Tác động của plasmid lên sự hợp tác giữa rhizobia và cây họ đậu trong các môi trường đa dạng

Symbiosis - Tập 73 - Trang 75-91 - 2017
Hamdi Hussein Zahran1
1Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Beni-Suef, Egypt

Tóm tắt

Rhizobia là một nhóm vi khuẩn đất nổi tiếng, thiết lập mối quan hệ cộng sinh với thực vật họ đậu, cố định nitơ từ khí quyển và cải thiện độ màu mỡ của đất. Để hoàn thành nhiều chức năng trong đất, rhizobia được phát triển với một bộ gen phức tạp và đa phần, bao gồm nhiều replicon. Vật liệu di truyền được phân bổ giữa các replicon khác nhau nhằm đáp ứng, và thỏa mãn các chức năng đa dạng của rhizobia. Ngoài nhiễm sắc thể chính, mang theo các gen thiết yếu (gen lõi) cần thiết cho sự sống của tế bào, bộ gen của rhizobia còn chứa nhiều plasmid ngoài nhiễm sắc thể, mang theo các gen không thiết yếu (gen phụ). Đôi khi, một số mega-plasmid, được gọi là nhiễm sắc thể thứ cấp hoặc chromid, mang thêm một số gen thiết yếu (gen lõi). Hơn nữa, một số trình tự gen phụ cụ thể (các đảo nhiễm sắc thể cộng sinh) được tích hợp vào nhiễm sắc thể chính của một số loài rhizobia trong các chi Bradyrhizobium và Mesorhizobium. Plasmid trong rhizobia có kích thước biến đổi. Tất cả các plasmid trong một tế bào Rhizobium chiếm khoảng 30–50% bộ gen. Plasmid rhizobia có nhiều đặc điểm như các gen khác nhau, hệ thống tái bản độc lập, khả năng tự truyền tải, và tính không ổn định. Plasmid điều tiết nhiều chức năng chuyển hóa tế bào và cho phép rhizobia chủ nhà tồn tại trong các môi trường khác nhau, thậm chí trong điều kiện căng thẳng. Plasmid cộng sinh trong rhizobia đang nhận được sự chú ý ngày càng tăng vì sự quan trọng của chúng trong quá trình cố định nitơ cộng sinh. Chúng mang theo các gen cộng sinh (nod, nif và fix), và một số gen không cộng sinh. Plasmid cộng sinh được chuyển giao đồng hợp bởi sự hỗ trợ của các plasmid không cộng sinh, tự truyền tải, do đó, mang lại những thay đổi đáng kể trong các tương tác cộng sinh và đặc điểm đặc hiệu của chủ nhà rhizobia. Bên cạnh đó, các tế bào rhizobia chứa một hoặc nhiều plasmid phụ không cộng sinh, mang theo các gen điều tiết các chức năng chuyển hóa khác nhau, khả năng thuộc địa của rhizosphere, và tính cạnh tranh trong nốt hình thành. Tất cả các plasmid rhizobia tương tác một cách hài hòa và cung cấp cho rhizobia khả năng đáng kể để hoàn thành các chức năng cộng sinh và không cộng sinh phức tạp của chúng trong các môi trường đa dạng. Các khái niệm trên đã được xem xét một cách sâu rộng và thảo luận một cách công bằng.

Từ khóa

#rhizobia #plasmid #sự hợp tác #cây họ đậu #cố định nitơ #môi trường đa dạng

Tài liệu tham khảo

Abdel-Salam MS, Abdel-Halim MM, Ibrahim SA, Badawy FM, Abo-Aba SEM (2013) Extension of rhizobial/plant host range and symbiosis improvement via plasmid transfer. Life Sci J 10:1346–1351 Abdel-Wahab AM, Zahran HH (1981) Effects of salt stress on nitrogenase activity and growth of four legumes. Biol Plantarum 23:16–23 Acosta JL, Eguiarte LE, Santamaria RI, Bustos P, Vinuesa P, Martínez-Romero E et al (2011) Genomic lineages of Rhizobium etli revealed by the extent of nucleotide polymorphisms and low recombination. BMC Evolution Biol 11:305 AlekshunMN LSB (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128:1037–1050 Alexandre A, Oliveira S (2012) Response to temperature stress in rhizobia. Crit Rev Microbiol 39:219–228 Allito BB, Ewusi-Mensah N, Alemneh AA (2015) Rhizobia strain and host-legume interaction effects on nitrogen fixation and yield of grain legume: a review. Molecular Soil Biology 6:1–12 Al-Saedi SA, Razaq IB, Ali NA (2016) Utilization of 15N dilution analysis for measuring efficiency of biological nitrogen fixation under soil salinity stress. World J Pharmacy Pharmaceutical Sci 5:1468–1479 Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C et al (2008) Genome sequence of the beta-Rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18:1472–1483 Anand A, Jaiswall SK, Dhar B, Vaishampayan A (2012) Surviving and thriving in terms of symbiotic performance of antibiotic and phage-resistant mutants of Bradyrhizobium of soybean [Glycine max (L.) Merrill]. Curr Microbiol 65:390–397 Ángeles Giusti M, Lozano MJ, Torres Tejerizo GA, Martini MC, Salas ME, López JL, Draghi WO, Del Papa MF, Pistorio M, Lagares A (2013) Conjugal transfer of a Sinorhizobium meliloti cryptic plasmid evaluated during a field release and in soil microcosms. Euro J Soil Biol 55:9–12 Anjum R, Grohmann E, Malik A (2011) Molecular characterization of conjugative plasmids in pesticide tolerant and multiresistant bacterial isolates from contaminated alluvial soil. Chemosphere 84:175–181 Archana G (2010) Engineering nodulation competitiveness of rhizobial bioinoculants in soils. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Verlag/Wien, New York, pp 157–194 Bailly X, Olivieri I, Brunel B, Cleyet-Marel JC, Béna G (2007) Horizontal gene transfer and homologus recombination drive the evolution of the nitrogen-fixing symbionts of Medicago species. J Bacteriol 189:5223–5236 Baldani JI, Weaver RW (1992) Survival of clover rhizobia and their plasmid cured derivatives in soil under heat and drought stress. Soil Biol Biochem 24:737–742 Baldani JI, Weaver RW, Hynes MF, Eardly BD (1992) Utilization of carbon substrates, electrophoretic enzyme patterns, and symbiotic performance of plasmid-cured clover rhizobia. Appl Environ Microbiol 58:2308–2314 Barbour WM, Elkan GH (1990) Physiological characteristics and competitive ability of plasmid-cured derivatives of Rhizobium fredii USDA 206. Arch Microbiol 154:1–4 Barcellos FG, Menna P, Batista JS, Hungria M (2007) Evidence for horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculants strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian savannah soil. Appl Environ Microbiol 73:2635–2643 Barnett MJ, Fisher R, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J et al (2001) Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A 98:9883–9888 Barreto EF, Straliotto R, Baldani JI (2012) Curing of a