Nitrogen Fixation by the Legume-Rhizobia Symbiosis
Manuel Becana Ausejo (PI)
Professor CSIC
Department of Plant Nutrition, Estación Experimental de Aula Dei, CSIC, Zaragoza, Spain
Other group members
Research lines
- Legume-rhizobia symbiosis
- Plant hemoglobins
- Free radicals, antioxidants and nitro-oxidative stress
Representative publications
- Wang L, Tian T, Deng Y, Ji J, Liang J, Guan Y,1 Li R, Huang X, Wang Y, Ning G, Fan Q, Becana M, Duanmu (2025) Plant glutamyl-tRNA reductases coordinate plant and rhizobial heme biosynthesis in nitrogen-fixing nodules. Plant Cell (doi.org/10.1093/plcell/koaf095).
- Becana M (2025) Recycling of purine nucleotides in legumes: functional specialization of enzyme isoforms in adenine salvage, cytokinin homeostasis, and nodulation control. J Exp Bot 76: 913-916.
- Minguillón S, Fischer-Schrader K, Pérez-Rontomé C, Matamoros MA, Becana M (2024) The enigmatic enzyme ‘amidoxime reducing component’ of Lotus japonicus. Characterization, expression, activity in plant tissues, and proposed role as a nitric oxide-forming nitrite reductase. Physiol Plant 176: e14438.
- Minguillón S, Román A, Pérez-Rontomé C, Wang L, Xu P, Murray J, Duanmu D, Rubio MC, Becana M (2024) Dynamics of hemoglobins during nodule development, nitrate response, and dark stress in Lotus japonicus. J Exp Bot 75: 1547-1564.
- Matamoros MA, Romero LC, Tian T, Roman A, Duanmu D, Becana M (2024) Persulfidation of plant and bacteroid proteins is involved in legume nodule development and senescence. J Exp Bot 75: 3009-3025.
- Zhou Y, Wang L, Rubio MC, Pérez-Rontomé C, Zhou Y, Qi Y, Tian T, Zhang W, Fan Q, Becana M, Duanmu D (2023) Heme catabolism mediated by heme oxygenase in uninfected interstitial cells enables efficient nitrogen fixation in Lotus japonicus nodules. New Phytol 239: 1989-2006.
- Wang L, Tian T, Liang J, Li R, Xin X, Qi Y, Zhou Y, Fan Q, Ning G, Becana M, Duanmu D (2023) A transcription factor of the NAC family regulates nitrate-induced legume nodule senescence. New Phytol 238: 2113-2129.
- Minguillón S, Matamoros MA, Duanmu D, Becana M (2022) Signaling by reactive molecules and antioxidants in legume nodules. New Phytol 236: 815-832.
- Wang L, Zhou Y, Li R, Liang J, Tian T, Ji J, Chen R, Zhou Y, Fan Q, Ning G, Larkin RM, Becana M, Duanmu D (2022) Single cell-type transcriptome profiling reveals genes that promote nitrogen fixation in the infected and uninfected cells of legume nodules. Plant Biotechnol J 20: 616-618.
- Matamoros MA, Becana M (2021) Molecular responses of legumes to abiotic stress: post-translational modifications of proteins and redox signaling. J Exp Bot 72: 5876-5892.
- Villar I, Rubio MC, Calvo-Begueria L, Pérez-Rontomé C, Larrainzar E, Wilson MT, Sandal N, Mur LA, Wang L, Reeder B, Duanmu D, Uchiumi T, Stougaard J, Becana M (2021) Three classes of hemoglobins are required for optimal vegetative and reproductive growth of Lotus japonicus: genetic and biochemical characterization of LjGlb2-1. J Exp Bot 72: 7778-7791.
- Quilbé J, Lamy L, Brottier L, Leleux P, Fardoux J, Rivallan R, Benichou T, Guyonnet R, Becana M,Villar I, Garsmeur O, Hufnagel B, Delteil A, Gully D, Chaintreuil C, Pervent M, Cartieaux F, Bourge M, Valentin N, Martin G, Fontaine L, Droc G, Dereeper A, Farmer A, Libourel C, Nouwen N, Gressent F, Mournet P, D’Hont A, Giraud E, Klopp C, Arrighi JF (2021) Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium-legume symbiosis. Nature Commun 12: 829 (doi: 10.1038/s41467-021-21094-7).
- Abbruzzetti S, Barker AJ, Villar I, Pérez-Rontomé C, Bruno S, Cerullo G, Viappiani C, Becana M (2021) Unusually fast bis-histidyl coordination in a plant hemoglobin. Int J Mol Sci 22: 2740 (doi: 10.3390/ ijms22052740).
- Villar I, Larrainzar E, Milazzo L, Pérez-Rontomé C, Rubio MC, Smulevich G, Martínez JI, Wilson MT, Reeder B, Huertas R, Abbruzzetti S, Udvardi MK, Becana M (2021) A plant gene encoding one-heme and two-heme hemoglobins with extreme reactivities toward diatomic gases and nitrite. Front Plant Sci 11: 600336 (doi: 10.3389/fpls.2020.600336).
- Becana M, Yruela I, Sarath G, Catalán P, Hargrove MS (2020) Plant hemoglobins: a journey from unicellular green algae to vascular plants. New Phytol 227: 1618-1635.
- Larrainzar E, Villar I, Rubio MC, Pérez-Rontomé C, Huertas R, Sato S, Mun JH, Becana M (2020) Hemoglobins in the legume-Rhizobium. New Phytol 228: 472-484.
- Matamoros MA, Cutrona MC, Wienkoop S, Begara-Morales JC, Sandal N, Orera I, Barroso JB, Stougaard J, Becana M (2020) Altered plant and nodule development and protein S-nitrosylation in Lotus japonicus mutants deficient in S-nitrosoglutathione reductases. Plant Cell Physiol 61: 105-117.
