Symbiotic Relationships between Nitrogen-fixing Bacteria and Leguminous Plants Ecological and Evolutionary Perspectives: A Review

Sushma Raj Chellem *

Department of Genetics and Plant Breeding, KL College of Agriculture, Koneru Lakshmaiah Education Foundation, Guntur, Andhra Pradesh, India.

Chiriki Vasantha Lakshmana Kishore

b Department of Agronomy, Himgiri zee university, Dehradun, India.

Gurrala Sai Vamsi Reddy

Department of Genetics and Plant Breeding, KL College of Agriculture, Koneru Lakshmaiah Education Foundation, Guntur, Andhra Pradesh, India.

D. V. S. Akshay

College of Agriculture, ANGRAU, Bapatla, Andhra Pradesh, India.

Kavuri Kalpana

Department of Genetics and Plant Breeding, KL College of Agriculture, Koneru Lakshmaiah Education Foundation, Guntur, Andhra Pradesh, India.

Purimetla Lavanya

KL College of Agriculture, Koneru Lakshmaiah Education Foundation, Guntur, Andhra Pradesh, India.

Kavya Harshita Choragudi

KL College of Agriculture, Koneru Lakshmaiah Education Foundation, Guntur, Andhra Pradesh, India.

*Author to whom correspondence should be addressed.


Abstract

The symbiotic relationships between nitrogen-fixing bacteria and leguminous plants play a Important role in enhancing soil fertility, boosting crop yields, and promoting sustainable agricultural practices. The molecular and biochemical mechanisms underpinning these interactions, including signal exchange, root nodule formation, and metabolic integration. The co-evolution of legumes and rhizobia, driven by reciprocal selective pressures, has resulted in highly specialized and efficient symbiotic relationships. Genetic adaptations in legumes, such as the evolution of receptor-like kinases and transcription factors, facilitate the establishment and maintenance of these symbioses. The evolutionary divergence among nitrogen-fixing bacteria, influenced by host specificity and environmental factors, has led to a diverse array of rhizobial strains with varying symbiotic capabilities. Horizontal gene transfer has further contributed to the spread of symbiotic traits, enhancing the adaptability and ecological success of rhizobia. In agricultural contexts, the benefits of symbiotic nitrogen fixation are substantial, reducing reliance on synthetic fertilizers and improving soil health. Sustainable practices such as crop rotation, intercropping, and cover cropping with legumes enhance soil nitrogen levels and overall farm productivity. Advances in genetic engineering and biofertilizer technology offer promising avenues to optimize symbiotic efficiency and extend nitrogen-fixing capabilities to non-leguminous crops. Challenges remain, including the need for effective delivery systems for biofertilizers and the variability of symbiotic performance under different environmental conditions. Future research should focus on understanding soil microbial interactions and developing resilient rhizobial strains. By leveraging these natural processes, we can enhance agricultural sustainability, ensuring food security and environmental health for future generations. This comprehensive review underscores the critical importance of nitrogen-fixing symbioses in agriculture and ecosystem management.

Keywords: Symbiosis, nitrogen-fixation, rhizobia, soil-fertility, biofertilizers


How to Cite

Chellem, S. R., Kishore, C. V. L., Reddy, G. S. V., Akshay, D. V. S., Kalpana, K., Lavanya, P., & Choragudi, K. H. (2024). Symbiotic Relationships between Nitrogen-fixing Bacteria and Leguminous Plants Ecological and Evolutionary Perspectives: A Review. UTTAR PRADESH JOURNAL OF ZOOLOGY, 45(13), 145–160. https://doi.org/10.56557/upjoz/2024/v45i134143

Downloads

Download data is not yet available.

References

Burns RC, Hardy RW. Nitrogen fixation in bacteria and higher plants; 2012.

Broughton WJ, Jabbouri S, Perret X. Keys to symbiotic harmony. Journal of Bacteriology. 2000;182(20):5641-5652.

Brill WJ. Biological nitrogen fixation. Scientific American. 1977;236(3):68-81.

