Systems Biology and Synthetic Biology Laboratory

We are a multidisciplinary program that includes 8 researchers who routinely use a large number of approaches and experimental models. One of our main interests is to combine systems and synthetic biology using genome-scale models to design bacterial phenotypes of biotechnological interest (Dr. José Utrilla). In addition, we are also interested in using a theoretical-experimental approach to study the genetic and metabolic mechanisms that allow bacterial populations to find collective strategies to survive in hostile and unpredictable environments, such as antimicrobial substances (Dr. Rafael Peña). On the same vein, we also seek to understand the effects of spatial structure on the temporal dynamics of the evolution of bacterial resistance to different combinations of antibiotics (Dr. Ayari Fuentes). We build a variety of evolutionary models to analyze specific genomic regions, such as the sex chromosomes, which are one of the most dynamic elements in the genomes of vertebrates. (Dr. Diego Cortez). Furthermore, using bacterial nitrogen fixation as an experimental model, we study the regulation of gene expression in response to various environmental stimuli and the mechanisms directing these responses (Dr. María de Lourdes Girard). We also study signal transduction and gene regulation in the genus Vibrio (Dr. David Zamorano). Additionally, we analyze the metagenomics of the skin of amphibians and their interaction with pathogenic fungi (Dr. Eria Rebollar). Finally, we study the system-level principles governing the organization and evolution of large-scale biological circuitry (Dr. Julio Freyre).

Group Staff

María de Lourdes Girard CuesyResearcherAssociate 3291686
Diego Cortez QuezadaResearcherAssociate 3291686
Ayari Fuentes HernándezResearcherAssistant 3291686
Marisa Rodríguez PadillaLaboratory TechnicianLaboratory 3291686
José Utrilla CarreriResearcherAssistant 3291686
Eria Rebollar CaudilloResearcherAssistant 5622 7777
David Salvador Zamorano SánchezResearcherAssistant 329 1777
María de la Paz Elizabeth Salas OcampoLaboratory TechnicianLaboratory 3291686
Rafael Peña MillerResearcherAssociate 3291686
David Correa GaleotePostdoctoral 3175867
Mónica Leticia Martínez PachecoPostdoctoral 3291686
Julio Augusto Freyre GonzálezResearcherAssistant 3133881

Group Publications

2018Rodriguez-Beltran, J., Hernandez-Beltran, J.C.R., Delafuente, J., Escudero, J.A., Fuentes-Hernández, A, MacLean, R.C., Peña-Miller, F and San Millan, A.. (2018). "Multicopy plasmids allow bacteria to escape from fitness trade-offs during evolutionary innovation". Nature Ecology & Evolution. 2(5):873-881. [doi:10.1038/s41559-018-0529-z]29632354
2017Moreno-Avitia, F., Lozano, L, Utrilla, J, Bolívar, F. and Escalante, A.. (2017). "Draft genome sequence of pseudomonas chlororaphis ATCC 9446, a nonpathogenic bacterium with bioremediation and industrial potential". Genome Announcements. 5(23):e00474-17-. [doi:10.1128/genomeA.00474-17]28596401
2016Peralta, H, Aguilar, A, Díaz-Mendez, R, Mora Y, Martínez-Batallar, AG, Salazar E, Vargas, MC, Martínez-Romero, E, Encarnación, S, Girard, L and Mora, J. (2016). "Genomic studies of nitrogen-fixing rhizobial strains from Phaseolus vulgaris seeds and nodules". Bmc Genomics. 17(1):1-1. [doi:10.1186/s12864-016-3053-z]27601031
2016Utrilla, J, Vargas-Tah, Alejandra, Trujillo-Martinez, Berenice, Gosset, Guillermo and Martinez, Alfredo. (2016). "Production of D-lactate from sugarcane bagasse and corn stover hydrolysates using metabolic engineered Escherichia coli strains". BIORESOURCE TECHNOLOGY. 220():208-214. [doi:10.1016/j.biortech.2016.08.067]27573474
2016Reyes-González, A, Talbi, Chouhra, Rodriguez, Susana, Rivera, Patricia, Zamorano-Sanchez, David and Girard, L. (2016). "Expanding the regulatory network that controls nitrogen fixation in Sinorhizobium meliloti: elucidating the role of the two-component system hFixL-FxkR". MICROBIOLOGY-SGM. 162(6):979-988. [doi:10.1099/mic.0.000284]27010660
