The importance of Rhizobium, Agrobacterium, Bradyrhizobium, Herbaspirillum, Sinorhizobium in sustainable agricultural production


  • Mohamad H. SHAHRAJABIAN Chinese Academy of Agricultural Sciences, Biotechnology Research Institute, Beijing 100081 (CN)
  • Wenli SUN Chinese Academy of Agricultural Sciences, Biotechnology Research Institute, Beijing 100081 (CN)
  • Qi CHENG State Key Laboratory of North China Crop Improvement and Regulation, Hebei Agricultural University, College of Life Sciences, Baoding, Hebei 071000, China; Global Alliance of HeBAU-CLS&HeQiS for BioAl-Manufacturing, College of Life Sciences, Hebei Agricultural University, Baoding, 071000 (CN)



nod, rhizobial genera, rhizobial nodulation, sustainable production


Rhizobia which are soil bacteria capable of symbiosis with legume plants in the root or stem nodules and perform nitrogen fixation. Rhizobial genera include Agrobacterium, Allorhizobium, Aminobacter, Azorhizobium, Bradyrhizobium, Devosia, Mesorhizobium, Methylobacterium, Microvirga, Ochrobacterum, Phyllobacterium, Rhizobium, Shinella and Ensifer (Sinorhizobium). Review of the literature was carried out using the keywords Rhizobium, Agrobacterium, Bradyrhizobium, Herbaspirillum and Sinorhizobium. Rhizobial nodulation symbioses steps are included flavonoid signaling, Nod factor induction, and Nod factor perception, root hair responses, rhizobial infection, cell division and formation of nitrogen-fixing nodule. Rhizobium improves sustainable production by boosting organic nitrogen content.


Abdallat AMA, Sawwan JS, Zoubi BA (2011). Agrobacterium tumefaciens-mediated transformation of callus cells of Crataegus aronia. Plant Cell Tissue and Organ Culture (PCTOC) 104:31-39.

Abdollahi M, Soleymani A, Shahrajabian MH (2018). Evaluation of yield and some physiological indices of potato cultivars in relation to chemical, biologic and manure fertilizers. Cercetari Agronomice in Moldova 51(2):53-66.

Acosta JL, Equiarte LE, Santamaria RI, Bustos P, Vinuesa P, Martinez-Romero E, Davila G, Gonzalez V (2011). Genomic lineages of Rhizobium etli revealed by the extent of nucleotide polymorphisms and low recombination. BMC Evolutionary Biology 11:305-317.

Ahemad M, Khan MS (2011). Effect of ebuconazole-tolerant and plant growth promoting Rhizobium isolate MRP1 on pea-Rhizobium symbiosis. Scientia Horticulturae 129:266-272.

Ahmad M, Zahir ZA, Khalid M, Nazli F, Arshad M (2013). Efficacy of Rhizobium and Pseudomonas strains to improve physiology, ionic balance and quality of mung bean under salt-affected conditions on farmer’s fields. Plant Physiology and Biochemistry 63:170-176.

Ahnia H, Bourebaba Y, Duran D, Boulila F, Palacios JM, Rey L, Ruiz-Argueso T, Boulila A, Imperial J (2018). Bradyrhizobium algeriense sp. nov., a novel species isolated from effective nodules of Retama sphaero carpa from Northeastern Algeria. Systematic and Applied Microbiology 41:333-339.

Alami S, Lamin H, Bouhnik O, El Faik S, Filali-Maltouf A, Abdelmoumen H, Bedmar EJ, El Idrissi MM (2019). Astragalus algarbiensis is nodulated by the genistearum symbiovar of Bradyrhizobium spp. in Morocco. Systematic and Applied Microbiology 42:440-447.

Alberton O, Kaschuk G, Hungria M (2006). Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biology and Biochemistry 38:1298-1307.

Alvarez-Martinez ER, Valverde A, Ramirez-Bahena MH, Garcia-Fraile P, Tejedor C, Mateos FP, … Velazquez E (2009). The analysis of core and symbiotic genes of rhizobia nodulatingVicia from different continents reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarum strains together with Vicia seeds. Archives in Microbiology 191:659-668.

Amarger N (2001). Rhizobia in the field. Advances in Agronomy 73:109-168.

Anyango B, Wilson KJ, Beynon JL, Giller KE (1995). Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Applied and Environmental Microbiology 61:4016-4021.

Arfaoui A, El Hadrami A, Mabrouk Y, Sifi B, Boudabous A, El Hadrami I, Daayf F, Cherif M (2007). Treatment of chickpea with Rhizobium isolates enhances the expression of phenylpropanoid defense-related genes in response to infection by Fusarium oxysporum f. sp. ciceris. Plant Physiology and Biochemistry 45:470-479.

Armendariz AL, Talano MA, Nicotra MFO, Escudero L, Breser ML, Porporatto C, Agostini E (2019). Impact of double inoculation with Bradyrhizobium japonicum E109 and Azospirillum brasilense Az39 on soybean plants grown under arsenic stress. Plant Physiology and Biochemistry 138:26-35.

Aserse AA, Rasanen LA, Assefa F, Hailemariam A, Lindstrom K (2012). Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Systematic and Applied Microbiology 35:120-131.

Babu S, Prasanna R, Bidyarani N, Nain L, Shivay YS (2015). Synergistic action of PGP agents and Rhizobium spp. for improved plant growth, nutrient mobilization and yields in different leguminous crops. Biocatalysis and Agricultural Biotechnology 4:456-464.

Bahramnejad B, Naji M, Bose R, Jha S (2019). A critical review on use of Agrobacterium rhizogenes and their associated binary vectors for plant transformation. Biotechnology Advances 37:107405.

Bahroun A, Jousset A, Mhamdi R, Mrabet M, Mhadhbi H (2018). Anti-fungal activity of bacterial endophytes associated with legumes against Fusarium solani: assessment of fungi soil suppressiveness and plant protection induction. Applied Soil Ecology 124:131-140.

Bai Y, Rottwinkel G, Feng J, Liu Y, Lamparter T (2016). Bacteriophytochromes control conjugation in Agrobacterium fabrum. Journal of Photochemistry and Photobiology B: Biology 161:192-199.

Balassa R (1957). Desoxyribonucleic acid induced changes in Rhizobia. Acta Microbiologica Academiae Scientiarum Hungaricae 4:77-84.

Baldani JI, BaldaniVLD, Seldin L, Dobereiner J (1986). Characterization of Hebaspirillum seropedicae gen. nov., sp. nov., a root-associated nitrogen-fixing bacterium. International Journal of Systematics and Bacteriology 36:86-93.

Baltrus DA, Dougherty K, Arendt KR, Huntemann M, Clum A, Pillay M, … Arnold AE (2017). Absence of genome reduction in diverse, facultative endohyphal bacteria. Microbial Genomics 3:1-12.

Belhadi D, Lajudie PD, Ramdani N, Le Roux C, Boulila F, Tisseyre P, … Laguerre G (2018). Vicia faba L. in the Bejaia region of Algeria is nodulated by Rhizobium leguminosarum sv. viciae, Rhizobium laguerreae and two new genospecies. Systematic and Applied Microbiology 41:122-130.

Bellini RG, Coronado MA, Paschoal AR, Rego TGD, Hungria M, Vasconcelos ATRD, Nicolas MF (2019). Structural analysis of a novel N-carbamoyl-D-amino acid amidohydrolase from a Brazilian Bradyrhizobium japonicum strain: In silico insights by molecular modeling, docking and molecular dynamics. Journal of Molecular Graphics and Modelling 86:35-42.