non-symbiotic plasmid of the Rhizobium tropici strain CIAT899 affected nodule occupancy and competitiveness of the bacteria in symbiosis with common beans. Eur J Soil Biol 50:91–96 Batut J, Andersson SG, O’Callaghan D (2004) The evolution of chronic infection strategies in the alpha-proteobacteria. Nat Rev Microbiol 2:933–945 Becker A (2009) Functional genomics of rhizobia. In: Pawlowski K (ed) Prokaryotic symbionts in plants, Microbiol Monogr, Springer-Verlag, vol 8. Berlin, Heidelberg, pp 71–100 Belachew T (2010) Intrinsic antibiotic resistance, survival of Rhizobium leguminosarum strains and fixation potential of pea varieties (Pisum sativum L.) in Southeast Ethiopia. Int J Microbiol Res 2:75–79 Béna G, Lyet A, Huguet T, Olivieri I (2005) Medicago-Sinorhizobium symbiotic specificity evolution and the geographic expansion of Medicago. J Evolution Biol 18:1547–1558 Bentley S (2009) Sequencing the species pan-genome. Nat Rev Microbiol 7:258–259 Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Ann Rev Genet 38:771–792 Bentley SD, Chater KF, Cerdeno-Tarraga AM et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3 (2). Nature 417:141–147 Berrada H, Fikri-Benbrahim K (2014) Taxonomy of the rhizobia: current perspectives. British Microbiol Res J 4:616–639 Black M, Moolhuijzen P, Chapman B, Barrero R, Howieson J, Hungria M et al (2012) The genetics of symbiotic nitrogen fixation: comparative genomics of 14 rhizobia strains by resolution of protein clusters. Genes 3:138–166 Blanca-Ordóñez H, Oliva-García JJ, Pérez-Mendoza D, Soto MJ, Olivares J, Sanjuán J, Nogales J (2010) pSymA-dependent mobilization of the Sinorhizobium meliloti pSymB mobilization. J Bacteriol 192:6309–6312 Boivin C, Malpica C, Rosenberg C, Goldman A, Flevry V, Maille M, Message B, Pamboukdjian N, Tepfer D (1990) Catabolism of the plant secondary metabolites calystegins and trigonelline by Rhizobium meliloti. Symbiosis 9:147–154 Borthakur D, Soedarjo M, Fox PM, Webb DT (2003) The mid genes of Rhizobium sp. strain TAL1145 are required for degradation of mimosine into 3-hydroxy-4-pyridine and are inducible by mimosine. Microbiology 149:537–546 Boussau B, Karlberg EO, Frank AC, Legault BA, Andersson SG (2004) Computational inference of scenarios for α-proteobacterial genome evolution. Proc Natl Acad Sci U S A 101:9722–9727 Boyd EF, Hill CW, Rich SM, Hartl DL (1996) Mosaic structure of plasmids from natural populations of Escherichia coli. Genetics 142:1091–1100 Brewin NJ, Wood EA, Johnston AWB, Dibb NJ, Hombrecher G (1982) Recombinant nodulation plasmids in Rhizobium leguminosarum. J Gen Microbiol 129:2973–2977 Brewin NJ, Wood EA, Young PW (1983) Contribution of the symbiotic plasmid to the competitiveness of Rhizobium leguminosarum. J Gen Microbiol 129:2973–2977 Brom S, de los Santos GA, Girard ML, Dávia G, Palacios R et al (1991) High-frequency rearrangements in Rhizobium Leguminosarum Bv. phaseoli plasmids. J Bacteriol 173:1344–1346 Brom S, de los Santos, García A, Stepkowsky T, Flores M, Dávila G et al. (1992) Different plasmids of Rhizobium leguminosarum bv. phaseoli are required for optimal symbiotic performance. J Bacteriol 174:5183–5189 Brom S, de los Santos GA, Cervantes L, Palacios R, Romero D (2000) In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid 44:34–43 Brom S, Girard MI, de los Santos, García A, Sanjuan-Pinilla JM, Olivares J, Sanjuan J (2002) Conservation of plasmid-encoded traits among bean-nodulating Rhizobium species. Appl Environ Microbiol 68:2555–2561 Brom S, Girard L, Tun-Garrido C, de los Santos, García A, Bustos P, González V, Romero D (2004) Transfer of the symbiotic plasmid of Rhizobium etli CFN42 requires co-integration with p42a, which may be mediated by site-specific recombination. J Bacteriol 186:7538–7548 Broughton WJ, Perret X (1999) Genealogy of legume-Rhizobium symbioses. Curr Opinion Plant Biol 2:305–311 Buell CR, Joardar V, Linderberg M (2003) The complete genome sequence of Arabidopsis and the tomato pathogen Pseudomonas syringae bv. tomato DC 3000. Proc Natl Acad Sci U S A 100:10181–10186 Capela D, Barloy-Hubler F, Gouzy J, Bothe G, Ampe F, Batut J et al (2001) Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci U S A 98:9877–9882 Cardoso P, Freitas R, Figueira E (2015) Salt tolerance of rhizobial populations from contrasting environmental conditions: understanding the implications of climate change. Ecotoxicology 24:143–152 Castillo-Ramírez S, Vázquez-Castellanos JF, González V, Cevallos MA (2009) Horizontal gene transfer and diverse functional constrains within a common replication-partitioning system in alpha proteobacteria: the repABC operon. BMC Genomics 18:536 Cervantes L, Bustos P, Girard L, Santamaria RI, Dávila G, Vinuesa P, Romero D, Brom S (2011) The conjugative plasmid of a bean-nodulating Sinorhizobium fredii strain is assembled from sequences of two Rhizobium plasmids and the chromosome of Sinorhizobium strain. BMC Microbiol 11:49 Cervantes-Rivera R, Pedraza-López F, Pérez-Segura G, Cevallos MA (2011) The replication origin of a repABC plasmid. BMC Microbiol 11:158 Cevallos MA, Portal H, Izquierdo J, Tun-Garrido C, de los Santos GA, Dávila G et al (2002) Rhizobium etli CFN42 contains at least three plasmids of the repABC family: a structural and evolutionary analysis. Plasmid 48:104–116 Cevallos MA, Cervantes-Rivera R, Gutiérrez-Rios RM (2008) The repABC plasmid family. Plasmid 60:19–37 Chain PS, Denef VJ, Konstantindis KT, Vergez LM, Agulló L, Reyes VL et al (2006) Burkholderia xenovorans LB 400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci U S A 103:15280–15287 Charles TC, Finan TM (1991) Analysis of a 1600-kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo. Genetics 127:5–20 Chen H, Gartner E, Rolfe BG (1993) Involvement of genes on megaplasmid in the acid-tolerant phenotype of Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 59:1058–1064 Chen H, Higgins J, Oresnik IJ, Hynes MF, Natera S, Djordjevic MA et al (2000) Proteome analysis demonstrates