Abstract
Background and Aims
Nitrogen (N) is essential for plant growth, yet the role of diazotrophic bacteria in non-nodulating plants, particularly from the β-class Pseudomonadota, remains unclear. We explored the mechanisms underlying the interaction of Cupriavidus taiwanensis LMG19424, belonging to this group and known for nodulation induction in Mimosa sp., with the non-nodulating plant Arabidopsis thaliana.
Methods
In vitro experiments with LMG19424 and Arabidopsis, varying N levels (KNO3), and utilizing plant and bacterial mutant lines were conducted. Then, we analyzed the physiological, nutritional, and molecular effects in the inoculated plants. We also evaluated the rhizospheric and endophytic colonization of the strain in this plant species.
Results
Inoculation with LMG19424 consistently increased rosette and root growth across a KNO3 gradient, except in roots in specific plant mutant lines (auxin and ethylene pathways). A nifH-deletion mutant of LMG19424 induced root development but lost the ability to stimulate rosette growth. C. taiwanensis colonized plants endophytically, increasing N and P content while decreasing Fe in plant tissues under varying KNO3 conditions. Furthermore, strain LMG19424 influenced plant gene expression in hormonal pathways and N transport/metabolism, with N conditions strongly affecting this regulation.
Conclusions
In Arabidopsis, LMG19424 acts as a Plant Growth Promoting Bacterium, with N availability critically influencing its effect on plant physiology and gene regulation. Microbial-N fixation modulates host plant growth, with contrasting shoot and root responses. This emphasizes the pivotal role of the abiotic environment, particularly N availability, in shaping microbial-plant interactions and offers insights into interactions among diazotrophic β-class Pseudomonadota and non-nodulating plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data that support the findings of this study are available on request from the corresponding author (MJP).
References
Adesemoye AO, Kloepper JW (2009) Plant-microbe interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12. https://doi.org/10.1007/s00253-009-2196-0
Amadou C, Mangenot S, Glew M, Bontemps C, Capela D, Dossat C, Marchetti M, Servin B, Saad M, Schenowitz C, Batut J, Masson-boivin C (2008) Genome sequence of the B-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18:1472–1483. https://doi.org/10.1101/gr.076448.108
Antoun H, Beauchamp CJ, Goussard N et al (1998) Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: Effect on radishes (Raphanus sativus L.). Plant Soil 204:57–67. https://doi.org/10.1023/A:1004326910584
Aquilanti L, Favilli F, Clemeti F (2004) Comparison of different strategies for isolation and preliminary identification of Azotobacter from soil samples. Soil Biol Biochem 36:1475–1483
Armijo G, Kraiser T, Medina MP, Gras DE, Zúñiga A, González B, Gutiérrez RA (2020) Arabidopsis thaliana interaction with Ensifer meliloti can support plant growth under N-deficiency. BioRxiv, 2020.07.25.221283. https://doi.org/10.1101/2020.07.25.221283
Bashan Y, de Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: Formulations and practical perspectives (1998–2013). Plant Soil 378:1–33. https://doi.org/10.1007/s11104-013-1956-x
Bashan Y, De-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136. https://doi.org/10.1016/S0065-2113(10)08002-8
Battenberg K, Potter D, Tabuloc CA, Chiu JC, Berry AM (2018) Comparative Transcriptomic Analysis of Two Actinorhizal Plants and the Legume Medicago truncatula Supports the Homology of Root Nodule Symbioses and Is Congruent With a Two-Step Process of Evolution in the Nitrogen-Fixing Clade of Angiosperms. Front Plant Sci 9:1256. https://doi.org/10.3389/fpls.2018.01256
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-011-0979-9