Better M, Lewis B, Corbin D, Ditta G, Helinski DR (1984). Structural relationships among Rhizobium meliloti symbiotic promoters. Cell 35:479-485.

Bhattacharya I, Das HR (2003). Cell surface characteristics of two halotolerant strains of Sinorhizobium meliloti. Microbiological Research 158:187-194.

Botsford JL, Lewis TA (1990). Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Applied and Environmental Microbiology 56:488-494.

Breedveld MW, ZevenhuizenLPTM, Zehnder AJB (1990). Osmotically induced oligo- and polysaccharide synthesis by Rhizobium meliloti SU-47. Microbiology 136:2511-2519.

Brewer TE, Stroupe ME, Jones KM (2014). The genome, proteome and phylogenetic analysis of Sinorhizobium meliloti phage ΦM12, the founder of a new group of T4-superfamily phages. Virology 450-451:84-97.

Brilli M, Fondi M, Fani R, Mengoni A, Ferri L, Bazzicalupo Mand Biondi EG (2010). The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Systems Biology 4:52.

Brique A, Devassine J, Pilard S, Cailleu D, Gosselin I (2010). Osmoregulated trehalose-derived oligosaccharides in Sinorhizobium meliloti. FEBS Letters 584:3661-3666.

Bromfield ESP, Cloutier S, Tambong JT, Thi TVT (2017). Soybeans inoculated with root zone soils of Canadian native legumes harbour diverse and novel Bradyrhizobium spp. that possess agricultural potential. Systematic and Applied Microbiology 40:440-447.

Bush AL, Pueppke SG (1991). Characterization of an unusual new Agrobacterium tumedacients strain from Chrysanthemum moriflorum Ram. Applied and Environmental Microbiology 57:2468-2472.

Cao Y, Wang E-T, Zhao L, Chen W-M, Wei G-H (2014). Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biology and Biochemistry 78:128-137.

Cao Y, Wang E, Tong W, QiaoY, Zhao L, Chen W, Wei G (2017). Population structure of Rhizobium etli-like strains nodulated with Phaseolusvulgaris in two ecoregions of China. Soil Biology and Biochemistry 112:14-23.

Cardoso P, Corticeiro S, Freitas R, Figueira E (2018). Different efficiencies of the same mechanisms result in distinct Cd tolerance within Rhizobium. Ecotoxicology and Environmental Safety 150:260-269.

Carelli M, Gnocchi S, Fancelli A, Mengoni D, Paffetti D, Scotti C, Bazzicalupo M (2000). Genetic diversity and dynamics of Sinorhizobiummeliloti populations nodulating different alfalfa cultivars in Italian soils. Applied and Environmental Microbiology 66:4785-4789.

Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009). Azospirillum brasilense Az39 and BradyrhizobiumjaponicumE109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). European Journal of Soil Biology 45:28-35.

Catalan AI, Ferreira F, Gill PR, Batista S (2007). Production of polyhydroxyalkanoates by Herbaspirillum seropedicae grown with different sole carbon sources and on lactose when engineered to express the lacZlacY genes. Enzyme and Microbial Technology 40:1352-1357.

Chahboune R, Carro L, Peix A, Barrijal A, Velazquez E, Bedmar EJ (2011). Bradyrhizobium cytisi sp. nov., isolated from effective nodules of Cytisusvillosus. International Journal of Systematic Evolution and Microbiology 61:2922-2927.

Chahboune R, Carro L, Peix A, Ramirez-Bahena MH, Barrijal S, Velazquez E, Bedmar EJ (2012). Bradyrhizobium rifense sp. nov. isolated from effective nodules of Cytisus villosus grown in the Moroccan Rif. Systematic and Applied Microbiology 35:302-305.

Chandra S, Chandra R (2011). Engineering secondary metabolite production in hairy roots. Phytochemistry Review 10:371-395.

Chaudhary SK, Inouhe M, Rai UN, Mishra K, Gupta DK (2011). Inoculation of Rhizobium (VR-1 and VA-1) induces an increasing growth and metal accumulation potential in Vigna radiate and Vigna angularis L. growing under fly-ash. Ecological Engineering 37:1254-1257.

Chaves DFS, de Souza EM, Monteiro RA, Pedrosa FDO (2009). A two-dimensional electrophoretic profile of the proteins secreted by Herbaspirillum seropedicae strain Z78. Journal of Proteomics 73:50-56.

Chekol T, Vough LR, Chaney RL (2004). Phytoremediation of polychlorinated biphenyl-contaminated soils: the rhizosphere effect. Environment International 30:799-804.

Chen X, Stone M, Schlagnhaufer C, Romaine CP (2000). A fruiting body tissue method for efficient Agrobacterium-mediated transformation of Agaricus bisporus. Applied and Environmental Microbiology 66(10):4510-4513.

Chen L, Cai Y, Liu X, Guo C, Sun S, WuC, Jiang B, Han T, Hou W (2018). Soybean hairy roots produced in vitro by Agrobacterium rhizogenese-mediated transformation. The Crop Journal 6:162-171.

Chilton WS, Stomp AM, Beringue V, Bouzar H, Vaudequin-Dransart V, Petit A, Dessaux Y (1995). The chrysopine family of Amadori-type crown gall opines. Phytochemistry 40:619-628.

Christey MC, Braun RH (2005). Production of hairy roots cultures and strategic plants by Agrobacterium rhizogenes-mediated transformation, in: Leandro Pena (Ed). Transgenic Plants: Methods and Protocols, Methods in Molecular Biology, Vol. 286, Humana Press, Totowa, New Jersey, USA 2005, pp 47-60.

Collier J (2012). Regulation of chromosomal replication in Caulobacter crescentus. Plasmid 67:76-87.

Conn HJ (1938). Taxonomic relationships of certain non-sporeforming rods in soil. Journal of Bacteriology 36:320-321.

Conn HJ (1942). Validity of the genus Alcaligenes. Journal of Bacteriology 44:353-360.

Cooper JE (2007). Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. Journal of Applied Microbiology 103:1355-1365.

Da HN, Deng SP (2003). Survival and persistence of genetically modified Sinorhizobiummeliloti in soil. Applied Soil Ecology 22:1-14.

Dai S, Ping Z, Marmey P, Zhang S, Tian W, Chen S, Beachy RN, Fauquet C (2001). Comparative analysis of transgenic rice plants obtained by Agrobacterium-mediated transformation and particle bombardment. Molecular Breeding 7:25-33.

Dall’Agnol RF, Ribeiro RA, Ormeno-Orrillo E, Rogel MA, DelamutaJRM, Andrade DS, Martinez-Romero R, Hungria M (2013). Rhizobium freirei sp. nov., a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. International Journal of Systematic and Evolutionary Microbiology 63:4167-4173.

Dang W, Wei Z-M (2007). An optimized Agrobacterium-mediated transformation for soybean for expression of binary insect resistance genes. Plant Science 173: 381-389.

Dardanelli MS, Cordoba FJFD, Espuny MR, Carvajal MAR, Diaz MES, Serrano AM, … Megias M (2008). Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biology and Biochemistry 40:2713-2721.

Das DR, Horvath B, Kundu A, Kalo P, DasGupta M (2019). Functional conservation of CYCLOPS in crack entry legume Arachis hypogaea. Plant Science 281:232-241.

Deepika KV, Raghuram M, KarialiE, Bramhachari PV (2016). Biological responses of symbiotic Rhizobium radiobacter strain VBCK1062 to the arsenic contaminated rhizosphere soils of mung bean. Ecotoxicology and Environmental Safety 134:1-10.