complex replicon and luteolin interactions in pSyma-cured derivatives of Sinorhizobium meliloti strain 2011. Electrophoresis 21:3833–3842 Crook MB, Lindsay DP, Biggs MB, Bentley JS, Price JC, Clement SC, Clement MJ, Long SR, Griffiths JS (2012) Rhizobial plasmids that cause impaired symbiotic nitrogen fixation and enhanced host invasion. Mol Plant-Microbe Interact 25:1026–1033 Crossman LC (2005) Plasmid replicons of Rhizobium. Biochem Soc Trans 33:157–158 Crossman LC, Castillo-Ramírez S, McAnnula C, Lozano L, Vernikos GS, Acosta JL et al (2008) A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen-fixing bacteria. PLoS One 3(7) Cytryn EJ, Jitacksorn S, Giraud E, Sadowsky MJ (2008) Insights learned from pBTAi1, a 229-kb accessory plasmid from Bradyrhizobium sp. strain BTAi1 and prevalence of accessory plasmids in other Bradyrhizobium sp. strains. Int Soc Microb Ecol J 2:158–170 Danino VE, Wilkinson A, Edwards A, Downie JA (2003) Recipient-induced transfer of the symbiotic plasmid pRl1JI in Rhizobium leguminosarum bv. viciae is regulated by a quorum-sensing relay. Mol Microbiol 50:511–525 Darmon E, Leach DRF (2014) Bacterial genome instability. Microbiol Mol Biol Rev 78:1–39 de los Santos GA, Brom S, Romero D (1996) Rhizobium plasmids in bacteria-legume interactions. World J Microbiol Biotech 12:119–125 de los Santos, García A, Brom S (1997) Characterization of two plasmid-borne lps β loci of R. etli required for lipopolysaccharide synthesis and for optimal interaction with plants. Mol Plant Microb Interact 10:891–902 de los Santos GA, López E, Cubillas CA, Noel KD, Brom S et al (2008) Requirement of a plasmid-encoded catalase for survival of Rhizobium etli CFN42 in a polyphenol-rich environment. Appl Environ Microbiol 74:2398–2403 Del Cerro P, Rolla-Santos AAP, Gomes DF, Marks BB et al (2015) Opening the “black box” of nodD3, nodD4 and nodD5 genes of Rhizobium tropici strain CIAT899. BMC Genomics 16:864 Del Cerro P, Rolla-Santos AAP, Valderrama-Fernández R et al (2016) NrcR, a new transcriptional regulator of Rhizobium tropici CIAT899 involved in the legume root-nodule symbiosis. PLoS ONE 11(4). doi:10.1371/journal.pone.0154029 Ding H, Hynes MF (2009) Plasmid transfer systems in the rhizobia. Can J Microbiol 55:917–927 Ding H, Yip CB, Geddes BA, Oresnik IJ, Hynes MF (2012) Glycerol utilization by Rhizobium leguminosarum requires an ABC transporter and affects competition for nodulation. Microbiology 158:1369–1378 Ding H, Yip CB, Hynes MF (2013) Genetic characterization of a novel rhizobial plasmid conjugation system in Rhizobium leguminosarum bv. Viciae VF39SM. J Bacteriol 195:328–339 Djordjevic MA, Zurkowski W, Shine J, Rolfe BG (1983) Sym plasmid transfer to various symbiotic mutants of Rhizobium trifolii, R leguminosarum and R meliloti. J Bacteriol 156:1035–1045 Dogra T, Priyadarshini A, Kanika KA, Singh NK (2013) Identification of genes involved in salt tolerance and symbiotic nitrogen fixation in chickpea rhizobium Mesorhizobium ciceri Ca181. Symbiosis 61:135–143 Domínguez-Ferreras A, Pérez-Arnedo R, Becker A, Olivares J, Soto M, Sanjuan J (2006) Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J Bacteriol 188:7617–7625 Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170 Dresler-Nurmi A, Fewer DP, Räsänen LA, Lindström K (2009) The diversity and evolution of rhizobia. In: Pawlowski K (ed) Prokaryotic symbionts in plants, Microbiol Monogr, Springer-Verlag, vol 8. Berlin, Heidelberg, pp 3–41 Drevon J-J, Alkama N, Bargaz A, Paula Rodiño A, Sangthongwises K, Zaman-Allah M (2015) The legume-rhizobia symbiosis. In: De AM (ed) Grain legumes. Handbook of plant breeding, Springer Science, New York, pp 267–290 Dunny GM (2007) The peptide pheromone-inducible conjugation system of Enterococcus fecalis pCF10: cell-cell signaling, gene transfer, complexity and evolution. Philos T Roy Soc B 362:1185–1193 Dziewit L, Pyzik A, Szuplewska M, Matlakowska R, Mielnicki S, Wibberg D, Schlüter A, Pühler A, Bartosik D (2015) Diversity and role of plasmids in adaptation of bacteria inhabiting the Lubin copper mine in Poland, an environment rich in heavy metals. Frontiers Microbiol 6:152 Edulamudi P, Johnson AA, Divi VR, Konada VM (2012) Plasmid profiles of mercuric chloride tolerant rhizobia from horse gram (Macrotyloma uniflorum). J Environ Biol 33:187–190 Edwards A, Prederix M, Wisniewski-Dyé F, Jones J, Zorreguieta A, Downie JA (2009) The cin and rai quorum-sensing regulatory systems in Rhizobium leguminosarum are coordinated by ExpR and CinS, a small regulatory protein coexpressed with CinL. J Bacteriol 191:3059–3067 Egamberdieva D, Berg G, Lindström K, Räsänen LA (2013) Alleviation of salt stress of symbiotic Galega officinals L. (goat’s rue) by co-inoculation of Rhizobium with root-colonization Pseudomonas. Plant Soil 369:453–465 Eugenia Marquina M, Enrigue González N, Castro Y (2011) Phenotypic and genotypic characterization of twelve rhizobial isolates from different regions of Venezuela. Trop Biol 59:1017–1036 Falla TJ, Chopra I (1999) Stabilization of Rhizobium symbiosis plasmids. Microbiology 145:515–516 Fauvart M, Sánchez-Rodríguez A, Beullens S, Marchal K, Michiels J (2011) Genome sequence of Rhizobium etli. CNPAF512, a nitrogen-fixing symbiont isolated from bean root nodules in Brazil. J Bacteriol 193:3158–3159 Finan TM, Weidner S, Wong K, Buhrmester J, Chain P, Vorhölter FJ, Hernández-Lucas I, Becker A, Cowie A, Gouzy J, Golding B, Pühler A (2001) The complete sequence of the 1683 kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci U S A 98:9889–9894 Flores M, Mavingui P, Girard L, Perret X, Broughton WJ, Martínez-Romero E, Dávila G, Palacios R (1998) Three replicons of Rhizobium sp. strain NGR234 harbor symbiotic gene sequences. J Bacteriol 180:6052–6053 Fox MA, Karunakaran R, Leonard ME, Mouhsine B, Williams A, East AK, Downie JA, Poole PS (2008) Characterization of the quaternary amine transporters of Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Lett 287:212–220 Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A et al (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394–401 Galibert F, Finan TM, Long SR, Pűhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672 Geddes BA, Pickering BS, Poysti NJ, Collins H, Yudistira H et al (2010) A locus necessary for the transport and catabolism of erythritol in Sinorhizobium meliloti. Microbiology 156:2970–2981 Geniaux E, Flores M, Palacios R, Martínez E (1995) Presence of megaplasmids in Rhizobium tropici and further evidence of differences between the two R. tropici subtypes. Int J Syst Bacteriol 45:392–394 Giuntini E, Mengoni A, De Filippo C, Cavalieri D, Aubin-Horth N, Landry CR et al (2005) Large-scale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains. BMC Genomics 6:158 González V, Bustos P, Ramírez-Romero MA, Madrano-Soto A, Salgado H et al (2003) The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments. Genome Biol 4:R36 González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Mareno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G (2006) The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci U S A 103:3834–3839 González V, Acosta JI, Santamaría RI, Bustos P, Fernández JI et al (2010) Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of Rhizobium etli. Appl Environ Microbiol 76:1604–1614 González-Pasayo R, Martínez-Romero E (2000) Multiresistance genes of Rhizobium etli CFN42. Mol Plant Microb Interact 13:572–577 Guo X, Flores M, Mavingui P, Fuentes SI, Hernández G, Dávila G et al (2003) Natural genomic design in Sinorhizobium meliloti: novel genomic architectures. Genomic Research 13:1810–1817 Hajare B, Ade A (2012) Confirming location of nitrogen-fixing genes on plasmids in Rhizobium isolated from Pisum sativum. Biosci Discov 3:160–164 Harrison SP, Jones DG, Schunmann PHD, Forster JW, Young JPW (1988) Variation in Rhizobum leguminosarum bv. trifolii Sym plasmids and the association with effectiveness of nitrogen fixation. J Gen Microbiol 134:2721–2730 Harrison PW, Lower RPJ, Kim NKD, Young JPW (2010) Introducing the bacterial chromid: not a chromosome, not a plasmid. Trends Microbiol 18:141–148 Hernández-Lucas I, Pardo MA, Segovia L, Miranda J, Martínez-Romero E (1995) Rhizobium tropici chromosomal citrate synthase gene. Appl Environ Microbiol 61:3992–3997 Hernández-Tamayo R, Sohlenkamp C, Puente JL, Brom S, Rmero D (2013) Characterization of IntA, a bidirectional site-specific recombinase required for conjugative transfer of the symbiotic plasmid of Rhizobium etli CFN42. J Bacteriol 195:4668–4677 Hossain MZ, Lundquist P-O (2016) Nodule inhabiting non-rhizobial bacteria and their influence in growth of selected plants in Bangladesh. Bioresearch Communications 2:134–138 Hynes MF, McGregor NF (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4:567–574 Hynes MF, Brucksch K, Priefer U (1988) Melanin production encoded by a cryptic plasmid in a Rhizobium leguminosarum strain. Arch Microbiol 150:326–332 Ibáñez F, Reinoso H, Fabra A (2010) Experimental evidences of pSym transfer in a native peanut-associated rhizobia. Microbiol Res 165:505–515 Kajić S, Hulak SS (2016) Environmental stress response and adaptation mechanisms in rhizobia. Agric Conspec Sci 81:15–19 Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S et al (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338 Karmakar K, Rana A, Rajwar A, Sahgal M, Johri BN (2015) Legume-rhizobia symbiosis under stress. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Springer, India, pp 241–258 Król JE, Mazur A, Marczak M, Skorupska A (2007) Syntenic arrangements of the surface polysaccharide biosynthesis genes in Rhizobium leguminosarum. Genomics 89:237–247 Król JE, Mazur A, Marczak M, Skorupska A (2008) Application of physical and genetic map of Rhizobium leguminosarum bv. trifolii TA1 to comparison of three closely related rhizobial genomes. Mol Gen Genomics 279:107–121 Kuhn S, Stiens M, Pűhler A, Schlüter A (2008) Prevalence of pSmeSM11a-like plasmids in indigenous Sinorhizobium meliloti strains isolated in the course of a field release experiment with genetically modified S. meliloti strains. FEMS Microbiol Ecol 63:118–131 Kumar N, Ganesh L, Giuntini E, Kaye ME, Udomwong P, Shamsani NJ, Young JPW, Bailly X (2015) Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum. Open Biology 5:140133 Kurchak ON, Provorov NA, Simarov BV (2001) Plasmid pSym1-32 of Rhizobium leguminosarum bv. Viciae controlling nitrogen fixation activity, effectiveness of symbiosis, competitiveness, and acid tolerance. Russ J Genet 37:1025–1031 Lagares A, Sanjuán J, Pistorio M (2014) The plasmid mobilome of the model plant-symbiont Sinorhizobium meliloti: coming up with new questions and answers. Microbiol Spectrum 2(5) Laguerre G, Bardin M, Amarger N (1993) Isolation from soil of symbiotic and nonsymbiotic Rhizobium leguminosarum by DNA hybridization. Can J Microbiol 39:1142–1149 Landeta C, Dávalos A, Cevallos MA, Geiger O, Brom S, Romero D (2011) Plasmids with a chromosome-like role in Rhizobium. J Bacteriol 193:1317–1326 Laranjo M, Alexandre A, Oliveira S (2014) Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol Res 169:2–17 Lee KB, De Backer P, Aono T, Liu CT, Suzuki S et al (2008) The genome of the versatile nitrogen fixer Azorhizobium caulinodans ORS571. BMC Genomics 9:271: doi:10.1186/1471-2164-9-27 Li F, Hou B, Hong G (2008) Symbiotic plasmid is required for NoIR to fully repress nodulation genes in Rhizobium leguminosarum A34. Acta Biochim Biophys Sin 40:901–907 Lithgrow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P, Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol Microbiol 37:81–97 Liu X, Luo Y, Mohamed OA, Liu D, Wei G (2014) Global transcriptome analysis of Mesorhizobium alhagi CCNWXJ12-2 under salt stress. BMC Microbiol 14:319 Long R-C, Li M-N, Kang J-M, Zhang T-J, Sun Y, Yang Q-C (2015) Small RNA deep sequencing identifies novel and salt-stress-regulated microRNAs from roots of Medicago truncatula. Physiol Plant 154:13–27 López-Guerrero MG, Ormeňo-Orrillo E, Acosta JL, Mendoza-Vargas A, Rogel MA, Ramírez MA, Rosenblueth M, Martínez-Romero J, Martínez-Romero E (2012) Rhizobial extrachromosomal replicon variability, stability, and expression in natural niches. Plasmid 68:149–158 Mabrouk Y, Belhadj O (2010) The potential use of Rhizobium-legume symbiosis for enhancing plant growth and management of plant diseases. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Microbes for legume improvement, Springer-Verlag, Wien, New York, pp 1–25 Mabrouk Y, Belhadj O (2012) Enhancing the biological nitrogen fixation of leguminous crops grown under stressed environments. Afr J Biotech 11:10809–10815 MacLean AM, Finan TM, Sadowsky MJ (2007) Genomes of the symbiotic nitrogen-fixing bacteria of legumes. Plant Physiol 144:615–622 Maclellan SR, Sibley CD, Finan TM (2004) Second chromosomes and megaplasmids in bacteria. In: Funnell BE, Phillips GJ (eds) Plasmid Biology. ASM Press, Washington, DC, pp 529–542 Maclellan SR, Zaheer R, Sartor AL, Maclean AM, Finan TM (2006) Identification of a megaplasmid centromere reveals genetic structural diversity within the repABC family of basic replicons. Mol Microbiol 59:1559–1575 Manchanda G, Garg N (2008) Salinity and its effects on the functional biology of legumes. Acta Physiol Plant 30:595–618 Mari C, Broughton WJ, Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 4:336–342 Martínez-Abarca F, Martínez-Rodriguez L, López-Contreras JA, Jiménez-Zurdo JI, Toro N (2013) Complete genome sequence of the alfalfa symbiont Sinorhizobium/Ensifer meliloti strain GR4. Genome Announcement 1(1). doi:10.1128/genomeA.00174-12AQ8 Martínez-Romero E, Caballero-Mellado J (1996) Rhizobium phylogenies and bacterial genetic diversity. Crit Rev Plant Sci 15:113–140 Martínez-Romero E, Rosenblueth M (1990) Increased bean (Phaseolus vulgaris L) nodulation competitiveness of genetically modified Rhizobium strains. Appl Environ Microbiol 56:2384–2388 Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17:458–466 Mavingui P, Flores M, Guo X, Dávila G, Perret X, Broughton WJ et al (2002) Dynamics of genome architecture in Rhizobium sp. strain NGR234. J Bacteriol 184:171–176 Mazur A, Koper P (2012) Rhizobial plasmids-replication, structure and biological role. Cent Eur J Biol 7:571–586 Mazur A, Majewska B, Stasiak G, Wielbo J, Skorupska A (2011a) repABC-based replication systems of Rhizobium leguminosarum bv. trifolii TA1 plasmids: incompatibility and evolutionary analysis. Plasmid 66:53–66 Mazur A, Stasiak G, Wielbo J, Kubik-Komar A, Marek-Kozaczuk M, Skorupska A (2011b) Intragenomic diversity of Rhizobium leguminosarum bv. trifolii clover nodule isolates. BMC Microbiol 11:123 McAnulla C, Edwards A, Sanchez-Contreras M, Sawers RG, Downie JA (2007) Quorum-sensing-regulated transcriptional initiation of plasmid transfer and replication genes in Rhizobium leguminosarum biovar Viciae. Microbiology 153:2074–2082 Meng N, Yu B-J, Guo J-S (2016) Ameliorative effects of inoculation with Bradyrhizobium japonicum on Glycine max and Glycine soja seedlings under salt stress. Plant Physiol Regulation 80:137–147 Mercado-Blanco J, Olivares J (1993) Stability and transmissibility of the cryptic plasmids of Rhizobium meliloti GR4. Their possible use in the construction of cloning vectors of rhizobia. Arch Microbiol 160:477–485 Mercado-Blanco J, Toro N (1996) Plasmids in rhizobia: the role of nonsymbiotic plasmids. Mol Plant Microb Interact 9:535–545 Miranda-Rios J, Morera C, Toboada H, Dávalos A, Encarnación S et al (1997) Expression of thiamin biosynthetic genes (thiCOGE) and production of symbiotic terminal oxidase cbb3 in Rhizobium etli. J Bacteriol 179:6887–6893 Moënne-Loccoz Y, Weaver RW (1995a) Plasmids and saprophytic growth of Rhizobium leguminosarum bv. trifolii W14-2 in soil. FEMS Microbiol Ecol 18:139–144 Moënne-Loccoz Y, Weaver RW (1995b) Plasmids influence growth of rhizobia in the rhizosphere of clover. Soil Biol Biochem 27:1001–1004 Moënne-Loccoz Y, Weaver RW (1996) Involvement of plasmids in saprophytic performance and sodium chloride tolerance of clover rhizobia W14-2 in vitro. Appl Soil Ecol 3:137–148 Moënne-Loccoz Y, Baldani JI, Weaver RW (1995) Sequential heat-curing of Tn5-mob-sac labelled plasmids from Rhizobium to obtain derivatives with various combinations of plasmids and no plasmid. Lett Appl Microbiol 20:175–179 Mohammed A, Sharma RS, Ali S, Babu CR (2001) Molecular diversity of the plasmid genotypes among Rhizobium gene pools of sesbanias from different habitats of a semi-arid regions (Delhi). FEMS Microbiol Lett 205:171–178 Musarrat J, Zaidi A, Khan MS (2010) Recent advances in Rhizobium-legume interactions: a proteomic approach. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Verlag, Wien, New York, pp 81–101 Naamala J, Jaiswal SK, Dakora FD (2016) Antibiotic resistance in Rhizobium: type, process, mechanism and benefit for agriculture. Curr Microbiol 72:804–816 Nadasena KG, O’Hara GW, Tiwari RP, Sezmis E, Howieson JG (2007) In situ lateral transfer of symbiotic islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9:2496–2511 Nahar M, Mahal Z, Zahid HM, Zaman K, Jahan F, Rahman MM, Noor R (2012) Effects of plasmid curing on Rhizobium spp. Stanford J Microbiol 2:34–37 Niste M, Vidican R, Pop R, Rotar I (2013) Stress factors affecting symbiosis activity and nitrogen fixation by Rhizobium cultured in vitro. Pro-Environment 6:42–45 Nogales J, Campos R, Ben Abdel Khalek H, Olivares J, LLuch C, Sanjuan J (2002) Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol Plant Microb Interact 15:225–232 O’Connell M, Noel TC, Yeung EC, Hynes M, Hynes MF (1998) Decreased symbiotic effectiveness of Rhizobium leguminosarum strains carrying plasmid RP4. FEMS Microbiol Lett 161:275–283 Okazaki S, Noisangiam R, Okubo T, Kaneko T, Oshima K et al (2015) Genome analysis of a novel Bradyrhizobium sp. DOA9 carrying a symbiotic plasmid. PLoS One 10(2) Oresnik IJ, Pacarynuk LA, O’Brien SAP, Yost CK, Hynes MF (1998) Plasmid-encoded catabolic