Bonkowski M, Villenave C, Griths B (2009) Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321:213–233. https://doi.org/10.1007/s11104-009-0013-2
Calderón Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L, Sheard LB, Tan X, Parry G, Mao H, Zheng N, Napier R, Kepinski S, Estelle M (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8:477–485. https://doi.org/10.1038/nchembio.926
Del Castillo LD, Hunt S, Layzell DB (1994) The Role of Oxygen in the Regulation of Nitrogenase Activity in Drought-Stressed Soybean Nodules. Plant Physiol 106:949–955. https://doi.org/10.1104/pp.106.3.949
Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545–559. https://doi.org/10.1105/tpc.006882
Chaput V, Li J, Séré D, Tillard P, Fizames C, Moyano T, Zuo K, Martin A, Gutiérrez RA, Gojon A, Lejay L (2023) Characterisation of the signalling pathways involved in the repression of root nitrate uptake by nitrate in Arabidopsis thaliana. J Exp Bot. https://doi.org/10.1093/jxb/erad149
Chen W, James EK, Prescott AR, Kierans M, Sprent JI (2003) Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. MPMI 16:1051–1061. https://doi.org/10.1094/MPMI.2003.16.12.1051
Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. IJSEM 51:1729–1735
Chen WM, Wu CH, James EK, Chang JS (2008) Metal biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica. J Hazard Mater 151:364–371
Cillero JI, Henríquez PA, Ledger TW, Ruz GA, González B (2022) Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species. BMC Microbiol 22:218. https://doi.org/10.1186/s12866-022-02633-8
Clavero-León C, Ruiz D, Cillero J, Orlando J, González B (2021) The multi metal-resistant bacterium Cupriavidus metallidurans CH34 affects growth and metal mobilization in Arabidopsis thaliana plants exposed to copper. PeerJ 9:e11373. https://doi.org/10.7717/peerj.11373
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17. https://doi.org/10.1104/pp.105.063743
Daubech B, Remigi P, Doin de Moura G, Marchetti M, Pouzet C, Auriac MC, Gokhale CS, Masson-Boivin C, Capela D (2017) Spatio-temporal control of mutualism in legumes helps spread symbiotic nitrogen fixation. Elife 6:e28683. https://doi.org/10.7554/elife.28683
Dawson JO (2007) Ecology of Actinorhizal plants. In: Pawlowski K and Newton W (eds) Nitrogen‐fixing actinorhizal symbioses. Nitrogen fixation: origins, applications, and research progress. Springer Netherlands, Dordrecht, pp 199–234
de Faria S, Ringelberg JJ, Gross EM, Koenen EJ et al (2022) The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes. New Phytol 235:2365–2377. https://doi.org/10.1111/nph.18321
Dobbelaere S, Vanderleyden J, Yaacov O (2003) Plant Growth-Promoting Effects of Diazotrophs in the Rhizosphere. Crit Rev Plant Sci 22:107–149. https://doi.org/10.1080/713610853
Elliott GN, Chen WM, Chou JH, Wang HC, Sheu SY, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, De Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173:168–180. https://doi.org/10.1111/j.1469-8137.2006.01894.x
Elliott GN, Chou JH, Chen WM, Bloemberg GV, Bontemps C, Martínez-Romero E, Velázquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778. https://doi.org/10.1111/j.1462-2920.2008.01799.x
Fan X, Naz M, Fan X, Xuan W, Miller AJ, Xu G (2017) Plant nitrate transporters: from gene function to application. J Exp Bot 68:2463–2475. https://doi.org/10.1093/jxb/erx011
Fernández-Crespo E, Scalschi L, Llorens E, García-Agustín P, Camañes G (2015) NH4+ protects tomato plants against Pseudomonas syringae by activation of systemic acquired acclimation. J Exp Bot 66:6777–6790
Fredes I, Moreno S, Díaz FP, Gutiérrez RA (2019) Nitrate signaling and the control of Arabidopsis growth and development. Curr Opin Plant Biol 47:112–118. https://doi.org/10.1016/j.pbi.2018.10.004
Fukami J, Cerezini P, Hungria M (2018) Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Expr 8:73. https://doi.org/10.1186/s13568-018-0608-1