Degefu T, Wolde-meskel E, Woliy K, Frostegard A (2017). Phylogenetically diverse groups of Bradyrhizobium isolated from nodules of tree and annual legume species growing in Ethiopia. Systematic and Applied Microbiology 40:205-214.

De Meyer SE, van Hoorde K, Vekeman B, Braeckman T, Willems A (2011). Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biology and Biochemistry 43:2384-2396.

De Meyer SE, De Beuf K, Vekeman B, Willems A (2015). A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biology and Biochemistry 83:1-11.

Deropp RS (1951). The crown-gall problem. Botanical Reviews 17:629-670.

Dessaux Y, Petit A, Tempe J (1993). Chemistry and biochemistry of opines, chemical mediators of parasitism. Phytochemistry 34:31-38.

Dewir YH, El-Mahrouk ME, El-Banna AN (2015). In vitro propagation and preliminary results of Agrobacterium-mediated genetic transformation of Cordyline fruticosa. South African Journal of Botany 98:45-51.

D’Haeze W, Holsters M (2002). Nod factor structures, responses and perception during initiation of nodule development. Glycobiology 12:79R-105R.

Dixon R, Kahn D (2004). Genetic regulation of biological nitrogen fixation. Nature Reviews Microbiology 2:621-631.

Dohlemann J, Brennecke M, Becker A (2010). Cloning-free genome engineering in Sinorhizobium meliloti advances applications of Cre/loxP site-specific recombination. Journal of Biotechnology 233:160-170.

Dos SantosCLR, Alves GC, Macedo AVDM, Giori FG, Pereira W, Urquiaga S, Reis VM (2017). Contribution of a mixed inoculants containing strains of Burkholderia spp. and Herbaspirillum ssp. to the growth of three sorghum genotypes under increased nitrogen fertilization levels. Applied Soil Ecology 113:96-106.

Duan C, Razavi BS, Shen G, Cui Y, Ju W, Li S, Fang L (2019). Deciphering the rhizobium inoculation effect on spatial distribution of phosphatase activity in the rhizosphere of alfalfa under copper stress. Soil Biology and Biochemistry 137:107574.

Earl CD, Ronson CW, Ausubel FM (1987). Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. Journal of Bacteriology 169:1127-1136.

Egamberdieva D, Reckling M, Wirth S (2017). Biochar-based Bradyrhizobium inoculums improves growth of lupin (Lupinus angustifolius L.) under drought stress. European Journal of Soil Biology 78:38-42.

Erman M, Demir S, Ocak E, Tufenkci S, Oguz F, Akkopru A (2011). Effects of Rhizobium, arbuscular mycorrhiza and whey applications on some properties in chickpea (Cicer arietinum L.) under irrigated and rainfed conditions 1-Yield, yield components, nodulation and AMF colonization. Field Crops Research 12:14-24.

Fabra A, Castro S, Taurian T, Angelini J, Ibanez F, Dardanelli M, Tonelli M, Bianucci E, Valetti L (2010). Interaction among Arachis hypogaea L. (peanut) and beneficial soil microorganisms: how much is it known? Critical Reviews in Microbiology 36:179-194.

Falk EC, Johnson JL, BaldaniVLD, Dobereiner J, Krieg NR (1986). Deoxyribonucleic and ribonucleic acid homology studies of the genera Azospirillum and Conglomeromona. International Journal of Systematics and Bacteriology 36:80-85.

Fall F, Le Roux C, Ba AM, Fall D, Bakhoum N, Faye MN, Kane A, Ndoye I, Diouf D (2019). The rhizosphere of the halophytic grass Sporobolus robustus Kunth hosts rhizobium genospecies that are efficient on Prosopis juliflora (Sw.) DC and Vacheliaseyal (Del.) P.J.H. Hurter seedlings. Systematic and Applied Microbiology 42:232-239.

Fei C, Wang T, Woldemicael A, He M, Zou S, Wang C (2019). Nitrogen supplemented by symbiotic Rhizobium stimulates fatty-acid oxidation in Chlorella variabilis. Algal Research 44:101692.

Feng J, Li FQ, Li Q, Hu HL, Hong GF (2002). Expression and purification of Rhizobium leguminosarum NodD. Protein Expression and Purification 26:321-328.

Ferri L, GoriA, Biondi EG, Mengoni A, Bazzicalupo M (2010). Plasmid electroporation of Sinorhizobium strains: The role of the restriction gene hsdR in type Rm1021. Plasmid 63:128-135.

Ferro L, Gojkovic Z, Munoz R, Funk C (2019). Growth performance and nutrient removal of a Chlorella vulgaris-Rhizobium sp. co-culture during mixotrophic feed-batch cultivation in synthetic wastewater. Algal Research 44:101690.

Ferroni FM, Guerrero SA, Rizzi AC, Brondino CD (2012). Overexpression, purification, and biochemical and spectroscopic characterization of copper-containing nitrite reductase from Sinorhizobium meliloti. Study of the interaction of the catalytic copper center with nitrite and NO. Journal of Inorganic Biochemistry 114:8-14.

Finan TM, Hartweig E, LeMieuz K, Bergman K, Walker GC, Signer ER (1984). General transduction in Rhizobium meliloti. Journal of Bacteriology 159:120-124.

Flores-Felix JD, Velazquez E, Garcia-Fraile P, Gonzalez-Andres F, Silva LR, Rivas R (2018). Rhizobium and Phyllobacterium bacterial inoculants increase bioactive compounds and quality of strawberries cultivated in field conditions. Food Research International 111:416-422.

Flores-Felix JD, Sanchez-Juanes F, Garcia-Fraile P, Valverde A, Mateos PF, Gonzalez-Buitrago JMG, … Rivas R (2019). Phaseolus vulgaris is nodulated by the symbiovarviciae of several genospecies of Rhizobium laguerreae complex in a Spanish region where Lens culinaris is the traditionally cultivated legume. Systematic and Applied Microbiology 42:240-247.

Flores-Felix JD, Menendez E, Peix A, Garcia-Fraile P, Velazquez E (2020). History and current taxonomic status of genus Agrobacterium. Systematic and Applied Microbiology 43:126046.

Frank B (1889). Uber die Pilzsymbiose der Leguminosen. Berichte der Deutschen Botanischen Gesellschaft. 7: 332-346 (in German).

Gabor M (1965). Transformation of streptomycin markers in rough strains of Rhizobium lupini II. The relation between the determinant of streptomycin dependence and those for streptomycin resistance and sensitiveness. Genetics 52: 05-913.

Gage DJ (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Research 68:280-300.

Galibert F (2001). The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.

Galvao CW, Pedrosa FO, Souza EM, Yates MG, Chubatsu LS, Steffens MBR (2004). Expression, purification, and DNA-binding activity of the Herbaspirillum seropedicae RecX protein. Protein Expression and Purification 35:298-303.

Gao C, Long D, Lenk I, Nielsen KK (2008). Comparative analysis of transgenic tall fescue (Festuca arundinaceae Schreb.) plant obtained by Agrobacterium-mediated transformation and particle bombardment. Plant Cell Reports 27:1601-1609.

Gao Y, Duan A, Qiu X, Liu Z, Sun J, Zhang J, Wang H (2010). Distribution of roots and root length density in a maize/soybean strip intercropping system. Agricultural Water Management 98(1):199-212.

Gao F-L, Che X-X, Yu F-H, Li J-M (2019). Cascading effects of nitrogen, rhizobia and parasitism via a host plant. Flora 251:62-67.