genes in Rhizobium leguminosarum bv. trifolii: evidence for a plant-inducible rhamnose locus involved in competition for nodulation. Mol Plant Microb Interact 11:1175–1185 Oresnik IJ, Twelker S, Hynes MF (1999) Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol 65:2833–2840 Oresnik IJ, Liu SL, Yost CK, Hynes MF (2000) Megaplasmid pRme2011a of Sinorhizobium meliloti is not required for viability. J Bacteriol 182:3582–3586 Ormeño-Orrillo E, Menna P, Gonzaga L, et al. (2012a) Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT899 and Rhizobium sp. PRF81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genomics 13, 735 Ormeño-Orrillo E, Rogel MA, Chueire LM, Tiedje JM, Martínez-Romero E, Hungria M (2012b) Genome sequences of Burkholderia sp. strains CCGE1002 and H160, isolated from legume nodules in Mexico and Brazil. J Bacteriol 194:6927–6937 Palacios R, Flores M (2005) Genome dynamics in rhizobial organisms. In: Palacios R, Newtonm WE (eds) Genomes and genomics of nitrogen-fixing organisms. Springer-Verlag, Dordrecht, Netherlands, pp 183–200 Pankhurst CE, MacDonald PE, Reeves JM (1986) Enhanced nitrogen fixation and competitive for nodulation of Lotus pedunculatus by a plasmid-cured derivative of Rhizobium loti. J Gen Microbiol 132:2321–2328 Pappas KM, Cevallos MA (2011) Plasmids of the Rhizobiaceae and their role in interbacterial and transkingdom interactions. In: Witzany G (ed) Soil biology, biocommunication in soil microorganisms, Volume 23, Austria, pp 295–337 Pardo MA, Lagünez J, Miranda J, Martínez E (1994) Nodulating ability of Rhizobium tropici is conditioned by a plasmid-encoded citrate synthase. Mol Microbiol 11:315–321 Patil CR, Alagawadi AR (2010) Microbial inoculants for sustainable legume production. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Verlag, Wien, New York, pp 515–535 Payakapong W, Tittabutr P, Teaumroong N, Boonkerd N, Singleton PW, Borthakur D (2006) Identification of two clusters of genes involved in salt tolerance in Sinorhizobium sp. strain BL3. Symbiosis 41:47–53 Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42 Peixoto L, Zavala A, Romero H, Musto H (2003) The strength of translational selection for codon usage varies in the three replicons of Sinorhizobium meliloti. Gene 320:109–116 Pérez-Mendoza D, Domínguez-Ferreras A, Muñoz S, Soto MJ, Olivares J, Brom S, Girard L, Herrera-Cervera JA, Sanjuán J (2004) Identification of functional mob regions in Rhizobium etli: evidence for self-transmissibility of the symbiotic plasmid pRetCFN42d. J Bacteriol 186:5753–5761 Pérez-Mendoza D, Sepúveda E, Pando V, Muñoz S, Nogales J, Olivares J, Soto MJ, Herrera-Cervera JA, Romero D, Brom S, Sanjuán J (2005) Identification of the rctA gene, which is required for repression of conjugative transfer of rhizobial symbiotic megaplasmids. J Bacteriol 187:7341–7350 Pérez-Montaño F, del Cerro P, Jiménez-Guerrero I, López-Baena FJ, Cubo MT, Hungria M, Megías M, Ollero FJ (2016) RNA-sequence analysis of the Rhizobium tropici CIAT988 transcriptome shows similarities in the activation patterns of symbiotic genes in the presence of apigenin and salt. BMC Genomics 17:198 Pérez-Segura G, Pérez-Oseguera A, Cevallos MA (2013) The repAC replication system of the Rhizobium leguminosarum pRL7 plasmid is functional: implications regarding the origin and evolution of repABC plasmids. Plasmid 69:49–57 Perret X, Freiberg C, Rosenthal A, Broughton WJ, Fellay R (1999) High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium sp. NGR234. Mol Microbiol 32:415–425 Phillips DA, Sande ES, Vriezen JAC, De Bruijn FJ, Le Rudulier D, Joseph CM (1998) A new genetic locus in Sinorhizobium meliloti is involved in stachydrine utilization. Appl Environ Microbiol 64:3954–3960 Pistorio M, Del Papa MF, Balagué LJ, Lagares A (2003) Identification of a transmissible plasmid from an argentine Sinorhizobium meliloti strain which can be mobilized by conjugative helper function of the European strain S. meliloti GR4. FEMS Microbiol Lett 225:15–21 Pistorio M, Giusti MA, Del Papa MF, Draghi WO, Lozano MJ, Tejerizo GT, Lagares A (2008) Conjugal properties of the Sinorhizobium meliloti plasmid mobilome. FEMS Microbiol Ecol 65:372–382 Poysti NJ, Loewen ED, Wang Z, Oresnik IJ (2007) Sinorhizobium meliloti pSymB carries genes necessary for arabinose transport and catabolism. Microbiology 153:727–736 Ramachandran VK, East AK, Karunakaran R, Downie JA, Poole PS (2011) Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics. Genome Biol 12:R106 Ramírez-Romero MA, Soberon N, Perez-Osequera A, Tẻllez-Sosa J, Cevallos MA (2000) Structural elements required for replication and incompatibility of the Rhizobium etli symbiotic plasmid. J Bacteriol 182:3117–3124 Ramírez-Romero MA, Téllez-Sosa J, Barrios H, Pérez-Oseguera A, Rosas V, Cevallos MA (2001) RepA negatively autoregulates the transcription of repABC operon of the Rhizobium etli symbiotic plasmid basic replicons. Mol Microbiol 42:195–204 Reeve W, Chain P, O’Hara G, Ardley J, Nandesena K, Bräu L et al (2010a) Complete genome sequence of the Medicago microsymbiont Ensifer (Sinorhizobium) medicae strain WSM419. Standards Genomic Sci 2:77–86 Reeve W, O’Hara G, Chain P, Ardley J, Bräu L, Nandesena K et al (2010b) Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM2304, an effective microsymbiont of the South America clover Trifolium polymorphum. Standards Genomic Sci 2:66–76 Reeve W, O’Hara G, Chain P, Ardley J, Bräu L, Nandesena K et al (2010c) Complete genome sequence of Rhizobium leguminosarum bv. trifolii strain WSM1325, an effective microsymbiont of annual mediterranean clovers. Standards Genomic Sci 2:347–356 Reguera M, Lloret J, Margaret I, Vinardell JM, Martin M, Buendia A, Rivilla R, Ruiz-Sainz JE, Bonilla I, Bolanos L (2009) Gene Smb21071 of plasmid pSymB is required for osmoadaptation of Sinorhizobium meliloti 1021 and is implicated in modifications of cell surface polysaccharides structure in response to hyperosmotic stress. Can J Microbiol 10:1145–1152 