Garrido-Oter R, Nakano RT, Dombrowski N, Ma KW, AgBiome Team, McHardy AC, Schulze-Lefert P (2018) Modular Traits of the Rhizobiales Root Microbiota and Their Evolutionary Relationship with Symbiotic Rhizobia. Cell Host Microbe 24:155-167.e5. https://doi.org/10.1016/j.chom.2018.06.006
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796. https://doi.org/10.1128/aem.61.2.793-796.1995
Griesmann M, Chang Y, Liu X, Song Y, Haberer G, Crook MB et al (2018) Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361:6398. https://doi.org/10.1126/science.aat1743
Hardoim PR, de Carvalho TLG, Ballesteros HGF, Bellieny-Rabelo D, Rojas CA et al (2020) Genome-Wide Transcriptome Profiling Provides Insights into the Responses of Maize (Zea mays L.) to Diazotrophic Bacteria. Plant Soil 451:121–143
Hernández-Reyes C, Lichtenberg E, Keller J, Delaux PM, Ott T, Schenk ST (2022) NIN-Like Proteins: Interesting Players in Rhizobia-Induced Nitrate Signaling Response During Interaction with Non-Legume Host Arabidopsis thaliana. Mol Plant Microbe Interact 35:230–243. https://doi.org/10.1094/MPMI-10-21-0261-R
Houmani H, Corpas FJ (2024) Can nutrients act as signals under abiotic stress? Plant Physiol Biochem 206:108313. https://doi.org/10.1016/j.plaphy.2023.108313
Jacoby R, Peukert M, Succurro A, Koprivova A, Kopriva S (2017) The Role of Soil Microorganisms in Plant Mineral Nutrition—Current Knowledge and Future Directions. Front Plant Sci 8:1617. https://doi.org/10.3389/fpls.2017.01617
Jia Z, von Wirén N (2020) Signaling pathways underlying nitrogen-dependent changes in root system architecture: From model to crop species. J Exp Bot 71:4393–4404. https://doi.org/10.1093/jxb/eraa033
Kechid M, Desbrosses G, Rokhsi W, Varoquaux F, Djekoun A, Touraine B (2013) The NRT2.5 and NRT2.6 genes are involved in growth promotion of arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain phyllobacterium brassicacearum STM196. New Phytol 198:514–524. https://doi.org/10.1111/nph.12158
Kolde R (2012) Pheatmap: pretty heatmaps. R Package Version 1.0.10. https://CRAN.R-project.org/package=pheatmap
Konishi M, Okitsu T, Yanagisawa S (2021) Nitrate-responsive NIN-like protein transcription factors perform unique and redundant roles in Arabidopsis. J Exp Bot 72:5735–5750. https://doi.org/10.1093/jxb/erab246
Kreutzer MF, Nett M (2012) Genomics-driven discovery of taiwachelin, a lipopeptide siderophore from Cupriavidus taiwanensis. Org Biomol Chem 10(47):9338–9343. https://doi.org/10.1039/c2ob26296g
Krouk G (2017) Nitrate signalling: Calcium bridges the nitrate gap. Nat Plants 19:17095. https://doi.org/10.1038/nplants.2017.95
Kuzma MM, Hunt S, Layzell DB (1993) Role of Oxygen in the Limitation and Inhibition of Nitrogenase Activity and Respiration Rate in Individual Soybean Nodules. Plant Physiol 101:161–169. https://doi.org/10.1104/pp.101.1.161
Ledger T, Zúñiga A, Kraiser T, Dasencich P, Donoso R, Pérez-Pantoja D, González B (2012) Aromatic compounds degradation plays a role in colonization of Arabidopsis thaliana and Acacia caven by Cupriavidus pinatubonensis JMP134. Antonie Van Leeuwenhoek 101(4):713–723. https://doi.org/10.1007/s10482-011-9685-8
Li Q, Li BH, Kronzucker HJ, Shi WM (2010) Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity. Plant Cell Environ 33:1529–1542
Li Y, Li Y, Zhang H, Wang M, Chen S (2019) Diazotrophic Paenibacillus beijingensis BJ-18 Provides Nitrogen for Plant and Promotes Plant Growth, Nitrogen Uptake and Metabolism. Front Microbiol 10:1119. https://doi.org/10.3389/fmicb.2019.01119
Lima JE, Kojima S, Takahashi H, von Wirén N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22:3621–3633
Lindström K, Mousavi SA (2020) Effectiveness of nitrogen fixation in rhizobia. Microb Biotechnol 13:1314–1335. https://doi.org/10.1111/1751-7915.13517
