Genetic Variability of Rhizobium and its Correspondence with Plant Genotype Response: A Systematic Review
DOI:
https://doi.org/10.59890/ijist.v3i12.243Keywords:
Genetic Variability, Genotype × Genotype Interaction, Plant Responsiveness, Rhizobium, Systematic ReviewAbstract
Rhizobium-legume symbiosis is a cornerstone of sustainable agriculture, yet the integrated understanding of how bacterial genomic variation determines phenotypic outcomes across different host genotypes remains fragmented. This systematic review aims to synthesize the correspondence between Rhizobium genetic variability and plant genotype responses. Using a structured PRISMA framework, 86 studies were selected to analyze genomic diversity patterns, host responsiveness, and Genotype × Genotype (G×G) interactions. The synthesis reveals that rhizobial diversity is shaped by variations in housekeeping genes, symbiotic islands, and plasmid-borne nod and nif clusters, which drive nodulation competitiveness and environmental adaptation. Correspondingly, host plant responsiveness is actively modulated by specific genetic architectures, such as Rj genes in soybeans and immune receptors in Medicago, creating a selective filter for bacterial partners. The results demonstrate consistent G×G specificity, ranging from strict compatibility in specialized systems to flexible interactions in woody legumes, all of which are influenced by environmental pressures. A conceptual framework is proposed, describing symbiosis as an emergent system where microbial genomic modules interact with plant regulatory networks to determine nitrogen fixation efficiency. The study concludes that optimizing agronomic performance requires coordinating microbial genomic traits with host plant genetics, emphasizing the need for genotype-matched inoculants and molecular breeding strategies to enhance biological nitrogen fixation stability.
References
Abd-Alla, M. H., Al-Amri, S. M., & El-Enany, A. W. E. (2023). Enhancing rhizobium–legume symbiosis and reducing nitrogen fertilizer use are potential options for mitigating climate change. Agriculture, 13(11), 2092. https://doi.org/10.3390/agriculture13112092
Andrade-Domínguez, A., Trejo-Hernández, A., Vargas-Lagunas, C., & Encarnación-Guevara, S. (2021). Phenotypic plasticity and a new small molecule are involved in a fungal-bacterial interaction. Scientific Reports, 11.0(1). https://doi.org/10.1038/s41598-021-98474-y
Araya, S., Elia, P., Quigley, C., & Song, Q. (2023). Genetic variation and genetic complexity of nodule occupancy in soybean inoculated with USDA110 and USDA123 rhizobium strains. BMC Genomics, 24.0(1). https://doi.org/10.1186/s12864-023-09627-4
Ayra, L., Reyero-Saavedra, M., Isidra-Arellano, M., Lozano, L., Ramirez-Yáñez, M., Leija-Salas, A., Fuentes, S., Girard, L., Valdés-López, O., & Hernández, G. (2021).
Control of the Rhizobia Nitrogen-Fixing Symbiosis by Common Bean MADS-Domain/AGL Transcription Factors. Frontiers in Plant Science, 12.0. https://doi.org/10.3389/fpls.2021.679463
Azib, S., Cheloufi, H., Attab, S., Bouras, N., & Holtz, M. (2022). Phenotypic and Genotypic Diversity of Microsymbionts Nodulating Medicago sativa (L.) in the Algerian Sahara. Jordan Journal of Biological Sciences, 15.0(2). https://doi.org/10.54319/jjbs/150210
Basbuga, S., Basbuga, S., Yayla, F., Mahmoud, A., & Can, C. (2021). Diversity of rhizobial and non-rhizobial bacteria nodulating wild ancestors of grain legume crop plants. International Microbiology, 24.0(2). https://doi.org/10.1007/s10123-020-00158-6
Batstone, R., Burghardt, L., & Heath, K. (2022). Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont. Proceedings of the Royal Society B: Biological Sciences, 289.0(1978). https://doi.org/10.1098/rspb.2022.0477
Batstone, R., Lindgren, H., Allsup, C., Goralka, L., Riley, A., Grillo, M., Marshall-Colón, A., & Heath, K. (2022). Genome-Wide Association Studies across Environmental and Genetic Contexts Reveal Complex Genetic Architecture of Symbiotic Extended Phenotypes. mBio, 13.0(6). https://doi.org/10.1128/mbio.01823-22
