cheriet D, Chekireb D, Ouartsi A. Caractérisation phénotypique et génotypique des rhizobia symbiotiques des légumineuses spontanées Melilotus indicus etMedicago littoralis des palmeraies de la région de Touggourt en Algérie. In: Conférence: Journées Internationales de Biotechnologie 2014, at Hammamet, Tunisie. Vol. 2014 - 79.
Guerrouj K, Bouterfas M, Abdelmoumen H, Missbah El Idrissi M. Diversity of bacteria nodulating Medicago arborea in the northeast area of Morocco. Chiang Mai Journal of Science. 2016;43 :440-451 - 80.
Mousavi SA, Österman J, Wahlberg N, Nesme X, Lavire C, Vial L, et al. Phylogeny of the Rhizobium clade supports the delineation ofNeorhizobium gen. nov. Systematic and Applied Microbiology. 2014;37 :208-215 - 81.
Flores-Felix JD, Carro L, Velaszquez E, Valverde A, Cerda Castillo E, Garcia-Fraile P, et al. Phyllobacterium endophyticum sp. nov., isolated from nodules ofPhaseolus vulgaris . International Journal of Systematic and Evolutionary Microbiology. 2013;63 :821-826 - 82.
Ardley J, O’Hara G, Reeve W, Yates R, Dilworth M, Tiwari R, et al. Root nodule bacteria isolated from South African Lotononis bainesii ,L. listii andL. solitudinis are species ofMethylobacterium that are unable to utilize methanol. Archives of Microbiology. 2009;191 :311-318 - 83.
Andam CP, Parker MA. Novel alphaproteobacterial root nodule symbiont associated with Lupinus texensis . Applied and Environmental Microbiology. 2007;73 :5687-5691. DOI: 10.1128/AEM.01413-07 - 84.
Reeve W, Chain P, O’Hara G, Ardley J, Nandesena K, Bräu L, et al. Complete genome sequence of the Medicago microsymbiontEnsifer (Sinorhizobium )medicae strain WSM419. Standards in Genomic Sciences. 2010;2 :77 - 85.
Tinick MJ, Hadobas PA. Nodulation of Trifolium repens with modified Bradyrhizobium and the nodulation of Parasponia withRhizobium leguminosarum biovar trifolii 1990a. Plant and Soil. 1990;125 :49-61 - 86.
Mahdhi M, Nzoué A, de Lajudie P, Mars M. Characterization of root-nodulating bacteria on Retama raetam in arid Tunisian soils. Progress in Natural Science. 2008;18 :43-49