Liu Y, Lai N, Gao K, Chen F, Yuan L, Mi G (2013) Ammonium inhibits primary root growth by reducing the length of meristem and elongation zone and decreasing elemental expansion rate in the root apex in Arabidopsis thaliana. PLoS ONE 8:e61031. https://doi.org/10.1371/journal.pone.0061031
Liu J, Moore S, Chen C, Lindsey K (2017) Crosstalk Complexities between Auxin, Cytokinin, and Ethylene in Arabidopsis Root Development: From Experiments to Systems Modeling, and Back Again. Mol Plant 10:1480–1496. https://doi.org/10.1016/j.molp.2017.11.002
Liu KH, Niu Y, Konishi M et al (2017) Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545:311–316. https://doi.org/10.1038/nature22077
Liu Y, von Wirén N (2017) Ammonium as a signal for physiological and morphological responses in plants. J Exp Botany 68:2581–2592. https://doi.org/10.1093/jxb/erx086
Louden BC, Haarmann D, Lynne AM (2011) Use of Blue Agar CAS Assay for Siderophore Detection. J Microbiol Biol Educ 12:51–53. https://doi.org/10.1128/jmbe.v12i1.249
Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Gen Dev 12:2175–2187. https://doi.org/10.1101/gad.12.14.2175
Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872. https://doi.org/10.1093/jxb/ers091
Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel J-C, Touraine B (2006) Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223:591–603
Marín O, González B, Poupin MJ (2021) From Microbial Dynamics to Functionality in the Rhizosphere: A Systematic Review of the Opportunities With Synthetic Microbial Communities. Front Plant Sci 12:650609. https://doi.org/10.3389/fpls.2021.650609
Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818. https://doi.org/10.1111/j.1365-313X.2005.02642.x
Mora V, López G, Molina R, Coniglio A, Nievas S, De Diego N, Zeljković SĆ, Sarmiento SS, Spíchal L, Robertson S, Wilkins O, Elías J, Pedraza R, Estevez JM, Belmonte MF, Cassán F (2023) Azospirillum argentinense Modifies Arabidopsis Root Architecture Through Auxin-dependent Pathway and Flagellin. J Soil Sci Plant Nutr 23:4543–4557
Muller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Gen 50:211–234
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. https://doi.org/10.1016/S0378-1097(98)00555-2
Oleńska E, Imperato V, Małek W, Włostowski T, Wójcik M, Swiecicka I, Vangronsveld J, Thijs S (2020) Trifolium repens-Associated Bacteria as a Potential Tool to Facilitate Phytostabilization of Zinc and Lead Polluted Waste Heaps. Plants 9:1002. https://doi.org/10.3390/plants9081002
Orellana D, Machuca D, Ibeas MA, Estevez JM, Poupin MJ (2022) Plant-growth promotion by proteobacterial strains depends on the availability of phosphorus and iron in Arabidopsis thaliana plants. Front Microbiol 13:1083270. https://doi.org/10.3389/fmicb.2022.1083270
Ortíz-Castro R, Valencia-Cantero E, López-Bucio J (2008) Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signal Behav 3:263–265. https://doi.org/10.4161/psb.3.4.5204
Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33:1486–1501
Pickett FB, Wilson AK, Estelle M (1990) The aux1 Mutation of Arabidopsis Confers Both Auxin and Ethylene Resistance. Plant Physiol 94:1462–1466. https://doi.org/10.1104/pp.94.3.1462
Pinedo I, Ledger T, Greve M, Poupin MJ (2015) Burkholderia phytofirmans PsJN induces long-term metabolic and transcriptional changes involved in Arabidopsis thaliana salt tolerance. Front Plant Sci 6:466. https://doi.org/10.3389/fpls.2015.00466
Poupin MJ, Greve M, Carmona V, Pinedo I (2016) A Complex Molecular Interplay of Auxin and Ethylene Signaling Pathways Is Involved in Arabidopsis Growth Promotion by Burkholderia phytofirmans PsJN. Front Plant Sci 7:492. https://doi.org/10.3389/fpls.2016.00492
Poupin MJ, Ledger T, Roselló-Móra R, González B (2023) The Arabidopsis holobiont: a (re)source of insights to understand the amazing world of plant-microbe interactions. Environ Microb 18:9. https://doi.org/10.1186/s40793-023-00466-0
