Exploring the potential of beta rhizobium in nitrogen fixation and agricultural sustainability
DOI:
https://doi.org/10.14719/pst.4958Keywords:
beta-rhizobia, nodulation, phylogeny, ParaburkholderiaAbstract
Some of the earliest discovered nitrogen-fixing symbiotic prokaryotes were
the ‘Rhizobia,’ microbes that associate with legume. A relatively recent group
of nitrogen-fixing bacteria, beta-rhizobia plays a significant role in sustainable
agriculture. Detailed insights into the relationships between beta-rhizobia
and leguminous plants can be found in the phylogeny and taxonomy section
on legumes. Here, we provide a discussion of recent literature focusing on the
molecular aspects of beta-rhizobia-plant interactions, with potential
implications for enhancing nitrogen fixation beyond nodulation processes.
Furthermore, we emphasize the importance of coordinating knowledge from
other disciplines in to harness these beneficial microbes and advance
sustainable crop farming practices. In other words, this review aims to explore
the potential of beta-rhizobia and their contributions to sustainable
agriculture.
Downloads
References
Kebede E. Contribution, utilization and improvement of legumes-driven biological nitrogen fixation in agricultural systems. Front Sustain Food Syst. 2021;5:767998. https://doi.org/10.3389/fsufs.2021.767998
Vance CP, Graham PH. Nitrogen fixation in agriculture: Application and perspectives. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE. (eds). Nitrogen Fixation: Fundamentals and Applications [Internet]. Dordrecht: Springer Netherlands. 1995; p. 77-86. Available from: http://link.springer.com/. https://doi.org/10.1007/978-94-011-0379-4_10
Allito BB, Nana EM, Alemneh AA. Rhizobia strain and legume genome interaction effects on nitrogen fixation and yield of grain legume: A review. Mol Soil Biol . 2015 ;6(2):1-6. https://doi.org/10.5376/msb.2015.06.0002
Kebede E. Competency of rhizobial inoculation in sustainable agricultural production and biocontrol of plant diseases. Front Sustain Food Syst. 2021;5:728014. https://doi.org/10.3389/fsufs.2021.728014
Moulin L, Munive A, Dreyfus B, Boivin-Masson C. Nodulation of legumes by members of the b-subclass of Proteobacteria. Nature. 2001;411(6840):948-50. https://doi.org/10.1038/35082070. Erratum in: Nature 2001;412(6850):926.
Goyal RK, Mattoo AK, Schmidt MA. Rhizobial–host interactions and symbiotic nitrogen fixation in legume crops toward agriculture sustainability. Front Microbiol. 2021;12:669404. https://doi.org/10.3389/fmicb.2021.669404
Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, et al. Legume-nodulating betaproteobacteria: Diversity, host range and future prospects. Mol Plant Microbe Interact. 2011;24(11):1276-88. https://doi.org/10.1094/MPMI-06-11-0172
Peter J, Young W, Haukka KE. Diversity and phylogeny of rhizobia. New Phytol. 1996;133(1):87-94. https://doi.org/10.1111/j.1469-8137.1996.tb04344.x
Willems A. The taxonomy of rhizobia: an overview. Plant Soil. 2006;287(1-2):3-14. https://doi.org/10.1007/s11104-006-9058-7
Bellés-Sancho P, Beukes C, James EK, Pessi G. Nitrogen-fixing symbiotic Paraburkholderia species: Current knowledge and future perspectives. Nitrogen. 2023 ;4(1):135-58. https://doi.org/10.3390/nitrogen4010010
Geurts R, Bisseling T. Rhizobium nod factor perception and signalling. Plant Cell. 2002 ;14 (suppl 1):S239-49. https://doi.org/10.1105/tpc.002451
Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol. 2018;16:291-303. https://doi.org/10.1038/nrmicro.2017.171