Harindintwali JD, Zhou J, Muhoza B, Wang F, Herzberger A, Yu X. Integrated eco-strategies towards sustainable carbon and nitrogen cycling in agriculture. Journal of Environmental Management. 2021;293: 112856.

Gruhn P, Goletti F, Yudelman M. Integrated nutrient management, soil fertility, and sustainable agriculture: Current issues and future challenges. Intl Food Policy Res Inst; 2000.

Day L. Proteins from land plants–potential resources for human nutrition and food security. Trends in Food Science and Technology. 2013;32(1):25-42.

Mathesius U. Are legumes different? Origins and consequences of evolving nitrogen fixing symbioses. Journal of Plant Physiology. 2022;276:153765.

Burns RC, Hardy RW. Nitrogen fixation in bacteria and higher plants; 2012.

Peoples MB, Faizah AW, Rerkasem B, Herridge DF. Methods for evaluating nitrogen fixation by nodulated legumes in the field; 1989.

Simmonds J. Community matters: A history of biological nitrogen fixation and nodulation research, 1965 to 1995. Rensselaer Polytechnic Institute; 2007.

O'hara GW. Nutritional constraints on root nodule bacteria affecting symbiotic nitrogen fixation: A review. Australian Journal of Experimental Agriculture. 2001;41(3):417-433.

Martínez-Hidalgo P, Hirsch AM. The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes Journal. 2017;1(2):70-82.

Vance CP. Legume symbiotic nitrogen fixation: Agronomic aspects. In The Rhizobiaceae: Molecular biology of model plant-associated bacteria. Dordrecht: Springer Netherlands. 1998;509-530.

Beringer JE, Brewin NJ, Johnston AWB, Schulman HM, Hopwood DA. The Rhizobium-legume symbiosis. Proceedings of the Royal Society of London. Series B. Biological Sciences. 1979;204(1155):219-233.

Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microbial Cell Factories. 2014;13:1-10.

Werner D, Newton WE. (Eds.). Nitrogen fixation in agriculture, forestry, ecology, and the environment. Springer Science and Business Media. 2005;4.

Hirsch AM, Lum MR, Downie JA. What makes the rhizobia-legume symbiosis so special? Plant Physiology. 2001;127(4):1484-1492.

Aloo BN, Tripathi V, Makumba BA, Mbega ER. Plant growth-promoting rhizobacterial biofertilizers for crop production: The past, present, and future. Frontiers in Plant Science. 2022;13:1002448.

Dixon RA. The genetic complexity of nitrogen fixation. Microbiology. 1984; 130(11):2745-2755.

Walker L, Lagunas B, Gifford ML. Determinants of host range specificity in legume-rhizobia symbiosis. Frontiers in Microbiology. 2020;11:585749.

Qureshi MI, Muneer S, Bashir H, Ahmad J, Iqbal M. Nodule physiology and proteomics of stressed legumes. In Advances in Botanical Research. Academic Press. 2010;56:1-48.

Epstein B, Tiffin P. Comparative genomics reveals high rates of horizontal transfer and strong purifying selection on rhizobial symbiosis genes. Proceedings of the Royal Society B. 2021;288(1942): 20201804.

Zhang X, Ward BB, Sigman DM. Global nitrogen cycle: Critical enzymes, organisms, and processes for nitrogen budgets and dynamics. Chemical Reviews. 2020;120(12):5308-5351.

Fisher K, Newton WE. Nitrogen fixation—a general overview. Nitrogen fixation at the millennium. Amsterdam: Elsevier. 2002; 1-34.

Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Biology. 1996;47(1):569-593.

Howard JB, Rees DC. How many metals does it take to fix N2? A mechanistic overview of biological nitrogen fixation. Proceedings of the National Academy of Sciences. 2006;103(46):17088-17093.

Einsle O, Rees DC. Structural enzymology of nitrogenase enzymes. Chemical Reviews. 2020;120(12):4969-5004.