Belousova, M., Malovichko, Y., Shikov, A., Nizhnikov, A., & Antonets, K. (2021). Dissecting the environmental consequences of bacillus thuringiensis application for natural ecosystems. Toxins, 13.0(5). https://doi.org/10.3390/toxins13050355
Borhani, B., Khodakaramian, G., & Velázquez, E. (2022). Diversity and phylogeny of the bacterial strains isolated from nodules of fenugreek (Trigonella foenum-graecum L.) in Iran. FEMS Microbiology Letters, 369.0(1). https://doi.org/10.1093/femsle/fnac045
Castellano-Hinojosa, A., Correa-Galeote, D., Ramírez-Bahena, M., Tortosa, G., González-López, J., Bedmar, E., & Peix, Á. (2021). Agrobacterium leguminum sp. Nov., isolated from nodules of phaseolus vulgaris in spain. International Journal of Systematic and Evolutionary Microbiology, 71.0(12). https://doi.org/10.1099/ijsem.0.005120
Chaddad, Z., Lamrabet, M., Bouhnik, O., Sportès, A., Alami, S., Lamin, H., Kaddouri, K., Bennis, M., Mnasri, B., Abdelmoumen, H., Wipf, D., Courty, P., & Missbah El Idrissi, M. (2023). Genetic diversity, phenotypic traits, and symbiotic efficiency of native Bradyrhizobium strains of Lupinus luteus in Morocco. Plant and Soil, 493.0(1-2). https://doi.org/10.1007/s11104-023-06236-8
Chen, M., Pu, X., Weng, M., Chen, L., Zhu, L., & Tuo, L. (2022). Description and genomic characterization of Jiella flava sp. nov., isolated from Acrostichum aureum. International Journal of Systematic and Evolutionary Microbiology, 72.0(10). https://doi.org/10.1099/ijsem.0.005514
Chen, W., Li, J., Yuan, H., You, L., Wei, Q., Feng, R., Jiang, S., & Zhao, X. (2023). Plant growth regulators improve nitrogen metabolism, yield, and quality of soybean–rhizobia symbiosis. Annals of Microbiology, 73.0(1). https://doi.org/10.1186/s13213-023-01721-y
Chhetri, G., Kim, J., Kim, I., Kang, M., So, Y., & Seo, T. (2021). Oryzicola mucosus gen. nov., sp. nov., a novel slime producing bacterium belonging to the family Phyllobacteriaceae isolated from the rhizosphere of rice plants. Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology, 114.0(11). https://doi.org/10.1007/s10482-021-01651-2
Da Silva, K., Quisen, R., Goldbach, J., Pepe, K., & Kalil Filho, A. (2022). Plant growth-promoting endophytic bacteria in peach palm seedlings; Bactérias endofíticas promotoras de crescimento de plantas em mudas de pupunheira. Pesquisa Agropecuaria Brasileira, 57.0. https://doi.org/10.1590/S1678-3921.PAB2022.V57.02962
Darrington, M., Leftwich, P., Holmes, N., Friend, L., Clarke, N., Worsley, S., Margaritopolous, J., Hogenhout, S., Hutchings, M., & Olujimi, T. (2022). Characterisation of the symbionts in the Mediterranean fruit fly gut. Microbial Genomics, 8.0(4). https://doi.org/10.1099/mgen.0.000801
de Moura, G., Mouffok, S., Gaudu, N., Cazalé, A., Milhes, M., Bulach, T., Valiere, S., Roche, D., Ferdy, J., Masson-Boivin, C., Capela, D., & Remigi, P. (2023). A Selective Bottleneck during Host Entry Drives the Evolution of New Legume Symbionts. Molecular Biology and Evolution, 40.0(5). https://doi.org/10.1093/molbev/msad116
Dwivedi, S., Quiroz, L., Reddy, A., Spillane, C., & Ortiz, R. (2023). Alternative Splicing Variation: Accessing and Exploiting in Crop Improvement Programs. International Journal of Molecular Sciences, 24.0(20). https://doi.org/10.3390/ijms242015205
Fagorzi, C., Bacci, G., Huang, R., Cangioli, L., Checcucci, A., Fini, M., Perrin, E., Natali, C., diCenzo, G., & Mengoni, A. (2021). Nonadditive transcriptomic signatures of genotype-by-genotype interactions during the initiation of plant-rhizobium symbiosis. mSystems, 6.0(1). https://doi.org/10.1128/mSystems.00974-20
Fahsi, N., Mahdi, I., Mesfioui, A., Biskri, L., & Allaoui, A. (2021). Phosphate solubilizing rhizobacteria isolated from jujube ziziphus lotus plant stimulate wheat germination rate and seedlings growth. PeerJ, 9.0. https://doi.org/10.7717/peerj.11583
Fall, F., Le Roux, C., Bá, A., Fall, D., Bakhoum, N., Faye, M., Sadio, O., & Diouf, D. (2021). The leguminous trees Vachellia seyal (Del.) and Prosopis juliflora (Swartz) DC and their association with rhizobial strains from the root-influence zone of the grass Sporobolus robustus Kunth. Symbiosis, 84.0(1).