Checcucci A, DiCenzo GC, Bazzicalupo M, Mengoni A. Trade, diplomacy and warfare: The quest for elite rhizobia inoculant strains. Front Microbiol. 2017;8:2207. https://doi.org/10.3389/fmicb.2017.02207
Whipps JM. Microbial interactions and biocontrol in the rhizosphere. J Exp Bot. 2001;52 (suppl 1):487-511. https://doi.org/10.1093/jexbot/52.suppl_1.487
Liu XY, Wu W, Wang ET, Zhang B, Macdermott J, Chen WX. Phylogenetic relationships and diversity of ?-rhizobia associated with Mimosa species grown in Sishuangbanna, China. Int J Syst Evol Microbiol. 2011;61(2):334-42. https://doi.org/10.1099/ijs.0.020560-0
Chen WF, Wang ET, Ji ZJ, Zhang JJ. Recent development and new insight of diversification and symbiosis specificity of legume rhizobia: mechanism and application. J Appl Microbiol. 2021;131(2):553-63. https://doi.org/10.1111/jam.14960
Graham PH, Vance CP. Legumes: Importance and constraints to greater use. Plant Physiol. 2003;131(3):872-77. https://doi.org/10.1104/pp.017004
Goyal RK, Habtewold JZ. Evaluation of legume–rhizobial symbiotic interactions beyond nitrogen fixation that help the host survival and diversification in hostile environments. Microorganisms. 2023;11(6):1454. https://doi.org/10.3390/microorganisms11061454
Zahran HH. Rhizobium - legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev. 1999;63(4):968-89. https://doi.org/10.1128/MMBR.63.4.968-989.1999
Sawada H, Kuykendall LD, Young JM. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol. 2003;49(3):155-79. https://doi.org/10.2323/jgam.49.155
Estrada-de Los Santos P, Vinuesa P, Martínez-Aguilar L, Hirsch AM, Caballero-Mellado J. Phylogenetic analysis of Burkholderia species by multilocus sequence analysis. Curr Microbiol. 2013;67:51-60. https://doi.org/10.1007/s00284-013-0330-9
El-Banna N, Winkelmann G. Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against streptomycetes. J Appl Microbiol. 1998 ;85(1):69–78. https://doi.org/10.1046/j.1365-2672.1998.00473.x
AuCoin DP, Crump RB, Thorkildson P, Nuti DE, LiPuma JJ, Kozel TR. Identification of Burkholderia cepacia complex bacteria with a lipopolysaccharide-specific monoclonal antibody. J Med Microbiol. 2010 ;59(1):41-47. https://doi.org/10.1099/jmm.0.012500-0
Lindström K, Mousavi SA. Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol. 2020;13(5):1314-35. https://doi.org/10.1111/1751-7915.13517
Rahimlou S, Bahram M, Tedersoo L. Phylogenomics reveals the evolution of root nodulating alpha- and beta-Proteobacteria (rhizobia). Microbiol Res. 2021;250:126788. https://doi.org/10.1016/j.micres.2021.126788
Beukes CW, Boshoff FS, Phalane FL, Hassen AI, Le Roux MM, St?pkowski T, et al. Both alpha- and beta-rhizobia occupy the root nodules of Vachellia karroo in South Africa. Front Microbiol. 2019;10:1195. https://doi.org/10.3389/fmicb.2019.01195
Hassen AI, Lamprecht SC, Bopape FL. Emergence of ?-rhizobia as new root nodulating bacteria in legumes and current status of the legume–rhizobium host specificity dogma. World J Microbiol Biotechnol. 2020;36:40. https://doi.org/10.1007/s11274-020-2811-x
Rajkumari J, Katiyar P, Dheeman S, Pandey P, Maheshwari DK. The changing paradigm of rhizobial taxonomy and its systematic growth upto postgenomic technologies. World J Microbiol Biotechnol. 2022;38:206. https://doi.org/10.1007/s11274-022-03370-w
Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX. Robust markers reflecting phylogeny and taxonomy of rhizobia. Badger JH, editor. PLoS ONE. 2012;7(9):e44936. https://doi.org/10.1371/journal.pone.0044936