Garcia-Fraile P, Mulas-Garcia D, Peix A, Rivas R, Gonzalez-Andres F, Velazquez E (2010). Phaseolus vulgaris is nodulated in northern Spain by Rhizobium leguminosarum strains harboring two nodC alleles present in American Rhizobium etli strains: biogeographical and evolutionary implications. Canadian Journal of Microbiology 56:657-666.

Garcia JE, Maroniche G, Creus C, Suarez-Rodriguez R, Ramirez-Trujillo JA, Groppa MD (2017). In vitro PGPR properties and osmotic tolerance of different Azospirillum native strains and their effects on growth of maize under drought stress. Microbiology Research 202:21-29.

Geurts R, Bisseling T (2002). Rhizobium nod factor perception and signaling. Plant Cell 14:S239-S249.

Gibson KE, Kobayashi H, Walker GC (2008). Molecular determinants of a symbiotic chronic infection. Annual Reviews in Genetics 42:413-441.

GillerKE, FrankeAC, Abaidoo R, Baijukya F, Bala A, Boahen S, … Vanlauwe B (2013). N2Africa: putting nitrogen fixation to work for smallholder farmers in Africa. In: Vanlauwe B, van AstenPJA, Blomme G (Eds). Agro-ecological Intensification of Agricultural Systems in the African Highlands, Routledge, London, pp 156-174.

Ghosh PK, SahaP, Mayilraj S, Maiti TK (2013). Role of IAA metabolizing enzymes on production of IAA in root, nodule of Cajanus cajan and its PGP Rhizobium sp. Biocatalysis and Agricultural Biotechnology 2:234-239.

Ghosh PK, Maiti TK (2016). Structure of extracellular polysaccharides (EPS) produced by rhizobia and their functions in legume-bacteria symbiosis: - A review. Achievements in the Life Sciences 10:136-143.

Gong Z, Zhu J, Yu G, Zou H (2007). Disruption of nifA gene influences multiple cellular processes in Sinorhizobiummeliloti. Journal of Genetics and Genomics 34(9):783-789.

Gonzalez LE, Bashan Y (2000). Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant-growth-promoting bacterium Azospirillumbrasilense. Applied and Environmental Microbiology 66:1527-1531.

Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, … Slater S (2001). Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323-2328.

Gosselin I, Wattraint O, Riboul D, Barbotin J-N, Portais J-C (2001). A deeper investigation on carbohydrate cycling in Sinorhizobiummeliloti. FEBS Letters 499:45-49.

Govarthanan M, Lee G-W, Park J-H, Kim JS, Lim S-S, Seo S-K, Cho M, Myung H, Kamala-Kannan S, Oh B-T (2014). Bioleaching characteristics, influencing factors of Cu solubilization and survival of Herbaspirillum sp. GW103 in Cu contaminated mine soil. Chemosphere 109:42-48.

Grange L, Hungria M (2004). Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biology and Biochemistry 36:1389-1398.

Gresta F, Trostle C, Sortino O, Santonoceto C, Avola G (2019). Rhizobium inoculation and phosphate fertilization effects on productive and qualitative traits of guar (Cyamopsis tetragonoloba (L.) Taub.). Industrial Crops and Products 139:111513.

Gu S-B, Yao J-M, Yuan Q-P, Xue P-J, Zheng Z-M, Yu Z-L (2006). Kinetics of Agrobacterium tumefaciens ubiquinone-10 batch production. Process Biochemistry 41:1908-1912.

Guo M, Gao D, Jin Y (2009). Progress in the formation and transfer of Agrobacterium T-complex. Progress in Biochemistry and Biophysics 36:1408-1414.

Guo M, Bian X, Wu X, Wu M (2011). Agrobacterium-mediated genetic transformation: history and progress. In: Alvarez M (Ed). Genetic Transformation. InTech, Rijeka, pp 3-28.

Guo M, Huang Z, Yang J (2017). Is there any crosstalk between the chemotaxis and virulence induction signaling in Agrobacterium tumefaciens? Biotechnology Advances 35:505-511.

Guo Y, Matsuoka Y, Miura T, Nishizawa T, Ohta H, Narisawa K (2018). Complete genome sequence of Agrobacterium pusense VsBac-Y9, a bacterial symbiont of the dark septate endophytic fungus Veronaeopsis simplexY34 with potential for improving fungal colonization in roots. Journal of Biotechnology 284:31-36.

Guo M, Ye J, Gao D, Xu N, Yang J (2019). Agrobacterium-mediated horizontal gene transfer: Mechanism, biotechnological application, potential risk and forestalling strategy. Biotechnology Advances 37:259-270.

Haag AF, Arnold MFF, Myka KK, Kerscher B, Dallangelo S, Zanda M, Mergaret P, Ferguson GP (2013). Molecular insights into bacteroid development during Rhizobium-legume symbiosis. FEMS Microbiology Reviews 37:364-383.

Han SZ, Wang ET, Chen WX (2005). Diverse bacteria isolated from root nodules of Phaseolus vulgaris and species within the genera Campylotropis and Cassia growtn in China. Systematic and Applied Microbiology 28:265-276.

Han TX, Wang ET, Han LL, Chen WF, Sui XH, Chen WX (2008). Molecular diversity and phylogeny of rhizobia associated with wild legumes native to Xinjiang, China. Systematic and Applied Microbiology 31:287-301.

Hanana M, Ayadi R, Mzid R, Khouja ML, Hanachi AS, Hamrouni L (2018). Efficient method of seed transformation via Agrobacterium tumefaciens for obtaining transgenic plants Hibiscus cannabinus L. Industrial Crops and Products 113:274-282.

He R, Pan J, Zhu L, He G (2010). Agrobacterium-mediated transformation of large DNA fragments using a BIBAC vector system in rice. Plant Molecular Biology Reporter 28:613-619.

Hidaka T, Omura M (1993). Transformation of citrus protoplasts by electroporation. Journal of Japan Society of Horticulture Sciences 62:371-376.

Hu J, Zhou Y, Lei Z, Liu G, Hua Y, Zhou W, Wan X, Zhu D, Zhao J (2020). Effects of Potamogeton crispus decline in the rhizosphere on the abundance of anammox bacteria and nirS denitrifying bacteria. Environmental Pollution 260:114018.

Huang P, Xu M, Xia L, Qing Z, Tang Q, Liu W, Zeng J (2017). Establishment of an efficient Agrobacterium-mediated genetic transformation method in Macleayacordata. Scientia Horticulturae 226:302-306.

Hungria M, Andrade DS, Chueire LMO, Probanza A, Guttierrez-Manero FJ, Megias M (2000). Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biology and Biochemistry 32(11):1515-1528.

Huser A, Takahara H, Schmalenbach W, O’Connell R (2009). Discovery of pathogenicity genes in the crucifer anthracnose fungus Colletotrichum higginsianum, using random insertional mutagenesis. Molecular Plant Microbe Interactions 22:143-156.

Ide Franzini V, Azcon R, Mendes FL, Aroca R (2010). Interaction between Glomus species and Rhizobium strains affect the nutritional physiology of drought-stressed legume hosts. Journal of Plant Physiology 167:614-619.

Idnurm A, Bailey AM, Cairns TC, Elliott CE, Foster GD, Laniri G, Jeon J (2017). A silver bullet in a golden age of functional genomics: the impact of Agrobacterium-mediated transformation of fungi. Fungal Biology and Biotechnology 4:6.