Sapra R, Bagramyan K, Adams MW. A simple energy-conserving system: Proton reduction coupled to proton translocation. Proceedings of the National Academy of Sciences. 2003;100(13):7545-7550.

Maier RJ. Chapter 5: Nitrogen fixation and respiration: two processes linked by the energetic demands of nitrogenase. In Respiration in Archaea and Bacteria: Diversity of Prokaryotic Respiratory Systems. Dordrecht: Springer Netherlands. 2004;101-120.

Raymond J, Siefert JL, Staples CR, Blankenship RE. The natural history of nitrogen fixation. Molecular Biology and Evolution. 2004;21(3):541-554.

Elmerich C, De Zamaroczy M, Arsene F, Pereg L, Paquelin A, Kaminski A. Regulation of nif gene expression and nitrogen metabolism in Azospirillum. Soil Biology and Biochemistry. 1997;29(5-6):847-852.

Mettert EL, Kiley PJ. Fe–S proteins that regulate gene expression. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 2015;1853(6):1284-1293.

Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends in Microbiology. 2016;24(1):63-75.

Marchal K, Vanderleyden J. The" oxygen paradox" of dinitrogen-fixing bacteria. Biology and Fertility of Soils. 2000;30: 363-373.

Cooper JE. Multiple responses of rhizobia to flavonoids during legume root infection. In Advances in Botanical Research. Academic Press. 2004;41:1-62.

Tuteja N, Mahajan S. Calcium signaling network in plants: An overview. Plant Signaling and Behavior. 2007;2(2): 79-85.

Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, Truchet G, Promé JC. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell. 1991;67(6):1131-1143.

Gage DJ, Margolin W. Hanging by a thread: Invasion of legume plants by rhizobia. Current Opinion in Microbiology. 2000;3(6):613-617.

Coba de la Pena T, Fedorova E, Pueyo JJ, Lucas MM. The symbiosome: Legume and rhizobia co-evolution toward a nitrogen-fixing organelle? Frontiers in Plant Science. 2018;8:305846.

Crespi M, Frugier F. De novo organ formation from differentiated cells: Root nodule organogenesis. Science Signaling. 2008;1(49):re11-re11.

Lodwig E, Poole P. Metabolism of Rhizobium bacteroids. Critical Reviews in Plant Sciences. 2003;22(1):37-78.

Miflin BJ, Habash DZ. The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany. 2002;53(370):979-987.

Horchani F, Prévot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Brouquisse R. Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiology. 2011;155(2):1023-1036.

Zipfel C, Oldroyd GE. Plant signalling in symbiosis and immunity. Nature. 2017;543(7645):328-336.

Kereszt A, Mergaert P, Montiel J, Endre G, Kondorosi É. Impact of plant peptides on symbiotic nodule development and functioning. Frontiers in Plant Science. 2018;9:396805.

Garg N, Geetanjali. Symbiotic nitrogen fixation in legume nodules: Process and signaling: A review. Sustainable Agriculture. 2009;519-531.

Scheublin TR, Van Der Heijden MG. Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytologist. 2006;172(4): 732-738.

Vitousek PM, Menge DN, Reed SC, Cleveland CC. Biological nitrogen fixation: Rates, patterns and ecological controls in terrestrial ecosystems. Philosophical Transactions of the Royal Society B: Biological Sciences. 2013;368(1621): 20130119.

Fageria NK. Role of soil organic matter in maintaining sustainability of cropping systems. Communications in Soil Science and Plant Analysis. 2012;43(16):2063-2113.

Babalola OO, Olanrewaju OS, Dias T, Ajilogba CF, Kutu FR, Cruz C. Biological nitrogen fixation: The role of underutilized leguminous plants. Microorganisms for Green Revolution: Volume 1: Microbes for Sustainable Crop Production. 2017;431-443.

Mitran T, Meena RS, Lal R, Layek J, Kumar S, Datta R. Role of soil phosphorus on legume production. Legumes for Soil Health and Sustainable Management. 2018;487-510.