Remigi P, Jun Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24:63–75 Richardson JS, Hynes MF, Oresnik IJ (2004) A genetic locus necessary for rhamnose uptake and catabolism in Rhizobium leguminosarum bv. trifolii. J Bacteriol 186:8433–8442 Roberts RG (2014) Symbiosis plasmids bring their own mutagen to the wedding party. PLoS Biol 12:9 Rodriguez-Quiñones F, Maguire M, Wallington EJ, Gould PS, Yerko V, Downie JA et al (2005) Two of the three groEL homologues in Rhizobium leguminosarum are dispensable for normal growth. Arch Microbiol 183:253–265 Rogel MA, Hernaňdez-Lucas I, Kuykendall LD, Balkwill DL, Martínez-Romero E (2001) Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl Environ Microbiol 67:3264–3268 Rogel MA, Ormeňo-Orrillo E, Martínez-Romero E (2011) Symbiovars in rhizoia reflect bacterial adaptation to legumes. Syst Appl Microbiol 34:96–104 Rogel MA, Bustos P, Santamaría RI, González V, Romero D, Cevallos MA, Lozano L, Castro-Mondragón J, Martínez-Romero J, Ormeño-Orrillo E (2014) Genomic basis of symbiovar mimosa in Rhizobium etli. BMC Genomics 15:575 Romero D, Brom S (2004) The symbiotic plasmids of the Rhizobiaceae. In: Funnell BE, Phillips GJ (eds) Plasmid Biology. ASM Press, Washington, pp 271–290 Rosenblueth M, Hynes MF, Martínez-Romero E (1998) Rhizobium tropici teu genes involved in specific uptake of Phaseolus vulgaris bean-exudate compounds. Mol Gen Genet 258:587–598 Roumiantseva ML (2009) Genetic resources of nodule bacteria. Russ J Genetics 45:1013–1026 Roumiantseva ML, Muntyan VS (2015) Root nodule bacteria Sinorhizobium meliloti: tolerance to salinity and bacterial genetic determinants. Microbiology 84:263–280 Roumiantseva ML, Onischuk OP, Belova VS, Kurchak ON, Simarov BV (2011) Polymorphism of Sinorhizobium meliloti strains isolated from diversity centers of alfalfa in various soil and climatic conditions. Rus J Genet Appl Res 1:97–102 Sakrouhi I, Meryem Belfquih M, Sbabou L, Moulin P, Bena G, Abdelkarim Filali-Maltouf M, Antoine Le Quéré A (2016) 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. Syst Appl Microbiol 39:122–131 Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quéré A, Wollherr A et al (2009) Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl Environ Microbiol 75:4035–4045 Schneiker-Bekel S, Wibberg D, Bekel T, Blom J, Linke B et al (2011) The complete genome sequence of the dominant Sinorhizobium meliloti field isolate SM11 extends the S. meliloti pangenome. J Biotechnol 155:20–33 Schumacher MA (2008) Structural biology of plasmid partition: uncovering the molecular mechanisms of DNA segregation. Biochem J 412:1–18 Segovia L, Piňero D, Palacios R, Martínez-Romero E (1991) Genetic structure of a soil population of nonsymbiotic Rhizobium leguminosarum. Appl Environ Microbiol 57:426–433 Selbitschka W, Lotz W (1991) Instability of cryptic plasmids affects the symbiotic efficiency of Rhizobium leguminosarum bv. Viciae strains. Mol Plant-Microbe Interact 4:608–618 Sessitsch A, Howieson JG, Peret X, Antoun H, Martínez-Romero E (2002) Advances in Rhizobium research. Crit Rev Plant Sci 21:323–378 Shamseldin A (2008) Plasmid content of salt stress-tolerant Rhizobium strains from Egyptian soils nodulating common bean (Phaseolus vulgaris L). World J Microbiol Biotech 24:1603–1606 Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50:11–16 Singh SK, Jaiswal SK, Vaishampayan A, Dhar B (2013) Physiological behavior and antibiotic response of soybean (Glycine max L.) nodulating rhizobia isolated from Indian soils. Afr J Microbiol Res 7:2093–2102 Skorupska A, Janczarek M, Marczak M, Mazur A, Krǒl J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Factories 5:7 Skorupska A, Wielbo J, Kidoj D, Marek-Kozaczuk M (2010) Enhancing Rhizobium-legume symbiosis using signaling factors. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Verlag, Wien, New York, pp 27–54 Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EPC, Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74:434–452 Soberón N, Venkova-Canova T, Ramírez-Romero MA, Téllez-Sosa J, Cevallos MA (2004) Incompatibility and the partitioning site of the repABC basic replicon of the symbiotic plasmid from R. etli. Plasmid 51:203–216 Soto M, Zorzano A, García-Rodriguez FM, Mercado-Blanco J, López-Lara JM, Olivares J, Toro N (1994) Identification of a novel R. meliloti nodulation efficiency nfe gene homology of Agrobacterium ornithine cyclodeaminase. Mol Plant Microbe Interaction 7:784–791 Stasiak G, Mazur A, Wielbo J, Marczak M, Zebracki K, Koper P, Skorupska A (2014) Functional relationships between plasmids and their significance for metabolism and symbiotic performance of Rhizobium leguminosarum bv. trifolii. J Appl Genet 55:515–527 Stiens M, Schneiker S, Keller M, Kuhn S, Pühler A, Schlüter A (2006) Sequence analysis of the 144-kilobase accessory plasmid pSmeSM11a, isolated from a dominant Sinorhizobium meliloti strain identified during a long-term field release experiment. Appl Environ Microbiol 72:36–62 Streit WR, Schmitz RA, Perret X, Staehelin C, Deakin WJ, Raasch C, Liesegang H, Broughton WJ (2004) An evolutionary hot spot: the pNGR234b replicon of Rhizobium sp. strain NGR234. J Bacteriol 186:535–542 Sugawara M, Epstein B, Badgley BD, Unno T, Xu L et al (2013) Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies. Genome Biol 14:R17 Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Nat Acad Sci USA 95:5145–5149 Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD, Elliot RM et al (2002) Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol 184:3086–3095 Takeyama H, Nakayama H, Matsunaga T (2000) Salinity-regulated replication of the endogenous plasmid pSY10 from the marine cyanobacterium Synechococcus sp. Appl Biochem Biotech 84-86:447–453 Thakur AK, Singh KJ (2014) Effect of cadmium on plasmid profile of nitrogen fixing Rhizobium. Ind J Plant Sci 3:68–70 Thomas CM (2000) Paradigm of plasmid organization. Mol Microbiol 37:485–491 Thurman NP, Lewis DM, Jones DG (1985) The relationship