María de Lourdes Girard Cuesy

Systems Biology and Synthetic Biology Laboratory Researcher

Associate Professor

Academic history

B.A. in Biology at the Universidad Autónoma Metropolitana-Iztapalapa, México.
M.S. and Ph.D in Basic Biomedical Research at the Universidad Nacional Autónoma de México (UNAM), México.
Professor (researcher) at the Centro de Ciencias Genómicas (CCG) UNAM for 20 years.

She performs research within the field of Molecular Genetics in bacteria, focusing primarily on nitrogen-fixing bacteria known as Rhizobia, that establish symbiosis with legume plants. She contributed to the establishment of the physical map of the symbiotic plasmid of Rhizobium etli CFN42 and to the analysis of its transcriptional activity. These were pioneer works in the rhizobiology area that lead to the structural and functional characterization of a complete replicon before the genomics era. Her main contributions are within the transcriptional regulation and the analysis of the functional networks that are essential to control biological nitrogen fixation in response of environmental stimuli such as oxygen and abiotic stresses. Her research combines genetics, molecular biology and genomic approaches; she has elucidated complex regulatory networks and their components, mainly from R. etli (the bean symbiont), thus contributing to understand what makes this bacteria different and particular from other bacteria of its kind. Recently, she expanded her interests to the global study of transcriptional expression, both bacterial and plant, using R. etli strains that confer advantages to the Rhizobium-bean symbiosis.
Dra. Girard’s research group maintain successful academic collaborations with the majority of CCG’s research groups and with other groups from Mexico and abroad. Her work has been supported by different national research grants (DGAPA-PAPIIT and CONACYT) as well as academic exchange agreements with foreign countries. She has directed the thesis research work of undergraduate and graduate students, as well as advised research projects of international Postdoctoral fellows.
She is Review Editor of the journal Frontiers in Microbiology- Frontiers in Microbial Symbioses.



Telephone: (777) 3291686


2016Peralta H, Aguilar A, Díaz R, Mora Y, Martínez-Batallar G, Salazar E, Vargas-Lagunas C, 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
2016Reyes-Gonzalez, Alma, 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
2015Hernandez, Victor M., Girard, L., Hernandez-Lucas, Ismael, Vazquez, Alejandra, Ortiz-Ortiz, Catalina, Diaz, Rafael and Dunn, M.F.. (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, Diaz, Rafael, Vargas-Lagunas, Carmen, Peralta, Humberto, Guerrero, Gabriela, Aguilar, Alejandro, Encarnacion, Sergio, 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 Membreño, Sara Isabel, Iñiguez Rabago, Luis Pedro, Aparicio Fabre, Rosaura, Zamorano-Sánchez, D., Encarnación Guevara, Sergio Manuel, 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, Alma Ruth, 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, Alma Ruth, 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, Rafael, Vargas Lagunas, María del Carmen, Villalobos López, Miguel Angel, Peralta Díaz, Humberto, Pérez-Tejada Domínguez, Yolanda, Encarnación Guevara, Sergio Manuel, 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 Lagunas, María del Carmen, Villalobos, M.A., Díaz Mendez, Rafael, Flores, M.A., Contreras Martínez, Sandra, Encarnación Guevara, Sergio Manuel, Pérez-Tejada Domínguez, Yolanda, Dunn, M.F., 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, Delfino, Bustos Arcos, Virginia Patricia, 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 Lagunas, María del Carmen, Encarnación Guevara, Sergio Manuel, 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 Arcos, Virginia Patricia, 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, M. del C., Encarnacin, 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 Arcos, Virginia Patricia, Ramírez Romero, Miguel Ángel, Medrano Soto, Luis Arturo, Salgado Osorio, Heladia, Hernández González, Ismael Luis, Hernández Celis, Juan Carlos, Quintero Hernández, Verónica, Moreno Hagelsieb, Gabriel, Girard, L., Rodríguez Sánchez, Oscar, Flores López, Margarita, Cevallos, M.A., 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 Rodríguez, Araceli Elvira, 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., Rodriguez, O, Cevallos, M.A. 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, Davalos, 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, M.A., 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
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
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
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
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
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
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
2011Cervantes de la Luz, Laura, Bustos Arcos, Virginia Patricia, Girard, L., Santamaria Gutiérrez, Rosa Isela, 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
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
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]
2016Aguilar A, Peralta H, Mora Y, Díaz R, Vargas-Lagunas C, 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
2017Vargas-Lagunas, Carmen, Mora, Yolanda, Diaz, Rafael, Martinez-Batallar, Gabriel, Girard, L., Encarnacion, Sergio, Peralta, Humberto 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
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
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