2016O'Brien EJ, Utrilla, J and Palsson BO. (2016). "Quantification and Classification of E. coli Proteome Utilization and Unused Protein Costs across Environments". Plos Computational Biology. 12(6):e1004998-. [doi:10.1371/journal.pcbi.1004998]27351952
2015Hernandez, Victor M., Girard, L, Hernandez-Lucas, Ismael, Vazquez, Alejandra, Ortiz-Ortiz, Catalina, Díaz-Mendez, R and Dunn, MF. (2015). "Genetic and biochemical characterization of arginine biosynthesis in Sinorhizobium meliloti 1021". MICROBIOLOGY-SGM. 161(8):1671-1682. [doi:10.1099/mic.0.000122]26271664
2015Nova-Franco B, Íñiguez LP, Valdés-López O, Alvarado-Affantranger X, Leija, A, Fuentes, SI, Ramírez, M, Paul S, Reyes JL, Girard, L and Hernández, G. (2015). "The Micro-RNA172c-APETALA2-1 Node as a Key Regulator of the Common Bean-Rhizobium etli Nitrogen Fixation Symbiosis". Plant Physiology. 168(1):273-502. [doi:10.1104/pp.114.255547]25739700
2014Mora, Yolanda, Díaz-Mendez, R, Vargas, MC, Peralta, H, Guerrero, G, Aguilar, A, Encarnación, S, Girard, L and Mora, J. (2014). "Nitrogen-fixing rhizobial strains isolated from common bean seeds: Phylogeny, physiology, and genome analysis". Applied And Environmental Microbiology. 80(18):5644-5654. [doi:10.1128/AEM.01491-14]25002426
2014Garcia-Garcia, J.D., Girard, L, Hernández, G, Saavedra, E., Pardo, J.P., Rodríguez-Zavala, J.S., Encalada, R., Reyes-Prieto, A., Mendoza-Cozatl, D.G. and Moreno-Sánchez, R.. (2014). "Zn-bis-glutathionate is the best co-substrate of the monomeric phytochelatin synthase from the photosynthetic heavy metal-hyperaccumulator Euglena Gracilis". Metallomics. 6(3):604-616. [doi:10.1039/c3mt00313b]24464102
2013Ramírez, M, Guillén, G., Fuentes, SI, Iñiguez Rabago, Luis Pedro, Aparicio Fabre, Rosaura, Zamorano-Sánchez, D, Encarnación, S, Panzeri, D., Castiglioni, B., Cremonesi, P., Strozzi, F., Stella, A., Girard, L, Sparvoli, F. and Hernández, G. (2013). "Transcript profiling of common bean nodules subjected to oxidative stress". Physiologia Plantarum. 149(3):389-407. [doi:10.1111/ppl.12040]23432573
2013Reyes-González, A, Zamorano-Sánchez, D, Rivera Rosas, Patricia and Girard, L. (2013). "hFixL-FxkR are the key regulators for fixKf-related gene expression". Mexican Journal of Scientific Research. ():-.
2013Ramírez, M, Flores-Pacheco, G., Reyes, J.L., Álvarez, A.L., Drevon, J.J., Girard, L and Hernández, G. (2013). "Two Common Bean Genotypes with Contrasting Response to Phosphorus Deficiency Show Variations in the microRNA 399-Mediated PvPHO2 Regulation within the PvPHR1 Signaling Pathway". International Journal Of Molecular Sciences. 14(4):8328-8344. [doi:10.3390/ijms14048328]23591845
2012Zamorano-Sánchez, D, Reyes-González, A, Gómez Hernández, Nicolás, Rivera, P., Georgellis, D. and Girard, L. (2012). "FxkR Provides the Missing Link in the fixL-fixK Signal Transduction Cascade in Rhizobium etli CFN42". Molecular Plant-Microbe Interactions. 25(11):1506-1517. [doi:10.1094/MPMI-05-12-0136-R]22809273
2012García-García, J.D., Olin-Sandoval, V., Saavedra, E., Girard, L, Hernández, G and Moreno-Sánchez, R.. (2012). "Sulfate uptake in photosynthetic Euglena Gracilis. Mechanisms of regulation and contribution to cysteine homeostasis". Biochimica Et Biophysica Acta-General Subjects. 1820(10):1567-1575. [doi:10.1016/j.bbagen.2012.05.002]22609877
2012Talbi, C., Sánchez, C., Hidalgo-García, A., González, E.M., Arrese-Igor, C., Girard, L, Bedmar, E.J. and Delgado, M.J.. (2012). "Enhanced expression of Rhizobium etli cbb(3) oxidase improves drought tolerance of common bean symbiotic nitrogen fixation". Journal Of Experimental Botany. 63(14):5035-5043. [doi:10.1093/jxb/ers101]22511804