Koskey G, Mburu SW, Kimiti JM, Ombori O, Maingi JM, Njeru EM. Genetic characterization and diversity of Rhizobium isolated from root nodules of mid-altitude climbing bean (Phaseolus vulgaris L.) varieties. Front Microbiol. 2018;9:968. https://doi.org/10.3389/fmicb.2018.00968
Lemaire B, Van Cauwenberghe J, Verstraete B, Chimphango S, Stirton C, Honnay O, et al. Characterization of the papilionoid– Burkholderia interaction in the Fynbos biome: The diversity and distribution of beta-rhizobia nodulating Podalyria calyptrata (Fabaceae, Podalyrieae). Syst Appl Microbiol. 2016;39(1):41-48. https://doi.org/10.1016/j.syapm.2015.09.006
Liu G, Liu X, Liu W, Gao K, Chen X, Wang ET, et al. Biodiversity and geographic distribution of rhizobia nodulating with Vigna minima. Front Microbiol. 2021;12:665839. https://doi.org/10.3389/fmicb.2021.665839
Lemaire B, Dlodlo O, Chimphango S, Stirton C, Schrire B, Boatwright JS, et al. Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa). FEMS Microbiol Ecol. 2015;91(2):1-17. https://doi.org/10.1093/femsec/fiu024
Gerding M, O’Hara GW, Bräu L, Nandasena K, Howieson JG. Diverse Mesorhizobium spp. with unique nodA nodulating the South African legume species of the genus Lessertia. Plant Soil. 2012 ;358(1-2):385-401. https://doi.org/10.1007/s11104-012-1153-3
Andrews M, De Meyer S, James EK, St?pkowski T, Hodge S, Simon MF, et al. Horizontal transfer of symbiosis genes within and between rhizobial genera: Occurrence and importance. Genes. 2018 ;9(7):321. https://doi.org/10.3390/genes9070321
Liu XY, Wei S, Wang F, James EK, Guo X, Zagar C, et al. Burkholderia and Cupriavidus spp. are the preferred symbionts of Mimosa spp. in Southern China. FEMS Microbiol Ecol. 2012;80(2):417-26. https://doi.org/10.1111/j.1574-6941.2012.01310.x
Heuer H, Smalla K. Horizontal gene transfer between bacteria. Environ Biosafety Res. 2007;6(1-2):3-13. https://doi.org/10.1051/ebr:2007034
Magnus Nielsen K, Van Elsas JD. Horizontal gene transfer and microevolution in soil.In: Nielsen KM, van Elsas JD. (Eds). Modern Soil Microbiology . 3rd ed. |CRC Press. 2019 ; p. 105-23.
Vandamme P, Goris J, Chen WM, De Vos P, Willems A. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol. 2002 ;25(4):507-12. https://doi.org/10.1078/07232020260517634
Shankar S, Haque E, Ahmed T, Kiran GS, Hassan S, Selvin J. Rhizobia–legume symbiosis during environmental stress.In: Shrivastava N, Mahajan S, Varma A. (eds).. Symbiotic Soil Microorganisms. Soil Biology, vol 60. Springer, Cham.2021;p. 201-20. https://doi.org/10.1007/978-3-030-51916-2_13,
Hawkins JP, Oresnik IJ. The Rhizobium-legume symbiosis: Co-opting successful stress management. Front Plant Sci. 2022;12:796045. https://doi.org/10.3389/fpls.2021.796045
Florentino LA, Jaramillo PMD, Silva KB, da Silva JS, de Oliveira SM, de Souza Moreira FM. Physiological and symbiotic diversity of Cupriavidus necator strains isolated from nodules of Leguminosae species. Sci Agric. 2012;69(4):247-58. https://doi.org/10.1590/S0103-90162012000400003
Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C. Legume symbiotic nitrogen fixation by ?-proteobacteria is widespread in nature. J Bacteriol. 2003 ;185(24):7266-72. https://doi.org/10.1128/JB.185.24.7266-7272.2003
Tsyganova AV, Brewin NJ, Tsyganov VE. Structure and development of the legume-rhizobial symbiotic interface in infection threads. Cells. 2021;10(5):1050. https://doi.org/10.3390/cells10051050