Poupin MJ, Timmermann T, Vega A, Zuñiga A, González B (2013) Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS ONE 8:e69435. https://doi.org/10.1371/journal.pone.0069435
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
Remigi P, Zhu J, Young JPW, Masson-Boivin C (2016) Symbiosis within Symbiosis: Evolving Nitrogen-Fixing Legume Symbionts. Trends Microbiol 24:63–75. https://doi.org/10.1016/j.tim.2015.10.007
Ringelberg JJ, Gross EM, Koenen EJ, Cardoso DD, Ametsitsi G et al (2022) The innovation of the symbiosome has enhanced the evolutionary stability of nitrogen fixation in legumes. New Phytol 235:2365–2377. https://doi.org/10.1111/nph.18321
Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA (2015) The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol 169:1397–1404
Rodríguez H, Fraga R, Gonzalez T et al (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21. https://doi.org/10.1007/s11104-006-9056-9
Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139:1393–1409. https://doi.org/10.1093/genetics/139.3.1393
Rosconi F, Souza EM, Pedrosa FO, Platero RA, González C, González M, Batista S, Gill PR, Fabiano ER (2015) Iron depletion affects nitrogenase activity and expression of nifH and nifA genes in Herbaspirillum seropedicae. FEMS Microbiol Lett 258:214–219. https://doi.org/10.1111/j.1574-6968.2006.00218.x
Salehin M, Bagchi R, Estelle M (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27:9–19. https://doi.org/10.1105/tpc.114.133744
Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767. https://doi.org/10.1093/aob/mct048
dos Santos SG, da Silva RF, Alves GC, Santos LA, Reis VM (2020) Inoculation with five diazotrophs alters nitrogen metabolism during the initial growth of sugarcane varieties with contrasting responses to added nitrogen. Plant Soil 451:25–44
Shi H, Li Y, Li P, Wang Z, Chen S (2016) Effect of nitrogen-fixing Paenibacillus spp. on wheat yield. J China Agric Univ 21:52–55
Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861. https://doi.org/10.1111/nph.12590
Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506. https://doi.org/10.1111/j.1574-6976.2000.tb00552.x
Steffen W, Richardson K, Rockstrom J, Cornell SE, Fetzer I, Bennett EM et al (2015) Planetary boundaries: guiding human development on a changing planet. Science 347:1259855. https://doi.org/10.1126/science.1259855
Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17:2230–2242. https://doi.org/10.1105/tpc.105.033365
Strittmatter CS, Poehlein A, Himmelbach A, Daniel R, Steinbüchel A (2023) Medium-Chain-Length Fatty Acid Catabolism in Cupriavidus necator H16: Transcriptome Sequencing Reveals Differences from Long-Chain-Length Fatty Acid β-Oxidation and Involvement of Several Homologous Genes. Applied Environ Microbiol 89:e0142822. https://doi.org/10.1128/aem.01428-22
Tang Q, Cotton A, Wei Z, Xia Y, Daniell T, Yan X (2022) How does partial substitution of chemical fertiliser with organic forms increase sustainability of agricultural production? Sci Total Environ 803:149933. https://doi.org/10.1016/j.scitotenv.2021.149933
Thanwisai L, Janket A, Siripornadulsil W, Siripornadulsil S (2022) A cadmium-tolerant bacterium (Cupriavidus taiwanensis KKU2500-3) reduces cadmium accumulation in grains of KDML105 rice cultivated in a contaminated paddy field. Environ Technol Innov 28:2352–1864. https://doi.org/10.1016/j.eti.2022.102685
Thomas J, Kim HR, Rahmatallah Y, Wiggins G, Yang Q, Id RS, Glazko G, Id AM (2019) RNA-Seq Reveals Differentially Expressed Genes in Rice (Oryza sativa) Roots during Interactions with Plant-Growth Promoting Bacteria. Azospirillum Brasilense Plos ONE 14:e0217309
Timmermann T, Armijo G, Donoso R, Seguel A, Holuigue L, González B (2017) Paraburkholderia phytofirmans PsJN Protects Arabidopsis thaliana Against a Virulent Strain of Pseudomonas syringae Through the Activation of Induced Resistance. MPMI 30:215–230. https://doi.org/10.1094/MPMI-09-16-0192-R