https://doi.org/10.1007/s13199-021-00763-7
Ford, S., Moeskjær, S., Young, P., Santamaría, R., & Harrison, E. (2021). Introducing a Novel, Broad Host Range Temperate Phage Family Infecting Rhizobium leguminosarum and Beyond. Frontiers in Microbiology, 12.0. https://doi.org/10.3389/fmicb.2021.765271
Hemmerle, L., Maier, B., Bortfeld-Miller, M., Ryback, B., Gäbelein, C., Ackermann, M., & Vorholt, J. (2022). Dynamic character displacement among a pair of bacterial phyllosphere commensals in situ. Nature Communications, 13.0(1).
https://doi.org/10.1038/s41467-022-30469-3
Hsouna, J., Ilahi, H., Han, J., Gritli, T., Ellouze, W., Zhang, X., Mansouri, M., Rahi, P., Missbah El Idrissi, M., Lamrabet, M., Oubla, M., Courty, P., Wipf, D., Tambong, J., & Mnasri, B. (2023). Rhizobium acaciae sp. nov., a new nitrogen-fixing symbiovar isolated from root nodules of Acacia saligna in Tunisia. International Journal of Systematic and Evolutionary Microbiology, 73.0(5).
https://doi.org/10.1099/ijsem.0.005900
Huang, Q. (2024). Enhancing soil health and biodiversity through nitrogen fixation symbiosis in leguminous plants. Molecular Microbiology Research, 14. http://dx.doi.org/10.5376/mmr.2024.14.0006
Hug, S., Liu, Y., Heiniger, B., Bailly, A., Ahrens, C., Eberl, L., & Pessi, G. (2021). Differential Expression of Paraburkholderia phymatum Type VI Secretion Systems (T6SS) Suggests a Role of T6SS-b in Early Symbiotic Interaction. Frontiers in Plant Science, 12.0. https://doi.org/10.3389/fpls.2021.699590
Huo, H., Wang, X., Liu, Y., Chen, J., & Wei, G. (2021). A Nod factor- And type III secretion system-dependent manner for Robinia pseudoacacia to establish symbiosis with Mesorhizobium amorphae CCNWGS0123. Tree Physiology, 41.0(5). https://doi.org/10.1093/treephys/tpaa160
Kang, M., & Seo, T. (2022). Rhizobium setariae sp. nov., an Indole-3-Acetic Acid-Producing Bacterium Isolated from Green Foxtail, Setaria viridis. Current Microbiology, 79.0(6). https://doi.org/10.1007/s00284-022-02860-2
Kawaharada, Y., Sandal, N., Gupta, V., Jin, H., Kawaharada, M., Taniuchi, M., Ruman, H., Nadzieja, M., Andersen, K., Schneeberger, K., Stougaard, J., & Andersen, S.