2011Gómez Hernández, Nicolás, Reyes-González, A, Sanchez, C., Pérez-Tejada Domínguez, Yolanda, Delgado, M.J. and Girard, L. (2011). "Regulation and Symbiotic Role of nirK and norC Expression in Rhizobium etli". Molecular Plant-Microbe Interactions. 24(2):233-245. [doi:10.1094/MPMI-07-10-0173]21043576
2011Díaz-Mendez, R, Vargas, MC, Villalobos López, Miguel Angel, Peralta, H, Pérez-Tejada Domínguez, Yolanda, Encarnación, S, Girard, L and Mora, J. (2011). "argC orthologs from Rhizobiales show diverse profiles of transcriptional efficiency and functionality in Sinorhizobium meliloti". Journal Of Bacteriology. 193(2):460-472. [doi:10.1128/JB.01010-10]21075924
2010Talbi, C., Delgado, M. J., Girard, L, Ramirez-Trujillo, A., Caballero-Mellado, J. and Bedmar, E. J.. (2010). "Burkholderia Phymatum Strains Capable of Nodulating Phaseolus vulgaris Are Present in Moroccan Soils". Applied And Environmental Microbiology. 76(13):4587-4591. [doi:10.1128/AEM.02886-09]20472732
2010Sanchez, Cristina, Gates, Andrew J., Meakin, Georgina E., Uchiumi, Toshiki, Girard, L, Richardson, David J., Bedmar, Eulogio J. and Delgado, Maria J.. (2010). "Production of Nitric Oxide and Nitrosylleghemoglobin Complexes in Soybean Nodules in Response to Flooding". Molecular Plant-Microbe Interactions. 23(5):702-711. [doi:10.1094/MPMI-23-5-0702]20367476
2010Talbi, C., Sánchez, C., Girard, L, Bedmar, E. and Delgado, M.J.. (2010). "La sobreexpresión de la oxidasa cbb3 de Rhizobium etli incrementa la tolerancia de Phaseolus vulgaris a la sequía". Avances en el metabolismo del Nitrógeno. ():223-228.
2008Valdes-Lopez, Oswaldo, Arenas-Huertero, Catalina, Ramírez, M, Girard, L, Sanchez, Federico, Vance, Carroll P., Reyes, Jose Luis and Hernández, G. (2008). "Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots". Plant Cell And Environment. 31(12):1834-1843. [doi:10.1111/j.1365-3040.2008.01883.x]18771575
2008Vargas, MC, Villalobos, M.A., Díaz-Mendez, R, Flores, M.A., Contreras-Martínez, S, Encarnación, S, Pérez-Tejada Domínguez, Yolanda, Dunn, MF, Girard, L and Mora, J. (2008). "Comparative Analysis of argC protein expression in Rhizobium species". Current Plant Science and Biotechnology. Agriculture Biological Nitrogen Fixation, Sustainable Agriculture and the Environment. 42(0):239-240.
2007Flores López, Margarita, Morales Reyes, Lucía Guadalupe, Gonzaga Jáuregui, Claudia Gabriela, Domínguez Vidaña, Rocío, Zepeda Mendoza, Cinthya Jeanette, Yáñez Cuna, Jorge Omar, Gutiérrez Arcelus, María, Lemus Vergara, Tzitziki Janik, Valle García, David, Ávila Arcos, María del Carmen, Blanco Melo, Daniel, Medina Ruiz, Sofía, Meza Sosa, Karla Fabiola, Ayala Ortega, Erandi, García-Alonso, D, Bustos, P, González, V, Girard, L, Tusie-Luna, T., Dávila Ramos, José Guillermo and Palacios de la Lama, Rafael. (2007). "Recurrent DNA inversion rearrangements in the human genome". PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 104(15):6099-6106. [doi:10.1073/pnas.0701631104]17389356
2007Granados Baeza, Manuel Jesús, Gómez Hernández, Nicolás, Mora, Yolanda, Delgado, M.J., Romero, D and Girard, L. (2007). "Novel reiterated Fnr-type proteins control the production of the symbiotic terminal oxidase cbb3 in Rhizobium etli CFN42". Molecular Plant-Microbe Interactions. 20(10):1241-1249. [doi:10.1094/MPMI-20-10-1241]17918626
2005Bueno, E., Gomez-Hernandez, Nicolas, Girard, L, Bedmar, E.J. and Delgado, M.J.. (2005). "Function of the Rhizobium etli CFN42 nirK gene in nitrite metabolism". BIOCHEMICAL SOCIETY TRANSACTIONS. 33(1):162-163. [doi:10.1042/BST0330162]15667294
2005Vargas, MC, Encarnación, S, Girard, L, Reyes Pérez, Agustín, Pérez-Tejada Domínguez, Yolanda and Mora, J. (2005). "Characterization of the alternative protection programs against oxidative-stress in free life and simbiosis from Rhizobium etli". Current Plant Science and Biotechnology. Agriculture Biological Nitrogen Fixation, Sustainable Agriculture and the Environment. 41():331-.