Timmermann T, Poupin MJ, Vega A, Urrutia C, Ruz GA, González B (2019) Gene networks underlying the early regulation of Paraburkholderia phytofirmans PsJN induced systemic resistance in Arabidopsis. PLoS ONE 14:e0221358. https://doi.org/10.1371/journal.pone.0221358
Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40:1971–1974. https://doi.org/10.1016/j.soilbio.2008.02.017
Vance C, Heichel G (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390
Verma SC, Chowdhury SP, Tripathi AK (2004) Phylogeny based on 16S rDNA and nifH sequences of Ralstonia taiwanensis strains isolated from nitrogen-fixing nodules of Mimosa pudica, in India. Can J Microbiol 50:313–322
Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467. https://doi.org/10.1016/j.tplants.2012.04.006
Wheal M, Fowles T, Palmer L (2011) A cost-effective acid digestion method using closed polypropylene tubes for inductively coupled plasma optical emission spectrometry (ICP-OES) analysis of plant essential elements. Anal Methods 3:2854–2863. https://doi.org/10.1039/c1ay05430a
Xie J, Shi H, Du Z, Wang T, Liu X, Chen S (2016) Comparative genomic and functional analysis reveal conservation of plant growth promoting traits in Paenibacillus polymyxa and its closely related species. Sci Rep 6:21329. https://doi.org/10.1038/srep21329
Xing Y, Du X, Xu X, Wang F, Jiang Y, Tian G, Zhu Z, Ge S, Jiang Y (2022) A balance between calcium and nitrate promotes the growth of M9T337 apple rootstocks. Sci Hortic 300:111063. https://doi.org/10.1016/j.scienta.2022.111063
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4. https://doi.org/10.1016/j.tplants.2008.10.004
Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G et al (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114. https://doi.org/10.1023/a:1004269902246
Zhang C, Yu Z, Zhang M, Li X, Wang M, Li L, Li X, Ding Z, Tian H (2022) Serratia marcescens PLR enhances lateral root formation through supplying PLR-derived auxin and enhancing auxin biosynthesis in Arabidopsis. J Exp Bot 73:3711–3725. https://doi.org/10.1093/jxb/erac074
Zhao CZ, Huang J, Gyaneshwar P, Zhao D (2018) Rhizobium sp. IRBG74 Alters Arabidopsis Root Development by Affecting Auxin Signaling. Front Microbiol 8:2556. https://doi.org/10.3389/fmicb.2017.02556
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632. https://doi.org/10.1104/pp.104.046367
Acknowledgements
We especially thank A & L Canada Laboratories Inc. and Dr. Soledad Saldías for completing the nutritional analysis of the samples. We also thank Dr. Delphine Capela for kindly providing us with the nifH mutant strain (CBM2568).
Funding
ANID PIA/BASAL FB0002 supported this work as, as did the ANID-Millennium Science Initiative Program— NCN2021_010, ANID PIA/ANILLOS ACT210052, ANID-FONDECYT 1211894, and ANID-FONDECYT 1230472. In addition, DR was supported by the ANID scholarship 2117145.
Author information
Authors and Affiliations
Contributions
DR and MJP conceived the experimental strategies. DR and NC performed the experiments throughout the manuscript and collected the data. DR, TL, AV, and MJP generally interpreted the results, analyzed the data, and generated the graphics. All authors contributed to data interpretation and discussion and edited the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted without any commercial or financial relationships that could potentially create a conflict of interest.
Additional information
Responsible Editor: Katharina Pawlowski.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ruiz, D., Céspedes-Bernal, N., Vega, A. et al. Nitrogen-modulated effects of the diazotrophic bacterium Cupriavidus taiwanensis on the non-nodulating plant Arabidopsis thaliana. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06736-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06736-1