(2021). Natural variation identifies a Pxy gene controlling vascular organisation and formation of nodules and lateral roots in Lotus japonicus. New Phytologist, 230.0(6). https://doi.org/10.1111/nph.17356
Kawaka, F. (2022). Characterization of symbiotic and nitrogen fixing bacteria. AMB Express, 12.0(1). https://doi.org/10.1186/s13568-022-01441-7
Khambani, L., Hassen, A., & Rumbold, K. (2023). Characterization of rhizobia for beneficial traits that promote nodulation in legumes under abiotically stressed conditions. Letters in Applied Microbiology, 76.0(9). https://doi.org/10.1093/lambio/ovad106
Kouki, S., L'Taief, B., Al-Qthanin, R., Rouaissi, M., & Sifi, B. (2022). PHENOTYPIC DIVERSITY AND BIOCHEMICAL CHARACTERISTICS OF SELECTED RHIZOBIA NODULATING THE COMMON BEAN (Phaseolus vulgaris L.); Diversidad fenotípica y características bioquímicas de cepas de Rhizobium nodulando el frijol (Phaseolus vulgaris L.). Bioagro, 34.0(1). https://doi.org/10.51372/bioagro341.2
Kuzmanović, N., Fagorzi, C., Mengoni, A., Lassalle, F., & diCenzo, G. (2022). Taxonomy of Rhizobiaceae revisited: proposal of a new framework for genus delimitation. International Journal of Systematic and Evolutionary Microbiology, 72.0(3). https://doi.org/10.1099/ijsem.0.005243
Kuzmanović, N., diCenzo, G., Bunk, B., Sproër, C., Frühling, A., Neumann-Schaal, M., Overmann, J., & Smalla, K. (2023). Genomics of the “tumorigenes” clade of the family Rhizobiaceae and description of Rhizobium rhododendri sp. nov.. MicrobiologyOpen, 12.0(2). https://doi.org/10.1002/mbo3.1352
Lebrazi, S., Fadil, M., Chraibi, M., & Fikri-Benbrahim, K. (2023). Phenotypic, molecular, and symbiotic characterization of the rhizobial symbionts isolated from Acacia saligna grown in different regions in Morocco: a multivariate approach. World Journal of Microbiology and Biotechnology, 39.0(12). https://doi.org/10.1007/s11274-023-03775-1
Li, C., Cao, P., Du, C., Zhang, X., Bing, H., Li, L., Sun, P., Xiang, W., Zhao, J., & Wang, X. (2021). Massilia rhizosphaerae sp. Nov., a rice-associated rhizobacterium with antibacterial activity against ralstonia solanacearum. International Journal of Systematic and Evolutionary Microbiology, 71.0(9). https://doi.org/10.1099/ijsem.0.005009
Li, F., Yu, L., Su, X., Wang, Q., Huang, S., Qin, X., & Tuo, L. (2023). Allorhizobium sonneratiae sp. nov., an endophytic bacterium isolated from the root of Sonneratia apetala. International Journal of Systematic and Evolutionary Microbiology, 73.0(2). https://doi.org/10.1099/ijsem.0.005641
Ma, T., Xue, H., Piao, C., Jiang, N., & Li, Y. (2023). Phylogenomic reappraisal of the family Rhizobiaceae at the genus and species levels, including the description of Ectorhizobium quercum gen. nov., sp. nov.. Frontiers in Microbiology, 14.0. https://doi.org/10.3389/fmicb.2023.1207256
Mahnert, A., Verseux, C., Schwendner, P., Koskinen, K., Kumpitsch, C., Blohs, M., Wink, L., Brunner, D., Goessler, T., Billi, D., & Moissl-Eichinger, C. (2021). Microbiome dynamics during the HI-SEAS IV mission, and implications for future crewed missions beyond Earth. Microbiome, 9.0(1). https://doi.org/10.1186/s40168-020-00959-x
Mansour, S., Elhaloos, B., & Abdel-Lateif, K. (2023). PHENOTYPIC AND GENETIC DIVERSITY OF NATIVE RHIZOBIUM ISOLATED FROM ROOT NODULES OF LEGUMINOUS PLANTS GROWN IN RECLAIMED SOIL, EGYPT. Sabrao Journal of Breeding and Genetics, 55.0(2). https://doi.org/10.54910/sabrao2023.55.2.7
Mavima, L., Beukes, C., Palmer, M., De Meyer, S., James, E., Maluk, M., Gross, E., Dos Reis Júnior, F., Avontuur, J., Chan, W., Venter, S., & Steenkamp, E. (2021).