Islam MN, Nizam S, Verma PK (2012). A highly efficient Agrobacterium mediated transformation system for chickpea wilt pathogen Fusarium oxysporum f. sp. ciceri using DsRed-Express to follow root colonization. Microbiology Research 167:32-338.

Jack CN, Wozniak KJ, Porter SS, Friesen ML (2019). Rhizobia protect their legume hosts against soil-borne microbial antagonists in a hose-genotype-dependent manner. Rhizosphere 9:47-55.

Janczarek M, Rachwal K, Marzec A, Grzadziel J, Palusinska-Szysz M (2015). Signal molecules and cell-surface components involved in early stages of the legume-rhizobium interactions. Applied Soil Ecology 85:94-113.

Jeon J, Park SY, Chi MH, Choi J, ParkJ, Rho HS, … Lee YH (2007). Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nature Genetics 39:561-565.

Ji Z, Liu T, Zhang J, Yan H, WangE, Cui Q, Chen Q, Chen W (2019). Genetic divergence among Bradyrhizobium strains nodulating wild and cultivated Kummerowia spp. in China. Systematic and Applied Microbiology 42:223-231.

Jiang DW, Zhu W, Wang YC, Sun C, Zhang KQ, Yang JK (2013). Molecular tools for functional genomics in filamentous fungi: recent advances and new strategies. Biotechnology Advances 31:1562-1574.

Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007). How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nature Reviews Microbiology 5:619-633.

Jones KM, Walker GC (2008). Responses of the model legume Medicago truncatula to the rhizobial exopolysaccharide succinoglycan. Plant Signalling andBehavior 3:888-890.

Jones RW (2016). Application of succulent plant leaves for Agrobacterium infiltration-mediated protein production. Journal of Microbiological Methods 120:65-67.

Jordan DC (1982). Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen nov., a genus of slow-growing, root nodule bacteria from leguminous plants. International Journal of Systematics and Bacteriology 32:136-139.

Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019). Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicology and Environmental Safety 167:218-226.

Junier P, Alfaro M, Guevara R, Witzel K-P, Caru M (2014). Genetic diversity of Rhizobium present in nodules of Phaseolus vulgaris L. cultivated in two soils of the central region in Chile. Applied Soil Ecology 80:60-66.

Kaneko T (2000). Complete genome structure of the nitrogen fixing symbiotic bacterium Mesorhizobium loti. DNA Research 7:331-338.

Kaneko T (2002). Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Research 9:189-197.

Karoney EM, Ochieno DMW, Baraza DL, Muge EK, Nyaboga EN, Naluyange V (2020). Rhizobium improves nutritive suitability and tolerance of Phaseolus vulgaris to Colletotrichum lindemuthianum by boosting organic nitrogen content. Applied Soil Ecology 149:103534.

Kastell A, Zrenner R, Schreiner M, Kroh L, Ulrichs C, Smetanska I, Mewis I (2015). Metabolic engineering of aliphatic glucosinolates in hairy root cultures of Arabidopsis thaliana. Plant Molecular Biology Reporter 33:598-608.

Kavitake D, Delattre C, Devi PB, Pierre G, Michaud P, Shetty PH, Andhare P (2019). Physical and functional characterization of succinoglycanexoplysaccharide produced by Rhizobium radiobacter CAS from curd sample. International Journal of Biological Macromolecules 134:1013-1021.

Keller J, Imperial J, Ruiz-Argueso T, Privet K, Lima O, Michon-Coudouel S, … Cabello-Hurtado F (2018). RNA sequencing and analysis of three Lupinus nodulomes provide new insights into specific host-symbiont relationships with compatible and incompatible Bradyrhizobium strains. Plant Science 266:102-116.

Kereszt A, Mergaert P, Kondorosi E (2011). Bacteroid development in legume nodules: evolution of mutual benefit or of sacrificial victims? MolecularPlant-Microbe Interactions 24:1300-1309.

Keyser HH, Munns DN (1979). Tolerance of rhizobia to acidity, aluminium, and phosphate. Soil Science Society of America Journal 43(3):519-523.

Khoshkharam M, Rezaei A, Soleymani A, Shahrajabian MH (2010). Effects of tillage and residue management on yield components and yield of maize in second cropping after barley. Research on Crops 11(3):659-666.

Kim B-H, Ramanan R, Cho D-H, Oh H-M, Kim H-S (2014). Role of Rhizobium, a plant growth promoting bacterium, in enhancing algal biomass through mutualistic interaction. Biomass and Bioenergy 69:95-105.

Kim JW, Lee J, Yoo AY, Choi JW, Park YI, Park JK (2017). Immune-stimulating activity of water-soluble extracellular polysaccharide isolated from Rhizobium massiliae. Process Biochemistry 63:236-243.

Kinkle BK, Angle JS, Keyser HH (1987). Long-term effects of metal-rich swage sludge application on soil populations of Bradyrhizobium japonicum. Applied and Environmental Microbiology 53(2):315-319.

Klee H, Horsch R, Rogers S (1987). Agrobacterium-mediated plant transformation and its further applications to plant biology. Annual Reviews in Plant Physiology 38:467-486.

Kobayashi S, Uchimiya H (1989). Expression and integration of a foreign gene in orange (Citrus sinensis Osb.) protoplasts by direct DNA transfer. Idengaku Zasshi 64:91-97.

Koetle MJ, Finnie JF, Balazs E, Van Staden J (2015). A review on factors affecting the Agrobacterium-mediated genetic transformation in ornamental monocotyledonous geophytes. South African Journal of Botany 98:37-44.

Kuykendall LD, Saxena B, Devine TE, Udell SE (1992). Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobiumelkanii sp. nov. Canadian Journal of Microbiology 38:501-505.

Leclerque A, Wan H, Abschutz A, Chen S, MitinaGV, Zimmermann G, Schairer HU (2004). Agrobacterium-mediated insertional mutagenesis (AIM) of the entomopathogenic fungus Beauveria bassiana. Current Genetics 45:111-119.

Laguerre G, Mazurier SI, Amarger N (1992). Plasmid profiles and restriction fragment length polymorphism of Rhizobium leguminosarum bv. viciae in field populations. FEMS Microbiology Letters 101(1):17-26.

Leon-Barrios M, Perez-Yepez J, Dorta P, Garrido A, Jimenez C (2017). Alkalinity of Lanzarote soils is a factor shaping rhizobial populations with Sinorhizobium meliloti being the predominant microsymbiont of Lotus lancerottensis. Systematic and Applied Microbiology 40:171-178.

LiY, Wang ET, Liu Y, Li X, Yu B, Ren C, Liu W, Li Y, Xie Z (2016). Rhizobium anhuiense as the predominant microsymbionts of Lathyrus maritimus along the Shandong Peninsula seashore line. Systematic and Applied Microbiology 39:384-390.

Li X, Jiang Z, Shen Y, Li F, Yu X, Qu S (2018). In vitro regeneration and Agrobacterium tumefaciens-mediated genetic transformation of D. lotus (Diospyroslotus L.). Scientia Horticulturae 236:229-237.

Li YH, Wang R, Sui XH, Wang ET, Zhang XX, Tian CF, Chen WF, Chen WX (2019). Bradyrhizobium nanningense sp. nov., Bradyrhizobium guangzhouense sp. nov. and Bradyrhizobium zhanjiangense sp. nov., isolated from effective nodules of peanut in Southeast China. Systematic and Applied Microbiology 42:126002.

Li J, Hong N, Peng B, Wu H, Gu Q (2019). Transformation of Corynespora cassiicola by Agrobacterium tumefaciens. Fungal Biology 123:669-675.