Temperton VM, Mwangi PN, Scherer-Lorenzen M, Schmid B, Buchmann N. Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia. 2007;151:190-205.

Jena J, Maitra S, Hossain A, Pramanick B, Gitari HI, Praharaj S, Jatav HS. Role of legumes in cropping system for soil ecosystem improvement. Ecosystem services: Types, management and benefits. Nova Science Publishers, Inc, New York. 2022;1-22.

Daehler CC. Performance comparisons of co-occurring native and alien invasive plants: Implications for conservation and restoration. Annual Review of Ecology, Evolution, and Systematics. 2003;34(1):183-211.

Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Trost J. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature. 2006;440(7086):922-925.

Wang X, Li S, Huang S, Cui Y, Fu H, Li T, Yang X. Pinus massoniana population dynamics: Driving species diversity during the pioneer stage of ecological restoration. Global Ecology and Conservation. 2021;27:e01593.

Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst. 2004;35:557-581.

Clúa J, Roda C, Zanetti ME, Blanco FA. Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis. Genes. 2018;9(3):125.

Benjelloun I, Thami Alami I, Douira A, Udupa SM. Phenotypic and genotypic diversity among symbiotic and non-symbiotic bacteria present in chickpea nodules in Morocco. Frontiers in Microbiology. 2019;10:436368.

Ahluwalia O, Singh PC, Bhatia R. A review on drought stress in plants: Implications, mitigation and the role of plant growth promoting rhizobacteria. Resources, Environment and Sustainability. 2021;5:100032.

Shrivastava P, Kumar R. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Sciences. 2015;22(2):123-131.

Coba de la Pena T, Fedorova E, Pueyo JJ, Lucas MM. The symbiosome: Legume and rhizobia co-evolution toward a nitrogen-fixing organelle? Frontiers in Plant Science. 2018;8:305846.

Rashid MHO, Krehenbrink M, Akhtar MS. Nitrogen-fixing plant-microbe symbioses. Sustainable Agriculture Reviews. 2015;15:193-234.

Nasr-Sharif M. Reverse genetic study of four Medicago truncatula defence genes to elucidate involvement in arbuscular mycorrhizal symbiosis (Doctoral dissertation, Université d'Ottawa/University of Ottawa); 2020.

Singh J, Verma PK. Role of Nod factor receptors and its allies involved in nitrogen fixation. Planta. 2023;257(3):54.

Liu J, Bisseling T. Evolution of NIN and NIN-like genes in relation to nodule symbiosis. Genes. 2020;11(7):777.

Aranjuelo I, Arrese-Igor C, Molero G. Nodule performance within a changing environmental context. Journal of Plant Physiology. 2014;171(12):1076-1090.

Schulze J. How are nitrogen fixation rates regulated in legumes? Journal of Plant Nutrition and Soil Science. 2004;167(2):125-137.

Wang ET, Tian CF, Chen WF, Young JPW, Chen WX. Ecology and evolution of rhizobia . Springer Singapore. 2019;1-13.

Wang Q, Liu J, Zhu H. Genetic and molecular mechanisms underlying symbiotic specificity in legume-rhizobium interactions. Frontiers in Plant Science. 2018;9:334639.

Slattery JF, Coventry DR, Slattery WJ. Rhizobial ecology as affected by the soil environment. Australian Journal of Experimental Agriculture. 2001;41(3):289-298.

Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within symbiosis: Evolving nitrogen-fixing legume symbionts. Trends in Microbiology. 2016;24(1):63-75.

Perrine FM, Hocart CH, Hynes MF, Rolfe BG. Plasmid‐associated genes in the model micro‐symbiont Sinorhizobium meliloti 1021 affect the growth and development of young rice seedlings. Environmental Microbiology. 2005;7(11): 1826-1838.

Mendoza-Suárez M, Andersen SU, Poole PS, Sánchez-Cañizares C. Competition, nodule occupancy, and persistence of inoculant strains: Key factors in the rhizobium-legume symbioses. Frontiers in Plant Science. 2021;12:690567.