Paraburkholderia youngii sp. nov. and ‘Paraburkholderia atlantica’ – Brazilian and Mexican Mimosa-associated rhizobia that were previously known as Paraburkholderia tuberum sv. mimosae. Systematic and Applied Microbiology, 44.0(1). https://doi.org/10.1016/j.syapm.2020.126152
Mechan-Llontop, M., Mullet, J., & Shade, A. (2023). Genome-sequenced bacterial collection from sorghum epicuticular wax. Microbiology Resource Announcements, 12.0(12). https://doi.org/10.1128/MRA.00484-23
Mendoza-Suárez, M., Andersen, S. U., Poole, P. S., & Sánchez-Cañizares, C. (2021). Competition, nodule occupancy, and persistence of inoculant strains: key factors in the rhizobium-legume symbioses. Frontiers in Plant Science, 12, 690567.
https://doi.org/10.3389/fpls.2021.690567
Missbah El Idrissi, M., & Abdelmoumen, H. (2021). Diversity of Trigonella foenum graecum Microsymbionts in Morocco. nan, **. https://doi.org/10.1007/978-981-16-1197-1_13
Missbah El Idrissi, M., & Abdelmoumen, H. (2021). Nodulation Process, Nitrogen Fixation, and Diversity of Fenugreek Rhizobia. nan, **. https://doi.org/10.1007/978-981-16-1197-1_12
Mohd-Radzman, N., & Drapek, C. (2023). Compartmentalisation: A strategy for optimising symbiosis and tradeoff management. Plant, Cell and Environment, 46.0(10). https://doi.org/10.1111/pce.14553
Moura, F., Helene, L., Ribeiro, R., Nogueira, M., & Hungría, M. (2023). The outstanding diversity of rhizobia microsymbionts of common bean (Phaseolus vulgaris L.) in Mato Grosso do Sul, central-western Brazil, revealing new Rhizobium species. Archives of Microbiology, 205.0(9). https://doi.org/10.1007/s00203-023-03667-w
Nasrollahi, V., Allam, G., Kohalmi, S., & Hannoufa, A. (2023). MsSPL9 Modulates Nodulation under Nitrate Sufficiency Condition in Medicago sativa. International Journal of Molecular Sciences, 24.0(11). https://doi.org/10.3390/ijms24119615
Nichio, B. T. D. L., Chaves, R. B. R., Pedrosa, F. D. O., & Raittz, R. T. (2025). Exploring diazotrophic diversity: unveiling Nif core distribution and evolutionary patterns in nitrogen-fixing organisms. BMC genomics, 26(1), 81. https://doi.org/10.1186/s12864-024-10994-9
Pang, Z., Chen, J., Wang, T., Gao, C., Li, Z., Guo, L., Xu, J., & Cheng, Y. (2021). Linking Plant Secondary Metabolites and Plant Microbiomes: A Review. Frontiers in Plant Science, 12.0. https://doi.org/10.3389/fpls.2021.621276
Parshuram, Z., Harrison, T., Simonsen, A., Stinchcombe, J., & Frederickson, M. (2023). Nonsymbiotic legumes are more invasive, but only if polyploid. New Phytologist, 237.0(3). https://doi.org/10.1111/nph.18579
Protachevicz, A., Paulitsch, F., Klepa, M., Hainosz, J., Olchanheski, L., Hungría, M., & Batista, J. (2023). Pioneering Desmodium spp. are nodulated by natural populations of stress-tolerant alpha- and beta-rhizobia. Brazilian Journal of Microbiology, 54.0(4). https://doi.org/10.1007/s42770-023-01113-z
Pulido Suarez, L., Flores-Félix, J., Socas-Pérez, N., Igual, J., Velázquez, E., Peix, Á., & León-Barrios, M. (2022). Endophytic Bosea spartocytisi sp. nov. Coexists with rhizobia in root nodules of Spartocytisus supranubius growing in soils of Teide National Park (Canary Islands). Systematic and Applied Microbiology, 45.0(6). https://doi.org/10.1016/j.syapm.2022.126374