Acosta-Jurado S, Fuentes-Romero F, Ruiz-Sainz JE, Janczarek M, Vinardell JM. Rhizobial exopolysaccharides: Genetic regulation of their synthesis and relevance in symbiosis with legumes. Int J Mol Sci. 2021;22(12):6233. https://doi.org/10.3390/ijms22126233
Gray JX, Rolfe BG. Exopolysaccharide production in Rhizobium and its role in invasion. Mol Microbiol. 1990;4(9):1425-31. https://doi.org/10.1111/j.1365-2958.1990.tb02052.x
Coba De La Peña T, Fedorova E, Pueyo JJ, Lucas MM. The symbiosome: Legume and rhizobia co-evolution toward a nitrogen-fixing organelle? Front Plant Sci. 2018;8:2229. https://doi.org/10.3389/fpls.2017.02229
Sprent JI, Ardley J, James EK. Biogeography of nodulated legumes and their nitrogen?fixing symbionts. New Phytol. 2017;215(1):40-56. https://doi.org/10.1111/nph.14474
Dénarié J, Debellé F, Promé JC. Rhizobium lipo-chitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem. 1996 ;65:503-35. https://doi.org/10.1146/annurev.bi.65.070196.002443
Geddes BA, Kearsley J, Morton R, diCenzo GC, Finan TM. The genomes of rhizobia. In: Advances in Botanical Research. Elsevier; 2020 . p. 213-49. https://doi.org/10.1016/bs.abr.2019.09.014
Spaink HP, Wijfjes AH, Lugtenberg BJ. Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides. J Bacteriol. 1995;177(21):6276-81. https://doi.org/10.1128/jb.177.21.6276-6281.1995
Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990;344:781-84. https://doi.org/10.1038/344781a0
Lee A, Hirsch AM. Signals and responses: Choreographing the complex interaction between legumes and ?- and ?-rhizobia. Plant Signal Behav. 2006;1(4):161-68. https://doi.org/10.4161/psb.1.4.3143
Shumilina J, Soboleva A, Abakumov E, Shtark OY, Zhukov VA, Frolov A. Signaling in legume–rhizobia symbiosis. Int J Mol Sci. 2023;24(24):17397. https://doi.org/10.3390/ijms242417397
Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM. Investigations of Rhizobium biofilm formation: Rhizobia form biofilms. FEMS Microbiol Ecol. 2006;56(2):195-206. https://doi.org/10.1111/j.1574-6941.2005.00044.x
Nascimento FX, Tavares MJ, Rossi MJ, Glick BR. The modulation of leguminous plant ethylene levels by symbiotic rhizobia played a role in the evolution of the nodulation process. Heliyon. 2018;4(12):e01068. https://doi.org/10.1016/j.heliyon.2018.e01068
Shaharoona B, Imran M, Arshad M, Khalid A. Manipulation of ethylene synthesis in roots through bacterial ACC deaminase for improving nodulation in legumes. Crit Rev Plant Sci. 2011;30(3):279-91. https://doi.org/10.1080/07352689.2011.572058
Fahde S, Boughribil S, Sijilmassi B, Amri A. Rhizobia: A promising source of plant growth-promoting molecules and their non-legume interactions: Examining applications and mechanisms. Agriculture. 2023;13(7):1279. https://doi.org/10.3390/agriculture13071279
Sun W, Shahrajabian MH. The effectiveness of Rhizobium bacteria on soil fertility and sustainable crop production under cover and catch crops management and green manuring. Not Bot Horti Agrobot Cluj-Napoca. 2022;50(2):12560. https://doi.org/10.15835/nbha50212560
Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L. Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech. 2015;5:355-77. https://doi.org/10.1007/s13205-014-0241-x
Jaiswal SK, Mohammed M, Ibny FYI, Dakora FD. Rhizobia as a source of plant growth-promoting molecules: Potential applications and possible operational mechanisms. Front Sustain Food Syst. 2021;4:619676. https://doi.org/10.3389/fsufs.2020.619676