Raymond J, Siefert JL, Staples CR, Blankenship RE. The natural history of nitrogen fixation. Molecular Biology and Evolution. 2004;21(3):541-554.

Mahmud K, Makaju S, Ibrahim R, Missaoui A. Current progress in nitrogen fixing plants and microbiome research. Plants. 2020;9(1):97.

Mfilinge A, Mtei K, Ndakidemi P. Effects of Rhizobium inoculation and supplementation with P and K, on growth, leaf chlorophyll content and nitrogen fixation of bush bean varieties; 2014.

Peoples MB, Hauggaard ‐Nielsen H, Jensen ES. The potential environmental benefits and risks derived from legumes in rotations. Nitrogen Fixation in Crop Production. 2009;52:349-385.

Kremen C, Miles A. Ecosystem services in biologically diversified versus conventional farming systems: benefits, externalities, and trade-offs. Ecology and Society. 2012;17(4).

Sutton MA, Bleeker A, Howard CM, Erisman JW, Abrol YP, Bekunda M, Zhang FS. Our nutrient world. The challenge to produce more food and energy with less pollution. Centre for Ecology and Hydrology; 2013.

Chamkhi I, Cheto S, Geistlinger J, Zeroual Y, Kouisni L, Bargaz A, Ghoulam C. Legume-based intercropping systems promote beneficial rhizobacterial community and crop yield under stressing conditions. Industrial Crops and Products. 2022;183:114958.

Sharma P, Singh A, Kahlon CS, Brar AS, Grover KK, Dia M, Stein RL. The role of cover crops towards sustainable soil health and agriculture—A review paper. American Journal of Plant Sciences. 2018;9(9):1935-1951.

Kahane R, Hodgkin T, Jaenicke H, Hoogendoorn C, Hermann M, Keatinge JDH, Looney N. Agrobiodiversity for food security, health and income. Agronomy for Sustainable Development. 2013;33:671-693.

Goyal RK, Schmidt MA, Hynes MF. Molecular biology in the improvement of biological nitrogen fixation by rhizobia and extending the scope to cereals. Microorganisms. 2021;9(1):125.

Liu J, Bisseling T. Evolution of NIN and NIN-like genes in relation to nodule symbiosis. Genes. 2020;11(7):777.

Vanlauwe B, Hungria M, Kanampiu F, Giller KE. The role of legumes in the sustainable intensification of African smallholder agriculture: Lessons learnt and challenges for the future. Agriculture, Ecosystems and Environment. 2019; 284:106583.

Morales-García YE, Baez A, Quintero-Hernández V, Molina-Romero D, Rivera-Urbalejo AP, Pazos-Rojas LA, Muñoz-Rojas J. Bacterial mixtures, the future generation of inoculants for sustainable crop production. Field crops: Sustainable management by PGPR, 11-44; 2019.

Thilakarathna MS, Raizada MN. A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions. Soil Biology and Biochemistry. 2017;105:177-196.

Brooks SM, Alper HS. Applications, challenges, and needs for employing synthetic biology beyond the lab. Nature Communications. 2021;12(1):1390.

Rogers C, Oldroyd GE. Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. Journal of Experimental Botany. 2014;65(8):1939-1946.

Iquebal MA, Jagannadham J, Jaiswal S, Prabha R, Rai A, Kumar D. Potential use of microbial community genomes in various dimensions of agriculture productivity and its management: A review. Frontiers in Microbiology. 2022;13: 708335.

Kebede E. Contribution, utilization, and improvement of legumes-driven biological nitrogen fixation in agricultural systems. Frontiers in Sustainable Food Systems. 2021;5:767998.

Souza EM, Chubatsu LS, Huergo LF, Monteiro R, Camilios-Neto D, Wassem R, de Oliveira Pedrosa F. Use of nitrogen-fixing bacteria to improve agricultural productivity. In BMC Proceedings. BioMed Central. 2014;8:1-3.