Quides, K., Weisberg, A., Trinh, J., Salaheldine, F., Cardenas, P., Lee, H., Jariwala, R., Chang, J., & Sachs, J. (2021). Experimental evolution can enhance benefits of rhizobia to novel legume hosts. Proceedings of the Royal Society B: Biological Sciences, 288.0(1951). https://doi.org/10.1098/rspb.2021.0812
Quilbé, J., Nouwen, N., Pervent, M., Guyonnet, R., Cullimore, J., Gressent, F., Araújo, N., Gully, D., Christophe, C., Giraud, E., & Arrighi, J. (2022). A mutant-based analysis of the establishment of Nod-independent symbiosis in the legume Aeschynomene evenia. Plant Physiology, 190.0(2). https://doi.org/10.1093/plphys/kiac325
Rahi, P., Khairnar, M., Hagir, A., Narayan, A., Jain, K., Madamwar, D., Pansare, A., & Shouche, Y. (2021). Peteryoungia gen. nov. with four new species combinations and description of Peteryoungia desertarenae sp. nov., and taxonomic revision of the genus Ciceribacter based on phylogenomics of Rhizobiaceae. Archives of Microbiology, 203.0(6). https://doi.org/10.1007/s00203-021-02349-9
Rajkumari, J., Katiyar, P., Dheeman, S., Pandey, P., & Maheshwari, D. (2022). The changing paradigm of rhizobial taxonomy and its systematic growth upto postgenomic technologies. World Journal of Microbiology and Biotechnology, 38.0(11). https://doi.org/10.1007/s11274-022-03370-w
Rajnović, I., Ramírez-Bahena, M., Kajić, S., Igual, J., Peix, Á., Velázquez, E., & Sikora, S. (2022). Rhizobium croatiense sp. nov. and Rhizobium redzepovicii sp. nov., two new species isolated from nodules of Phaseolus vulgaris in Croatia. Systematic and Applied Microbiology, 45.0(3). https://doi.org/10.1016/j.syapm.2022.126317
Ratu, S., Hirata, A., Kalaw, C., Yasuda, M., Tabuchi, M., & Okazaki, S. (2021). Multiple Domains in the Rhizobial Type III Effector Bel2-5 Determine Symbiotic Efficiency With Soybean. Frontiers in Plant Science, 12.0. https://doi.org/10.3389/fpls.2021.689064
Rehling, F., Sandner, T., & Matthies, D. (2021). Biomass partitioning in response to intraspecific competition depends on nutrients and species characteristics: A study of 43 plant species. Journal of Ecology, 109.0(5). https://doi.org/10.1111/1365-2745.13635
Rios-Galicia, B., Villagómez-Garfias, C., De-La-Vega-Camarillo, E., Guerra-Camacho, J., Medina-Jaritz, N., Arteaga-Garibay, R., Villa-Tanaca, L., & Hernández-Rodríguez, C. (2021). The Mexican giant maize of Jala landrace harbour plant-growth-promoting rhizospheric and endophytic bacteria. 3 Biotech, 11.0(10). https://doi.org/10.1007/s13205-021-02983-6
Rodríguez-Navarro, D., Lorite, M., Temprano-Vera, F., & Camacho, M. (2022). Selection and characterization of Spanish Trifolium-nodulating rhizobia for pasture inoculation. Systematic and Applied Microbiology, 45.0(2). https://doi.org/10.1016/j.syapm.2021.126290
Rogato, A., Valkov, V., Nadzieja, M., Stougaard, J., & Chiurazzi, M. (2021). The lotus japonicus AFB6 gene is involved in the auxin dependent root developmental program. International Journal of Molecular Sciences, 22.0(16). https://doi.org/10.3390/ijms22168495
Romanenko, L., Otstavnykh, N., Tanaka, N., Kurilenko, V., Svetashev, V., Tekutyeva, L., Mikhaǐlov, V., & Isaeva, M. (2023). Characterization and Genomic Analysis of Fererhizobium litorale gen. nov., sp. nov., Isolated from the Sandy Sediments of the Sea of Japan Seashore. Microorganisms, 11.0(10). https://doi.org/10.3390/microorganisms11102385