Lindstrom K, Mousavi SA (2010). Rhizobium and other N-fixing symbioses. In: Encyclopedia of life science (ELS). John Wiley & Sons, Ltd., Chichester.

Lindstrom K, Aserse AA, Mousavi SA (2013). Taxonomy and evolution of nitrogen-fixing organisms. In: de Bruijn FJ (Ed). Biological Nitrogen Fixation. John Wiley & Sons, Inc.

Liu L, He Z, Wang K, Xie Y, Xie Q, O׳Donnell AG, Chen C (2015). The Bradyrhizobium-legume symbiosis is dominant in the shrubby ecosystem of the Karst region, Southwest China. European Journal of Soil Biology 68:1-8.

Liu C-W, Murray JD (2016). The role of flavonoids in nodulation host-range specificity: an update. Plants Basel Switz. 5.

Liu YH, Wang ET, Jiao YS, Tian CF, Wang L, Wang ZJ, … Chen WF (2018). Symbiotic characteristics of Bradyrhizobium diazoefficiens USDA 110 mutants associated with shrubby sophora (Sophora flavescens) and soybean (Glycine max). Microbiological Research 214:19-27.

Long SR (1989). Rhizobium-legume nodulation: life together in the underfound. Cell 56:203-214.

Long L, LinQ, Shi Y, Wang J, Ding S (2018). Highly efficient transformation of a (hemi-)cellulases-producting fungus Eupenicillium parvum 4-14 by Agrobacterium tumefaciens. Journal of Microbiological Methods 146:40-45.

Lopez-Lopez A, Rogel-Hernandez MA, Barois I, Ceballos AIO, Martinez J, Ormeno-Orrillo E, Martinez-Romero E. (2012). Rhizobium grahamii sp. nov., from nodules of Dalea leporine, Leucaena leucocephala and Clitoriaternatea, and Rhizobium mesoamericanum sp. nov., from nodules of Phaseolus vulgaris, siratro, cowpea and Mimosa pudica. International Journal of Systematic and Evolutionary Microbiology 62:2264-2271.

Lubambo AF, Benelli EM, Klein JJ, Schreiner WH, Silveira E, de Camargo PC (2013). Tuning protein GlnB-Hs surface interaction with silicon: FTIR-ATR, AFM and XPS study. Colloids and Surfaces B: Biointerfaces 102:348-353.

Majumdar S, Garaj S, Jha S. (2011). Genetic transformation of Bacopamonnieri by wild type strains of Agrobacterium rhizogenes stimulates production of bacopa saponins in transformed calli and plants. Plant Cell Reports 30:941-954.

Marek-Kozaczuk M, Leszcz A, Wielbo J, Wdowiak-Wrobel S, Skorupska A (2013). Rhizobium pisi sv. trifolii K3.22 harboring nod genes of the Rhizobium leguminosarumsv. trifolii cluster. Systematic and Applied Microbiology 36:252-258.

Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991). Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. International Journal of Systematic Bacteriology 41:417-426.

Matos D, Sa C, Cardoso P, Pires A, Rocha SM, Figueira E (2019). The role of volatiles in Rhizobium tolerance to cadmium: effects of aldehydes and alcohols on growth and biochemical endpoints. Ecotoxicology and Environmental Safety 186:109759.

Mehmannavaz R, Prasher SO, Ahmad D (2002). Rhizospheric effects of alfalfa on biotransformation of polychlorinated biphenyls in a contaminated soil augmented with Siorhizobium meliloti. Process Biochemistry 37:955-963.

Mellal H, Yacine B, Boukaous L, Khouni S, Benguedouar A, Castellano-Hinojosa A, Bedmar EJ (2019). Phylogenetic diversity of Bradyrhizobium strains isolated from root nodules of Lupinus angustifolius grown wild in the North East of Algeria. Systematic and Applied Microbiology 42:397-402.

Michielse CB, Hooykaas PJ, Van Den Hondel CA, Ram AF (2008). Agrobacterium-mediated transformation of the filamentous fungus Aspergillus awamori. Nature Protocols 3:1671-1678.

Michielse CB, van Wijk R, Reijnen L, Cornelissen BJ, Rep M (2009). Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biology10:R4.

Miller KJ, Wood JM (1996). Osmoadaptation by rhizosphere bacteria. Annual Reviews in Microbiology 50:101-136.

Mnasri B, Saidi S, Chihaoui SA, Mhamdi R (2012). Sinorhizobium Americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Systematic and Applied Microbiology 35:263-269.

Mnasri B, Liu TY, Saidi S, Chen WF, Chen WX, Zhang XX, Mhamdi R (2014). Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. International Journal of Systematic and Evolutionary Microbiology 058651-058650.

Moawad H, Beck DP (1991). Some characteristics of Rhizobium leguminosarum isolates from uninoculated field-grown lentil. Soil Biology and Biochemistry 23(10):933-937.

Monteiro RA, Souza EM, Yates MG, Pedrosa FO, Chubatsu LS (1999). In-trans regulation of the N-truncated-NIFA protein of Herbaspirillum seropedicae by the N-terminal domain. FEMS Microbiology Letters 180:157-161.

Monteiro RA, de Souza EM, Wassem R, Geoffrey Yates M, Pedrosa FO, Chubatsu LS (2001). Inter-domain cross-talk control the NifA protein activity of Herbaspirillum seropedicae. FEBS Letters 508:1-4.

Monteiro RA, Souza EM, Yates MG, Steffens MBR, Pedrosa FO, Chubatsu LS (2003). Expression, purification, and functional analysis of the C-terminal domain of HerbaspirillumseropedicaeNifA protein. Protein Expression and Purification 27:313-318.

Moon YS, Donzelli BG, Krasnoff SB, McLane H, Griggs MH, Cooke P, … Churchill AC (2008). Agrobacterium-mediated disruption of a nonribosomal peptide synthetase gene in the invertebrate pathogen Metarhizium anisopliae reveals a peptide spore factor. Applied and Environmental Microbiology 74(14):4366-4380.

Moorman TB (1986). Effects of herbicides on the survival of Rhizobium japonicum strains. Weed Science 34(4):628-633.

Moraes NDJ, Neto VPDC, Araujo ASFD, Figueiredo MDVB, Bonifacio A, Rodriguez AC (2016). Bradyrhizobium sp. inoculation ameliorates oxidative protection in cowpea subjected to long-term composted tannery sludge amendment. European Journal of Soil Biology 76:35-45.

Moulin L, Bena G, Boivin-Masson C, Stepkowski T (2004). Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Molecular Phylogenetics and Evolution 30:720-732.

Mousavi SA, Osterman J, Wahlberg N, Nesme X, Lavire C, Vial L, … Lindstrom K (2014). Phylogeny of the Rhizobium-Allorhizobium-Agrobacterium clade supports the delineation of Neorhizobium gen. nov. Systematic and Applied Microbiology 37:208-215.

Mullins ED, Kang S (2001). Transformation: a tool for studying fungal pathogens plants. Cellular and Molecular Life Sciences 58:2043-2052.

Mullins ED, Chen X, Romaine P, Raina R, Geiser DM, Kang S (2001). Agrobacterium-mediated transformation of Fusarium oxysporum: an efficient tool for inserional mutagenesis and gene transfer. Phytopathology 91(2):173-180.

Murugan A, Prathiviraj R, Mothay D, Chellapandi P (2019). Substrate-imprinted docking of Agrobacterium tumefaciens urinate dehydrogenase for increased substrate selectivity. International Journal of Biological Macromolecules 140:1214-1225.