of plasmid number to growth, acid tolerance and symbiotic efficiency in isolates of Rhizobium trifolii. J Appl Bacteriol 58:1–6 Torres-Tejerizo G, Del Papa MF, Giusti M, Draghi W, Lozano M, Lagares A, Pistorio M (2010) Characterization of extrachromosomal replicons present in the extended host range Rhizobium sp. LPU83. Plasmid 64:177–185 Torres-Tejerizo G, Pistorio M, Althabegioiti MJ et al (2014) Rhizobial plasmid pLPU83a is able to switch between different transfer machineries depending on its genomic background. FEMS Microbiol Ecol 88:565–578 Tun-Garrido C, Bustos P, González V, Brom S (2003) Conjugative transfer of p42a from Rhizobium etli CFN42, which is required for mobilization of the symbiotic plasmid, is regulated by quorum sensing. J Bacteriol 185:1681–1692 Velázquez E, Mateos PF, Velasco N, Santos F, Burgos PA, Villadas P, Toro N, Martínez-Molina E (1999) Symbiotic characteristics and selection of autochthonous strains of Sinorhizobium meliloti populatios in different soils. Soil Biol Biochem 31:1039–1047 Vercruysse M, Fauvart M, Jans A, Beullens S, Braeken K et al (2011) Stress response regulators identified through genome-wide transcriptome analysis of the (p)ppGpp-dependent response in Rhizobium etli. Genome Biol 12:R17 Villaseňor T, Brom S, Dávalos A, Lozano L, Romero D, de los Santos GA (2011) Housekeeping genes essential for pantothenate biosynthesis are plasmid-encoded in Rhizobium etli and Rhizobium leguminosarum. BMC Microbiol 11:66 Vinardell JM, Acosta-Jurado S, Göttfert M et al (2015) The Sinorhizobium fredii HH103 genome: a comparative analysis with S. fredii strains differing in their symbiotic behavior with soybean. Mol Plant-Microbe Interact 28:811–824 Vinuesa P, Reuhs BL, Breton C, Werner D (1999) Identification of a plasmid-borne locus in Rhizobium etli KIM55 involved in lipopolysaccharide O-chain biosynthesis and nodulation of Phaseolus vulgaris. J Bacteriol 181:5606–5614 Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbio 28:1381–1389 Vos K, Braeken K, Fauvart M, Ndayizeye M, Verhaert J, Zachorzok S, Lambrichts I, Michiels J (2007) The R. etli opt operon is required for symbiosis and stress resistance. Environ Microbiol 9:1665–1674 Wang ET, Van Berkum P, Sui XH, Beyene D, Chen WX et al (1999) Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int J Syst Bacteriol 49:51–65 Wang Y, Zhang Z, Zhang P, Cao Y, Hu T, Young P (2016) Rhizobium symbiosis contribution to short-term salt stress tolerance in alfalfa (Medicago sativa L.). Plant Soil 402:247–261 Weaver RW, Wei GR, Berryhill DL (1990) Stability of plasmids in Rhizobium phaseoli during culture. Soil Biol Biochem 22:465–469 Wegrzyn G, Wegrzyn A (2002) Stress responses and replication of plasmids in bacterial cells. Microb Cell Factories 1:2 Weidner S, Baumgarth B, Göttfert M, Jaenicke S, Pühler A, Schneiker-Bekel S, Serrania J, Szczepanowski R, Becker A (2013) Genome sequence of Sinorhizobium meliloti Rm41. Genome Announcement 1(1). doi:10.1128/genomeA.00013-12 Wernegreen JJ, Harding EE, Riley MA (1997) Rhizobium gone native: unexpected plasmid stability of indigenous Rhizobinm leguminosarum. Proc Natl Acad Sci U S A 94:5483–5488 Wielbo J, Marek-Kozaczuk M, Mazur A, Kubik-Komar A, Skorupska A (2010) Genetic and metabolic divergence within a Rhizobium leguminosarum bv. trifolii population recovered from clover nodules. Appl Environ Microbiol 76:4593–4600 Wong K, Finan TM, Golding GB (2002) Dinucleotide compositional analysis of Sinorhizobium meliloti using the genome signature: distinguishing chromosomes and plasmids. Funct Integrat Genomic 2:274–281 Xie P, Hao X, Herzberg M, Luo Y, Nies DH, Wei G (2015) Genome analysis of metal resistance genes in three plant growth promoting bacteria of legume plants in northwest mine tailings, China. J Environ Sci 27:179–187 Yip CB, Ding H, Hynes MF (2015) Counter-transcribed RNAs of Rhizobium leguminosarum repABC plasmids exert incompatibility effects only when highly expressed. Plasmid 78:37–47 Yost CK, Rath AM, Noel TC, Hynes MF (2006) Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae. Microbiology 152:2061–2074 Young JP, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH et al (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7:R34 Zahran HH (1991) Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol Fertil Soils 12:73–80 Zahran HH (1992) Characterization of root-nodule bacteria indigenous in the salt-affected soils of Egypt by lipopolysaccharide, protein and plasmid profiles. J Basic Microbiol 32:279–287 Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989 Zahran HH (2009) Enhancement of rhizobia-legumes symbiosis and nitrogen fixation for crops productivity improvement. In: Khan MS, Zaidi A, Musarrat J (eds) Microbial strategies for crop improvement. Springer-Verlag, Berlin, Hidelberg, pp 227–254 Zahran HH (2010) Legumes-microbes interactions under stressed environments. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer-Verlag, Berlin, Hidelberg, pp 353–387 Zahran HH, Sprent JI (1986) Effects of sodium chloride and polyethelene glycol on root-hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta 167:303–309 Zahran HH, Chahboune R, Moreno S, Bedmar EJ, Abdel-Fattah M, Yasser MM, Mahmoud AM (2013) Identification of rhizobial strains nodulating Egyptian grain legumes. Int Microbiol 16:157–163 Żebracki K, Koper P, Marczak M, Skorupska A, Mazur A (2015) Plasmid-encoded RepA proteins specifically autorepress individual repABC operons in the multipartite Rhizobium leguminosarum bv. Trifolii genome. PLoS ONE 10(7). doi:10.1371/journal.pone.0131907AQ10 Zhang X-S, Cheng HP (2006) Identification of Sinorhizobium meliloti early symbiotic genes by use of a positive functional screen. Appl Environ Microbiol 72:2738–2748 Zhang XX, Kosier B, Prifer UB (2001) Symbiotic plasmid rearrangement in Rhizobium leguminosarum bv. viciae VF 39SM. J Bacteriol 183:2141–2144 Zou X, Li F, Chen H (1997) Characteristics of plasmids in Rhizobium huakuii. Curr Microbiol 35:215–220