Sadiq, M., Rahim, N., Iqbal, M., Alqahtani, M., Tahir, M., Majeed, A., & Ahmed, R. (2023). Rhizobia Inoculation Supplemented with Nitrogen Fertilization Enhances Root Nodulation, Productivity, and Nitrogen Dynamics in Soil and Black Gram (Vigna mungo (L.) Hepper). Land, 12.0(7). https://doi.org/10.3390/land12071434
Santos-Torres, M., Romero-Perdomo, F., Mendoza-Labrador, J., Gutiérrez, A., Vargas Baquero, C., Castro-Rincon, E., Caro-Quintero, A., Uribe-Vélez, D., & Estrada Bonilla, G. (2021). Genomic and phenotypic analysis of rock phosphate-solubilizing rhizobacteria. Rhizosphere, 17.0. https://doi.org/10.1016/j.rhisph.2020.100290
Schumacher, K., Brameyer, S., & Jung, K. (2023). Bacterial acid stress response: from cellular changes to antibiotic tolerance and phenotypic heterogeneity. Current Opinion in Microbiology, 75.0. https://doi.org/10.1016/j.mib.2023.102367
Shen, H., Luo, X., Xia, Z., & Wan, C. (2022). R hizobium alarense sp. nov. and Rhizobium halophilum sp. nov. isolated from the nodule and rhizosphere of Lotus japonicus. Archives of Microbiology, 204.0(11). https://doi.org/10.1007/s00203-022-03202-3
Shen, L., Liu, J., Liu, P., An, M., He, X., & Zhao, G. (2022). A non-symbiotic novel species, Rhizobium populisoli sp. nov., isolated from rhizosphere soil of Populus popularis. Archives of Microbiology, 204.0(1). https://doi.org/10.1007/s00203-021-02706-8
Shin, J., Marx, H., Richards, A., Vaneechoutte, D., Jayaraman, D., Maeda, J., Chakraborty, S., Sussman, M., Vandepoele, K., Ané, J., Coon, J., & Roy, S. (2021). A network-based comparative framework to study conservation and divergence of proteomes in plant phylogenies. Nucleic Acids Research, 49.0(1). https://doi.org/10.1093/nar/gkaa1041
Silva, U., Cuadros-Orellana, S., Silva, D., Freitas-Júnior, L., Fernandes, A., Leite, L., de Oliveira-Paiva, C., & Dos Santos, V. (2021). Genomic and Phenotypic Insights Into the Potential of Rock Phosphate Solubilizing Bacteria to Promote Millet Growth in vivo. Frontiers in Microbiology, 11.0. https://doi.org/10.3389/fmicb.2020.574550
Sofla, A., Taheri, H., Ghodoum Parizipour, M., & Soleymani, F. (2023). Molecular and Phenotypic Responses of Rhizobacteria-Treated Tomato Plants to Tomato Mosaic Virus Under Greenhouse Conditions. Iranian Journal of Biotechnology, 21.0(1). https://doi.org/10.30498/ijb.2022.319382.3220
Sondo, M., Wonni, I., Koïta, K., Rimbault, I., Barro, M., Tollenaere, C., Moulin, L., & Klonowska, A. (2023). Diversity and plant growth promoting ability of rice root-associated bacteria in Burkina-Faso and cross-comparison with metabarcoding data. PLOS ONE, 18.0(11 November). https://doi.org/10.1371/journal.pone.0287084
Stella, M., Sharma, R., Nema, S., Ramakrishnan, R., & Kumar, A. (2021). Genetic characterization and diversity of Rhizobia isolated from root nodules of green gram (Vigna radiata L.) found in central plateau of India. Legume Research, 44.0(3). https://doi.org/10.18805/LR-4258
Su, L., Liu, S., Liu, X., Zhang, B., Li, M., Zeng, L., & Li, L. (2021). Transcriptome profiling reveals histone deacetylase 1 gene overexpression improves flavonoid, isoflavonoid, and phenylpropanoid metabolism in Arachis hypogaea hairy roots. PeerJ, 9.0. https://doi.org/10.7717/peerj.10976
Su, X., Liu, G., Zhang, L., Zhou, X., Qiao, W., & Jiang, J. (2021). Rhizobium flavescens sp. nov., Isolated from a Chlorothalonil-Contaminated Soil. Current Microbiology, 78.0(5). https://doi.org/10.1007/s00284-021-02462-4