2004Brom, S, Girard, L, Tun Garrido, Cristina Soleda, García-de los Santos, A, Bustos, P, González, V and Romero, D. (2004). "Transfer of the symbiotic plasmid of Rhizobium etli CFN42 requires cointegration with p42a, which may be mediated by site-specific recombination". Journal Of Bacteriology. 186(22):7538-7548. [doi:10.1128/JB.186.22.7538-7548.2004]15516565
2004Vargas, MC, Encarnación, S, Girard, L, Reyes, A., Mora, Y. and Mora, J. (2004). "Physiological and proteome characterizations of oxidative-stress response in Rhizobium etli during free life and symbiosis with Phaseolus vulgaris.". MOLECULAR & CELLULAR PROTEOMICS. 3(10, S):160-160.
2003González, V, Bustos, P, Ramírez Romero, Miguel Ángel, Medrano Soto, Luis Arturo, Salgado, H, Hernández González, Ismael Luis, Hernández Celis, Juan Carlos, Quintero Hernández, Verónica, Moreno Hagelsieb, Gabriel, Girard, L, Rodríguez, O, Flores López, Margarita, Cevallos, MA, Collado-Vides, J, Romero, D and Dávila Ramos, José Guillermo. (2003). "The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments.". Genome Biology. 4(6):R36-. [doi:10.1186/gb-2003-4-6-r36]12801410
2000Girard, L, Brom, S, Dávalos, A, López, O., Soberón Chávez, Mario and Romero, D. (2000). "Differential regulation of fixN-reiterated genes in Rhizobium etli by a novel fixL-fixK cascade". Molecular Plant-Microbe Interactions. 13(12):1283-1292. [doi:10.1094/MPMI.2000.13.12.1283]11106020
1999Soberon, M, Lopez, O, Morera, C, Girard, L, Tabche, ML and Miranda, J. (1999). "Enhanced nitrogen fixation in a Rhizobium etli ntrC mutant that overproduces the Bradyrhizobium japonicum symbiotic terminal oxidase cbb(3)". Applied And Environmental Microbiology. 65(5):2015-2019. 10223993
1997RamirezRomero, MA, Bustos, P, Girard, L, Rodríguez, O, Cevallos, MA and Davila, G. (1997). "Sequence, localization and characteristics of the replicator region of the symbiotic plasmid of Rhizobium etli". MICROBIOLOGY-SGM. 143(8):2825-2831. [doi:10.1099/00221287-143-8-2825]9274036
1996Girard, L, Valderrama, B, Palacios, R, Romero, D and Davila, G. (1996). "Transcriptional activity of the symbiotic plasmid of Rhizobium etli is affected by different environmental conditions". MICROBIOLOGY-SGM. 142(10):2847-2856. [doi:10.1099/13500872-142-10-2847]
1996Valderrama, B, Dávalos, A, Girard, L, Morett, E and Mora, J. (1996). "Regulatory proteins and CIS-acting elements involved in the transcriptional control of Rhizobium etli reiterated nifH genes". Journal Of Bacteriology. 178(11):3119-3126. [doi:10.1128/jb.178.11.3119-3126.1996]8655489
1995Romero, D, MARTINEZSALAZAR, J, Girard, L, Brom, S, DAVILA, G, PALACIOS, R, FLORES, M and RODRIGUEZ, C. (1995). "Discrete amplifiable regions (amplicons) in the symbiotic plasmid of Rhizobium etli CFN42". Journal Of Bacteriology. 177(4):973-980. [doi:10.1128/jb.177.4.973-980.1995]7860608
1993Flores López, Margarita, Brom, S, Stepkowsky, Tomász, Girard, L, Dávila Ramos, José Guillermo, Romero, D and Palacios de la Lama, Rafael. (1993). "Gene amplification in Rhizobium: Identification and in vivo cloning of discrete amplifiable DNA regions (amplicons) from Rhizobium leguminosarum biovar phaseoli". PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 90(11):4932-4936. [doi:10.1073/pnas.90.11.4932]8506337