- Wang L, Rubio MC, Xin X, Zhang B, Fan Q, Wang Q, Ning G, Becana M, Duanmu D (2019) CRISPR/Cas9 knockout of leghemoglobin genes in Lotus japonicus uncovers their synergistic roles in symbiotic nitrogen fixation. New Phytol 224: 818-832.
- Fukudome M, Watanabe E, Osuki K, Imaizumi R, Aoki T, Kucho K, Becana M, Uchiumi T (2019) Stably transformed Lotus japonicus plants overexpressing phytoglobin LjGlb1-1 show decreased nitric oxide levels in roots and nodules as well as delayed nodule senescence. Plant Cell Physiol 60: 816-825.
- Rubio MC, Calvo-Begueria L, Díaz-Mendoza M, Elhiti M, Moore M, Matamoros MA, James EK, Díaz I, Pérez-Rontomé C, Villar I, Calvo V, Hebelstrup KH, Dietz KJ, Becana M (2019) Phytoglobins in the chloroplasts, nuclei and cytoplasm modulate nitric oxide signaling and interact with abscisic acid. Plant J 100: 38-54.
- Calvo-Begueria L, Rubio MC, Martínez JI, Pérez-Rontomé C, Delgado MJ, Bedmar EJ, Becana M (2018) Redefining nitric oxide production in legume nodules through complementary insights from electron paramagnetic resonance spectroscopy and specific fluorescent probes. J Exp Bot 69: 3703-3714.
- Matamoros MA, Kim A, Peñuelas M, Ihling C, Griesser E, Hoffmann R, Fedorova M, Frolov A, Becana M (2018) Protein carbonylation and glycation in legume nodules. Plant Physiol 177: 1510-1528.
- Calvo-Begueria L, Cuypers B, Van Doorslaer S, Abbruzzetti S, Bruno S, Berghmans H, Dewilde S, Ramos J, Viappiani C, Becana M (2017) Characterization of the heme pocket structure and ligand binding kinetics of non-symbiotic hemoglobins from the model legume Lotus japonicus.Front Plant Sci 8:407 (doi: 10.3389/fpls.2017.00407).
- Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N, Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in legume root nodules. J Exp Bot 66: 2979-2990.
- Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M (2015) Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J 81: 723-735.
- Matamoros MA, Fernández-García N, Wienkoop S, Loscos J, Saiz A, Becana M (2013) Mitochondria are an early target of oxidative modifications in senescing legume nodules. New Phytol 197: 873-885.
Grants
- Becana M (IP) (2022-2025) Función de las hemoglobinas en la simbiosis rizobio-leguminosa en condiciones fisiológicas y de estrés nutricional. Agencia Estatal de Investigación, Ministerio de Ciencia e Innovación (PID2020-113985GB-I00)
- Becana M (IP1), Matamoros MA (IP2) (2024-2027) Regulación de las hemoglobinas en la simbiosis rizobio-leguminosa en la respuesta a bajo y alto nitrato. Agencia Estatal de Investigación, Ministerio de Ciencia, Innovación y Universidades (PID2023-147035NB-I00)
- Becana M (IP), Matamoros MA, Rubio MC, Pérez-Rontomé C, Minguillón S, Duanmu D, Wienkoop S, Stasolla C, Reeder B (2021-2024) Función de las hemoglobinas en la simbiosis rizobio-leguminosa en condiciones fisiológicas y de estrés nutricional. Agencia Estatal de Investigación, Ministerio de Ciencia e Innovación. PID2020-113985GB-I00.
- Becana M (coordinator), Abadía J, Picorel R, Gogorcena Y (2010-2022) Functions of genes, proteins and metabolites of plants. Aragón Government. Group A53 (2010-2016), A09_17R (2017-2019) and A09_20R (2020-2022).
- Becana M (IP), Rubio MC (co-IP), Matamoros MA, Pérez-Rontomé C, Villar I, Minguillón S, Wienkoop S, Sandal N, Duanmu D (2018-2021) Función de las hemoglobinas y del óxido nítrico en la simbiosis rizobio-leguminosa. Ministerio de Ciencia e Innovación. AGL2017-85775-R.
- Becana M (IP), Matamoros MA (co-IP), Pérez-Rontomé C, Calvo-Begueria L, Calvo V, Villar I, Cutrona C, Uchiumi T, Hoffmann R, Viappiani C (2015-2017) Fijación de nitrógeno por la simbiosis rizobio-leguminosa: hemoglobinas y modificaciones oxidativas de las proteínas durante el desarrollo y senescencia de los nódulos. Ministerio de Economía y Competitividad. AGL2014-53717-R.
Relevant methods
- Production of recombinant proteins and biochemical characterization of hemoglobins
- Determination and localization of antioxidants and reactive oxygen and nitrogen species
- Post-translational modifications of proteins mediated by free radicals
Collaborations with other national and international research groups
- Deqiang Duanmu (Huazhong Agricultural University, China)
- Estíbaliz Larrainzar (Universidad Pública de Navarra, Spain)
- Jesús I. Martínez (Universidad de Zaragoza, Spain)
- Brandon Reeder (University of Essex, UK)
- Niels Sandal and Jens Stougaard (University of Aarhus, Denmark)
- Stefanie Wienkoop (University of Vienna, Austria)
- Marta Martínez-Júlvez (Universidad de Zaragoza, Spain)
- Jeremy Murray (Shanghai Institute of Plant Physiology and Ecology, China)
- Didier Reinhardt (University of Fribourg, Switzerland)
Links to the group's websites and social media pages
https://www.eead.csic.es