Suproniene, S., Decorosi, F., Pini, F., Bellabarba, A., Calamai, L., Giovannetti, L., Bussotti, F., Kadžiulienė, Z., Razbadauskienė, K., Toleikienė, M., & Viti, C. (2021). Selection of Rhizobium strains for inoculation of Lithuanian Pisum sativum breeding lines. Symbiosis, 83.0(2). https://doi.org/10.1007/s13199-021-00747-7
Taha, K., El Attar, I., Hnini, M., Raif, A., Béna, G., Aurag, J., & Berraho, E. (2022). Beneficial effect of Rhizobium laguerreae co-inoculated with native Bacillus sp. and Enterobacter aerogenes on lentil growth under drought stress. Rhizosphere, 22.0. https://doi.org/10.1016/j.rhisph.2022.100523
Tesfaye, D., Mendesil, E., & Keneni, G. (2023). Response of field pea genotypes to the infestation of Adzuki bean beetle (Callosobruchus chinensis L.) under different soil fertility regimes and locations in Ethiopia. International Journal of Tropical Insect Science, 43.0(1). https://doi.org/10.1007/s42690-022-00928-x
Tu, T., Lin, S., & Shen, F. (2021). Enhancing symbiotic nitrogen fixation and soybean growth through co-inoculation with bradyrhizobium and pseudomonas isolates. Sustainability (Switzerland), 13.0(20). https://doi.org/10.3390/su132011539
Venado, R., Wange, L., Shen, D., Pinnau, F., Andersen, T., Enard, W., & García-Marín, M. (2022). Tissue-specific regulation of lipid polyester synthesis genes controlling oxygen permeation into Lotus japonicus nodules. Proceedings of the National Academy of Sciences of the United States of America, 119.0(47).
https://doi.org/10.1073/pnas.2206291119
Wang, C., Bian, D., Jiang, N., Xue, H., Piao, C., & Li, Y. (2022). Rhizobium quercicola sp. nov., isolated from the leaf of Quercus variablis in China. Archives of Microbiology, 204.0(9). https://doi.org/10.1007/s00203-022-03188-y
Wang, P., Wei, H., Ke, T., Fu, Y., Zeng, Y., Chen, C., & Chen, L. (2023). Characterization and genome analysis of Acinetobacter oleivorans S4 as an efficient hydrocarbon-degrading and plant-growth-promoting rhizobacterium. Chemosphere, 331.0. https://doi.org/10.1016/j.chemosphere.2023.138732
Youseif, S., Abd El-Megeed, F., Mohamed, A., Ageez, A., Veliz, E., & Martinez-Romero, E. (2021). Diverse Rhizobium strains isolated from root nodules of Trifolium alexandrinum in Egypt and symbiovars. Systematic and Applied Microbiology, 44.0(1). https://doi.org/10.1016/j.syapm.2020.126156
Zaw, M., Rathjen, J., Zhou, Y., Ryder, M., & Denton, M. (2021). Symbiotic effectiveness, ecological adaptation and phylogenetic diversity of chickpea rhizobia isolated from a large-scale Australian soil collection. Plant and Soil, 469.0(1-2). https://doi.org/10.1007/s11104-021-05119-0
Zhang, J., Wang, N., Li, S., Peng, S., Andrews, M., Zhang, X., Zhang, Y., Yu, H., Song, J., Chen, W., Wang, E., & Li, Y. (2023). Bradyrhizobium zhengyangense sp. nov., isype strains of the most closely related species ofolated from effective nodules of Arachis hypogaea L. in central China. International Journal of Systematic and Evolutionary Microbiology, 73.0(3). https://doi.org/10.1099/ijsem.0.005723
Zhao, W., Zhu, H., Wei, F., Zhou, D., Li, Y., & Zhang, X. (2021). Investigating the involvement of cytoskeletal proteins MreB and FtsZ in the origin of legume-rhizobial symbiosis. Molecular Plant-Microbe Interactions, 34.0(5).
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