Mwenda GM, O’Hara GW, De Meyer SE, Howieson JG, Terpolilli JJ (2018). Genetic diversity and symbiotic effectiveness of Phaseolus vulgaris-nodulating rhizobia in Kenya. Systematic and Applied Microbiology 41:291-299.

Nabeshima T, Doi M, Hosokawa M (2016). Agrobacterium-mediated inoculation of chrysanthemum (Chrysanthemum morifolium) plants with chrysanthemum stunt viroid. Journal of Virological Methods 234:169-173.

Nandasena KG, O’Hara GW, Tiwari RP, Yates RJ, Kishinevsky BD, Howieson JG (2004). Symbiotic relationships and root nodule ultrastructure of the pasture legume Biserrula pelecinus L.- a new legume in agriculture. Soil Biology and Biochemistry 36:1309-1317.

Nathoo N, MacDonald J, Weselowski B, Yuan Z-C (2019). Comparative transcriptomic analysis reveals different responses of Arabidopsis thaliana roots and shoots to infection by Agrobacterium tumefaciens in a hydroponic co-cultivation system. Physiological and Molecular Plant Pathology 106:109-119.

Nester EW (2015). Agrobacterium: nature’s genetic engineer. Frontiers in Plant Science 5:730.

Niazian M, Sadat-Noori SA, Tohidfar M, Galuscka P, Mortazavian SMM (2019). Agrobacterium-mediated genetic transformation of ajowan (Trachys permumammi (L.) Sprague): an important industrial medicinal plant. Industrial Crops and Products 132:29-40.

Nick G, de Lajudie P, Eardly BD, Suomalainen S, Paulin L, Zhang XP, Gillis M, Lindstrom K (1999). Sinorhizobium arboris sp. nov. and Sinorhzobium kostiense sp. nov., isolated from leguminous tress in Sudan and Kenay. International Journal of Systematic and Evolutionary Microbiology 49:1359-1368.

Niedz RP, McKendree WL, Shatters RC (2003). Electroporation of embryogenic protoplasts of sweet organe (Citrus sinensis (L.) Osbeck) and regeneration of transformed plants. In Vitro Cellular & Developmental Biology-Plant 39:586-594.

Noindorf L, Bonatto AC, Monteiro RA, Souza EM, Rigo LU, Pedrosa FO, Steffens MB, Chubatsu LS (2011). Role of P II proteins in nitrogen fixation control of Herbaspirillum seropedicae strain SmR1. BMC Microbiology 11:8.

Nowak P, Soupas L, Thomas-Oates J, Lindstrom K (2004). Acacia senegal and Prosopis chilensis-nodulating rhizobia Sinorhizobium arboris HAMBI 2361 and S. kostiense HAMBI 2362 produce tetra- and pentameric LCOs that are N-methylated, O-6-carbamoylated and partially sulfated. Carbohydrate Research 339:1061-1067.

Nyoki D, Ndakidemi PA (2018). Rhizobium inoculation reduces P and K fertilization requirement in corn-soybean intercropping. Rhizosphere 5:51-56.

Oliveira MAS, Baura VA, Aquino B, Hergo LF, Kadowaki MAS, Chubatsu LS, … Monteiro RA (2009). Role of conserved cysteine residues in Herbaspirillum seropedicae NifA activity. Research in Microbiology 160:389-395.

Oliveira MAS, Aquino B, Bonatto AC, Huergo LF, Chubatsu LS, Pedrosa FO, … Monteiro RA (2012). Interaction of GlnK with the GAF domain of Herbaspirillum seropedicae NifA mediates NH4+-regulation. Biochimie 94:1041-1047.

O’Neill K, Larsen JS, Curtis WR (2008). Scale-up of Agrobacterium-mediated transient protein expression in bioreactor-grown Nicotiana glutinosa plant cell suspension culture. Biotechnology Programme 24:372-376.

Osei O, Abaidoo RC, AhiaborBDK, Boddey RM, Rouws LFM (2018). Bacteria related to Bradyrhizobium yuanmingense from Ghana are effective groundnut micro-symbionts. Applied Soil Ecology 127:41-50.

Ozawa K (2009). Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). Plant Science 176:522-527.

Ozawa K, Takaiwa F (2010). Highly efficient Agrobacterium-mediated transformation of suspension-cultured cell clusters of rice (Oryza sativa L.). Plant Science 179:333-337.

Pacurar DI, Thordal-Christensen H, Pacurar ML, Pamfil D, Botez C, Bellini C (2011). Agrobacterium tumefaciens: From crown gall tumors to genetic transformation. Physiological and Molecular Plant Pathology 76:76-81.

Palanichelvam K, Oger P, Clough SJ, Cha C, Bent AF, Farrand SK (2000). A second t-region of the soybean-supervirulentchrysopine-type Ti plasmid pTiChry5, and construction of a fully disarmed vir helper plasmid. MolecularPlant-Microbe Interactions 13:1081-1091.

Park SY, Jeong MH, Wang HY, Kim JA, Yu NH, Kim S, … Hur JS (2013). Agrobacterium tumefaciens-mediated transformation of the lichen fungus, Umbilicaria muehlenbergii. PLoS One 8(12):e83896.

Pedrosa FO, Benelli EM, Yates MG, Wassem R, Monteiro RA, Klassen G, … Rigo LU (2001). Recent developments in the structural organization and regulation of nitrogen fixation genes in Herbaspirilum seropedicae. Journal of Biotechnology 91:189-195.

Peix A, Ramirez-Bahena MH, Velazquez E, Bedmar EJ (2015). Bacterial associations with legumes. Critical Reviews in Plant Science 34:17-42.

Perez-Peralta PJ, Ferrera-Cerrato R, Alarcon A, Trejo-Tellez LI, Cruz-Ortega R, Silva-Rojas HV (2019). Respuesta del simbiosistema frijol (Phaseolus vulgaris L.) y Rhizobium tropici CIAT899 ante elefectoalelopatico de Ipomoea purpurea L. Roth. Revista Argentina De Microbiologia 51(1):47-55.

Pessoa DDV, Vidal MS, Baldani JI, Simoes-Araujo JL (2016). Validation of reference genes for RT-qPCR analysis in Herbaspirillum seropedicae. Journal of Microbiology Methods 127:193-196.

Pizzimenti S, Ciamporcero E, Daga M, Pettazzoni P, Arcaro A (2013). Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Frontiers in Physiology 4:1-17.

Prell J, Poole P (2006). Metabolic changes of rhizobia in legume nodules. Trends in Microbiology 14(4):161-168.

Radwan SS, Dashti N, El-Nemer I, Khanafer M (2007). Hydrocarbon utilization by nodule bacteria and plant growth-promoting rhizobacteria. International Journal of Phytoremediation 9:475-486.

Ramirez-Bahena MH, Velazquez E, Fernandez-Santos F, Peix A, Martinez-Molina E, Mateos PF (2009). Phenotypic, genotypic and symbiotic diversities in strain nodulating clover in different soils in Spain. Canadian Journal of Microbiology 55:1207-1216.

Ramirez-Bahena MH, Peix A, Rivas R, Camacho R, Rodriguez-Navarro DN, Mateos PF, … Velazquez E (2009). Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizuserosus. International Journal of Systematics and Evolutionary Microbiology 59:1929-1934.

Ramirez-Bahena MH, Flores-Felix JD, Velazquez E, Peix A (2010). The Mimosoid tree Leucaena leucocephala can be nodulated by the symbiovargenistearum of Bradyrhizobium canariense. Systematic and Applied Microbiology 43:126041.