1991MARTINEZSALAZAR, JM, Romero, D, Girard, L and DAVILA, G. (1991). "Molecular cloning and characterization of the recA gene of Rhizobium phaseoli and construction of recA mutants". Journal Of Bacteriology. 173(10):3035-3040. [doi:10.1128/jb.173.10.3035-3040.1991]2022610
1991Romero, D, Brom, S, MARTINEZSALAZAR, J, Girard, L, PALACIOS, R and DAVILA, G. (1991). "Amplification and deletion of a nod-nif region in the symbiotic plasmid of Rhizobium phaseoli". Journal Of Bacteriology. 173(8):2435-2441. [doi:10.1128/jb.173.8.2435-2441.1991]2013567
1991Brom, S, García-de los Santos, A, Girard, L, DAVILA, G, PALACIOS, R and Romero, D. (1991). "High-frequency rearrangements in Rhizobium leguminosarum bv. phaseoli plasmids". Journal Of Bacteriology. 173(3):1344-1346. [doi:10.1128/jb.173.3.1344-1346.1991]1991727
1985Quinto, Carmen, de la Vega, Humberto, Flores López, Margarita, Leemans, J., Cevallos, MA, Pardo Galván, Marco Aurelio, Azpiroz, Ricardo, Girard, L, Calva Mercado, Edmundo and Palacios de la Lama, Rafael. (1985). "NITROGENASE REDUCTASE - A FUNCTIONAL MULTIGENE FAMILY IN Rhizobium-phaseoli". PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 82(4):1170-1174. [doi:10.1073/pnas.82.4.1170]16593543
2009Onofre-Lemus, Janette, Hernandez-Lucas, Ismael, Girard, L and Caballero-Mellado, Jesus. (2009). "ACC (1-Aminocyclopropane-1-Carboxylate) Deaminase Activity, a Widespread Trait in Burkholderia Species, and Its Growth-Promoting Effect on Tomato Plants". Applied And Environmental Microbiology. 75(20):6581-6590. [doi:10.1128/AEM.01240-09]19700546
2016Aguilar, A, Peralta, H, Mora Y, Díaz-Mendez, R, Vargas, MC, Girard, L and Mora, J. (2016). "Genomic comparison of Agrobacterium Pusense strains isolated from bean nodules". Frontiers in Microbiology. 7(OCT):1720-1720. [doi:10.3389/fmicb.2016.01720]27833604
2018Latif, H., Federowicz, S., Ebrahim, A., Tarasova, J., Szubin, R., Utrilla, J, Zengler, K. and Palsson, B.O.. (2018). "ChIP-exo interrogation of Crp, DNA, and RNAP holoenzyme interactions". Plos One. 13(5):e0197272-. [doi:10.1371/journal.pone.0197272]29771928
2018Chiozzotto, Remo, Ramírez, M, Talbi, Chouhra, Cominelli, Eleonora, Girard, L, Sparvoli, Francesca and Hernández, G. (2018). "Characterization of the symbiotic nitrogen-fixing common bean Low phytic acid (Lpa1) mutant response to water stress". Genes. 9(2):99-. [doi:10.3390/genes9020099]29462877
2017Vargas, MC, Mora, Yolanda, Díaz-Mendez, R, Martínez-Batallar, AG, Girard, L, Encarnación, S, Peralta, H and Mora, J. (2017). "Overproduction of Sinorhizobium meliloti argC (N-acetyl-gamma-glutamyl phosphate reductase) promotes growth delay and inefficient nodules". Fems Microbiology Letters. 364(23):fnx233-. [doi:10.1093/femsle/fnx233]29121239
1991Girard, L, FLORES, M, Brom, S, Romero, D, PALACIOS, R and DAVILA, G. (1991). "Structural complexity of the symbiotic plasmid of Rhizobium leguminosarum bv. phaseoli". Journal Of Bacteriology. 173(8):2411-2419. [doi:10.1128/jb.173.8.2411-2419.1991]2013564
2017Steffani-Vallejo, J.L., Zuñiga, C., Cruz-Morales, P., Lozano, L, Morales, M., Licona-Cassani, C., Revah, S. and Utrilla, J. (2017). "Draft genome sequence of Sphingobacterium sp. CZ-UAM, isolated from a methanotrophic consortium". Genome Announcements. 5(33):e00792-17-. [doi:10.1128/genomeA.00792-17]28818899