Vio SA, García SS, Casajus V, Arango JS, Galar ML, Bernabeu PR, et al. Paraburkholderia. In: Amaresan N, Senthil Kumar N, Annapurna K, Kumar K, Sankaranarayanan A. (Eds).Beneficial microbes in agro-ecology . Academi Press/ 2020; p. 271-311. https://doi.org/10.1016/B978-0-12-823414-3.00015-0
Herpell JB, Schindler F, Bejtovi? M, Fragner L, Diallo B, Bellaire A, et al. The potato yam phyllosphere ectosymbiont Paraburkholderia sp. Msb3 is a potent growth promotor in tomato. Front Microbiol. 2020;11:581. https://doi.org/10.3389/fmicb.2020.00581
Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A. Role of plant growth promoting rhizobacteria in agricultural sustainability—A review. Molecules. 2016;21(5):573. https://doi.org/10.3390/molecules21050573
Concha C, Doerner P. The impact of the rhizobia–legume symbiosis on host root system architecture. Gutiérrez R, editor. J Exp Bot. 2020;71(13):3902-21. https://doi.org/10.1093/jxb/eraa198
Bellés-Sancho P, Liu Y, Heiniger B, Von Salis E, Eberl L, Ahrens CH, et al. A novel function of the key nitrogen-fixation activator NifA in beta-rhizobia: Repression of bacterial auxin synthesis during symbiosis. Front Plant Sci. 2022;13:991548. https://doi.org/10.3389/fpls.2022.991548
Afzal M, Khan QM, Sessitsch A. Endophytic bacteria: Prospects and applications for the phytoremediation of organic pollutants. Chemosphere. 2014;117:232-42. https://doi.org/10.1016/j.chemosphere.2014.06.078
Teng Y, Wang X, Li L, Li Z, Luo Y. Rhizobia and their bio-partners as novel drivers for functional remediation in contaminated soils. Front Plant Sci . 2015 ;6:32. https://doi.org/10.3389/fpls.2015.00032
Keller KR, Lau JA. When mutualisms matter: Rhizobia effects on plant communities depend on host plant population and soil nitrogen availability. J Ecol. 2018;106(3):1046-56. https://doi.org/10.1111/1365-2745.12938
Sawana A, Adeolu M, Gupta RS. Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet. 2014 ;5:429 https://doi.org/10.3389/fgene.2014.00429
Howieson JG, De Meyer SE, Vivas-Marfisi A, Ratnayake S, Ardley JK, Yates RJ. Novel Burkholderia bacteria isolated from Lebeckia ambigua – A perennial suffrutescent legume of the fynbos. Soil Biol Biochem. 2013;60:55-64. https://doi.org/10.1016/j.soilbio.2013.01.009
Moulin L, Béna G, Boivin-Masson C, St?pkowski T. Phylogenetic analyses of symbiotic nodulation genes support vertical and lateral gene co-transfer within the Bradyrhizobium genus. Mol Phylogenet Evol. 2004;30(3):720-32. https://doi.org/10.1016/S1055-7903(03)00255-0
Garau G, Yates RJ, Deiana P, Howieson JG. Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem. 2009;41(1):125-34. https://doi.org/10.1016/j.soilbio.2008.10.011
Elliott GN, Chen WM, Bontemps C, Chou JH, Young JPW, Sprent JI, et al. Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot. 2007;100(7):1403-11. https://doi.org/10.1093/aob/mcm227
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 SS Amal, R Raghu, R Anandham, M Djanaguiraman
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright and Licence details of published articles
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Open Access Policy
Plant Science Today is an open access journal. There is no registration required to read any article. All published articles are distributed under the terms of the Creative Commons Attribution License (CC Attribution 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited (https://creativecommons.org/licenses/by/4.0/). Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