Reichman SM (2007). The potential use of the legume-rhizobium symbiosis for the remediation of arsenic contaminated sites. Soil Biology and Biochemistry 39:2587-2593.

Reichman SM (2014). Probing the plant growth-promoting and heavy metal tolerance characteristics of BradyrhizobiumjaponicumCB1809. European Journal of Soil Biology 63:7-13.

Reinhold BB, Chan SY, Reuber TL, Marra A, Walker GC, Reinhold VN (1994). Detailed structural characterization of succinoglycan, the major exopolysaccharide of Rhizobium meliloti Rm 1021. Journal of Bacteriology 176:1997-2002.

Rejili M, Mahdhi M, Fterich A, Dhaoui S, Guefrachi I, Abdeddayem R, Mars M (2012). Symbiotic nitrogen fixation of wild legumes in Tunisia: soil fertility dynamics, field nodulation and nodules effectiveness. Agriculture, Ecosystems and Environment 157:60-69.

Riah N, Bena G, Djekoun A, Heulin K, de Lajudie P, Laguerre G (2014). Genotypic and symbiotic diversity of rhizobium populations associated with cultivated lentil and pea in sub-humid and semi-arid regions of Eastern Algeria. Systematic and Applied Microbiology 37(5):368-375.

Riaziat A, Soleymani A, Shahrajabian MH (2012). Changes in seed yield and biological yield of six wheat cultivars on the basis of different sowing dates. Journal of Food, Agriculture and Environment 10(1):467-469.

Rogel MA, Ormeno-Orrillo E, Martinez-Romero E (2011). Symbiovars in rhizobia reflect bacterial adaptation to legumes. Systematic and Applied Microbiology 34:96-104.

Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC (1996). Sinorhizobium medicae sp. non., isolated from annual Medicago spp. International Journal of Systematic Bacteriology 46:972-980.

Roumiantseva ML, YakutkinaVV, Damman-Kalinowski T, Sharypova LA, Keller M, Simarov BV (1999). Comparative analysis of structural organization of the genome in alfalfa nodule bacteria Sinorhizobium medicae and Sinorhizobium meliloti. Russian Journal of Genetics 35:135-159.

Sadowskyt MJ, Bohloolt BBEN (1986). Growth of fast- and slow-growing rhizobia. Applied and Environmental Microbiology 52:951-953.

Saidi S, Ramirez-Bahena MH, Santillana N, Zuniga D, Alvarez-Martinez E, Peix A, Mhamdi R, Velazquez E (2014). Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. International Journal of Systematic and Evolutionary Microbiology 64:242-247.

Sanchez-Pardo B, Zornoza P (2014). Mitigation of Cu stress by legume-Rhizobium symbiosis in white lupin and soybean plants. Ecotoxicology and Environmental Safety 102:1-5.

Sanchez AC, Gutierrez RT, Santana RC, Urrutia AR, Fauvart M, Michiels J, Vanderleyden J (2014). Effects of co-inoculation of native Rhizobium and Pseudomonas strains on growth parameters and yield of two contrasting Phaseolus vulgaris L. genotypes under Cuban soil conditions. European Journal of Soil Biology 62:105-112.

Sanchez-Romero JJ, Olguin LF (2015). Choline sulfatase from Ensifer (Sinorhizobium) meliloti: Characterization of the unmodified enzyme. Biochemistry and Biophysics Reports 3:161-168.

Saranya Devi E, Vijayendra SVN, Shamala TR (2012). Exploration of rice bran, an agro-industry residue, for the production of intra- and extra-cellular polymers by Sinorhizobium meliloti MTCC 100. Biocatalysis and Agricultural Biotechnology 1:80-84.

Satyavathi VV, Prasad V, Gita Lakshmi B, Lakshmi Sita G (2002). High efficiency transformation protocol for three Indian cotton varieties via Agrobacterium tumefaciens. Plant Science 162:215-223.

Sawada H, Kuykendall LD, Young JM (2003). Changing concepts in the systematic of bacterial nitrogen-fixing legume symbionts. Journal of General and Applied Microbiology 49:155-179.

Selvaraj A, Thangavel K, Uthandi S (2020). Arbuscular mycorrhizal fungi (Glomus intraradices) and diazotrophic bacterium (Rhizobium BMBS) primed defense in blackgram against herbivorous insect (Spodoptera litura) infestation. Microbiological Research 231:126355.

Serrato RV, Balsanelli E, Sassaki GL, Carlson RW, Muszynski A, Monteiro RA, … Iacomini M (2012). Structural analysis of Herbaspirillum seropedicae lipid- A and of two mutants defective to colonize maize roots. International Journal of Biological Macromolecules 51:384-391.

Servin-Garciduenas LE, Moral AZ-D, Ormeno-Orrillo E, Rogel MA, Delgado-Salinas A, Sanchez F, Martinez-Romero E (2014). Symbiont shift towards Rhizobium nodulation in a group of phylogenetically related Phaseolus species. Molecular Phylogenetics and Evolution 79:1-11.

Shah V, Subramaniam S (2018). Bradyrhizobium japonicum USDA110: A representative model organism for studying the impact of pollutants on soil microbiota. Science of the Total Environment 624:963-967.

Shahid M, Saghir Khan M (2019). Fungicide tolerant Bradyrhizobium japonicum mitigate toxicity and enhance green gram production under hexaconazole stress. Journal of Environmental Sciences 78:92-108.

Shamseldin A, Abdelkhalek A, Sadowsky MJ (2017). Recent changes to the classification of symbiotic, nitrogen-fixing, legume-associating bacteria: a review. Symbiosis 71:91-109.

Sharajabian MH, Sun W, Cheng Q (2019a). Climate change, acupuncture and traditional Chinese herbal medicines. Pharmacognosy Communications 9(3):91-95.

Shahrajabian MH, Sun W, Cheng Q (2019b). Clinical aspects and health benefits of ginger (Zingiber officinale) in both traditional Chinese medicine and modern industry. Acta Agriculturae Scandinavica, Section B - Soil and Plant Science.

Shahrajabian MH, Sun W, Cheng Q (2020). Chinese star anise (lllicium verum) and pyrethrum (Chrysanthemum cinerariifolium) as natural alternatives for organic farming and health care- A review. Australian Journal of Crop Science 14(03):517-523.

Shamala TR, Rohinishree YS, Vijayendra SVN (2014). Biosynthesis of multiple biopolymers by Sinorhizobium meliloti CFR 14 in high cell density cultures through fed batch fermentation. Biocatalysis and Agricultural Biotechnology 3:316-322.

Shamseldin A, Moawad H, El-Rahim WMA, Sadowsky MJ (2014). Near-full length sequencing of 16S rDNA and RFLP indicates that Rhizobium etli is the dominants species nodulating Egyptian winter Berseem clover (Trifolium alexandrum L.). Systematic and Applied Microbiology 37:121-128.

Shamseldin A, Carro L, Peix A, Velazquez E, Moawad H, Sadowsky MJ (2016). The symbiovartrifolii of Rhizobium bangladeshense and Rhizobium aegyptiacum sp. nov.




How to Cite

SHAHRAJABIAN, M. H., SUN, W., & CHENG, Q. (2021). The importance of Rhizobium, Agrobacterium, Bradyrhizobium, Herbaspirillum, Sinorhizobium in sustainable agricultural production. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(3), 12183.



Review Articles
DOI: 10.15835/nbha49312183