2017Utrilla, J. (2017). "Evolutionary Engineering of Microorganisms to Overcome Toxicity During Lignocellulose Hydrolysates Utilization". Engineering of Microorganisms for the Production of Chemicals and Biofuels from Renewable Resources. ():181-200. [doi:]
2016Utrilla, J, O'Brien, E.J., Chen, K., McCloskey, D., Cheung, J., Wang, H., Armenta-Medina, D., Feist, A.M. and Palsson, B.O.. (2016). "Global Rebalancing of Cellular Resources by Pleiotropic Point Mutations Illustrates a Multi-scale Mechanism of Adaptive Evolution". Cell systems. 2(4):260-271. [doi:10.1016/j.cels.2016.04.003]27135538
2018Aguilar, A, Mora Y, Dávalos, A, Girard, L, Mora, J and Peralta, H. (2018). "Analysis of genome sequence and symbiotic ability of rhizobial strains isolated from seeds of common bean (Phaseolus vulgaris).". Bmc Genomics. 19(1):645-645. [doi:10.1186/s12864-018-5023-0]30165827
2015Girard, L and Zamorano-Sánchez, D. (2015). "Fnr - like proteins in Rhizobia: past and future". Biological Nitrogen Fixation. 1():155-166. [doi:10.1002/9781119053095]
1998Flores, M, Mavingui, P, Girard, L, Perret, X, Broughton, WJ, Martínez-Romero, E, Davila, G and Palacios, R. (1998). "Three replicons of Rhizobium sp. strain NGR234 harbor symbiotic gene sequences". Journal Of Bacteriology. 180(22):6052-6053. 9811668
2013Aparicio Fabre, Rosaura, Guillén, G., Loredo, M., Arellano García, José de Jesús, Valdes López, Oswaldo, Ramírez, M, Iñiguez Rabago, Luis Pedro, Panzeri, D., Castiglioni, B., Cremonesi, P., Strozzi, F., Stella, A., Girard, L, Sparvoli, F. and Hernández, G. (2013). "Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency". Bmc Plant Biology. 13():26-26. [doi:10.1186/1471-2229-13-26]23402340
2000Reyes, J.D., Tabche, M.L., Morera, C., Girard, L, Romero, D, Krol, E., Miranda, J. and Soberón Chávez, Mario. (2000). "Expression pattern of Rhizobium etli ccmIEFH genes involved in c-type cytochrome maturation". Gene. 250(1-2):149-157. [doi:10.1016/S0378-1119(00)00176-1]10854788
2011Cervantes, L, Bustos, P, Girard, L, Santamaria, RI, Dávila Ramos, José Guillermo, Vinuesa, P, Romero, D and 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 a Sinorhizobium strain". Bmc Microbiology. 11(1):1-11. [doi:10.1186/1471-2180-11-149]21702991
2001López, O., Morera, C., Miranda-Ríos, J., Girard, L, Romero, D and Soberón Chávez, Mario. (2001). "Regulation of gene expression in response to oxygen in Rhizobium etli: Role of FnrN in fixNOQP expression and in symbiotic nitrogen fixation". Journal Of Bacteriology. 183(24):6999-7006. [doi:10.1128/JB.183.24.6999-7006.2001]11717256
2002Brom, S, Girard, L, García-de los Santos, A, Sanjuan-Pinilla, J.M., Olivares, J. and Sanjuan, J.. (2002). "Conservation of plasmid-encoded traits among bean-nodulating Rhizobium species". Applied And Environmental Microbiology. 68(5):2555-2561. [doi:10.1128/AEM.68.5.2555-2561.2002]11976134
2018Isidra-Arellano, M.C., Reyero-Saavedra, M.D.R., Sánchez-Correa, M.D.S., Pingault, L., Sen, S., Joshi, T., Girard, L, Castro-Guerrero, N.A., Mendoza-Cozatl, D.G., Libault, M. and Valdés-López, O.. (2018). "Phosphate deficiency negatively affects early steps of the symbiosis between common bean and Rhizobia". Genes. 9(10):498-. [doi:10.3390/genes9100498]30326664