Effects of inoculation of wheat (Triticum aestivum) with rhizosphere bacteria in Victoria, Australia
Merfat Ben Mahmud A B † , Grant J. Hollaway
C D and Ann C. Lawrie A *
A
B
C
D Present address:
† Merfat Ben Mahmud died in Libya in 2022 while this manuscript was being finalised. The manuscript is based on her research for her completed PhD thesis at RMIT University (Ben Mahmud 2008).
Handling Editor: M Denton
Abstract
Wheat (Triticum aestivum) is an important food crop around the world. Its value depends on high grain yield and high protein content, which requires large inputs of nitrogenous fertiliser.
The aim of this study was to test if inoculation with a N2-fixing bacterium could improve wheat yield and/or protein content.
RMBMTa1 bacteria were isolated from soil in a wheat field at Horsham, Victoria, Australia. Wheat was inoculated with this bacterium in pot and field experiments with three factors: (1) one treatment of N2-fixing bacterium with isolate RMBMTa1; (2) two N treatments (ammonium sulfate, AS; urea); and (3) four N fertiliser rates (1, 50, 100, 150 kg ha−1).
RMBMTa1 was closest (93%) to Paraburkholderia species based on 16S sequencing. In the pot trial, inoculated treatments had the greatest grain dry weight with 100 kg ha−1 AS, potentially doubling profit per hectare. In a field trial during a drought year, inoculation reduced grain weight by 9% but increased grain protein by 50%, with a maximum at 100 kg ha−1 AS, thus increasing its grading.
Inoculating with RMBMTa1 increased both grain yield and protein content when rainfall did not limit yield. Larger-scale coordinated trials of inoculation of wheat varieties with other such native bacteria are needed to test if they offer similar benefits across a range of farming conditions.
RMBMTa1 could potentially increase the value of the wheat crop while saving on input costs and pollution from nitrogenous fertiliser.
Keywords: inoculation, N2-fixing, nitrogen, Paraburkholderia, PGPR, protein, wheat, yield.
References
AEGIC (2023) Australian grain industry facts. Available at https://www.aegic.org.au/ [accessed 8 July 2024]
Agriculture Victoria (2020) Measuring and interpreting soil pH. Available at https://vro.agriculture.vic.gov.au/dpi/vro/vrosite.nsf/pages/soilhealth_measure_ph [accessed 7 January 2024]
Agriculture Victoria (2023) Growing wheat in Victoria. Available at https://agriculture.vic.gov.au/crops-and-horticulture/grains-pulses-and-cereals/growing-grains-pulses-and-cereals/growing-wheat-in-victoria [accessed 8 July 2024]
Ahmed MF, Kennedy IR, Choudhury ATMA (2014) Evaluation of phosphorus mobilization potentials of six bacterial strains from four insoluble phosphorus sources. Communications in Soil Science and Plant Analysis 45(17), 2341-2362.
| Crossref | Google Scholar |
Alemneh AA, Zhou Y, Ryder MH, Denton MD (2022) Soil environment influences plant growth-promotion traits of isolated rhizobacteria. Pedobiologia 90, 150785.
| Crossref | Google Scholar |
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25(17), 3389-3402.
| Crossref | Google Scholar | PubMed |
Angus JF (2001) Nitrogen supply and demand in Australian agriculture. Australian Journal of Experimental Agriculture 41(3), 277-288.
| Crossref | Google Scholar |
AOAC International (2023) Official methods of analysis of AOAC International. (Oxford University Press) Available at https://academic.oup.com/officialmethodsofanalysis-aoac [accessed 8 July 2024]
Australian Bureau of Statistics (2008) 7123.2.55.001 – Agricultural state profile, Victoria, 2006-07. Available at https://www.abs.gov.au/ausstats/abs@.nsf/mf/7123.2.55.001 [accessed 7 January 2024]
Azcón R (1989) Selective interaction between free-living rhizosphere bacteria and vesiculararbuscular mycorrhizal fungi. Soil Biology and Biochemistry 21(5), 639-644.
| Crossref | Google Scholar |
Azcón R (1993) Growth and nutrition of nodulated mycorrhizal and non-mycorrhizal Hedysarum coronarium as a result of treatment with fractions from a plant growth-promoting rhizobacteria. Soil Biology and Biochemistry 25(8), 1037-1042.
| Crossref | Google Scholar |
Balandreau J, Viallard V, Cournoyer B, Coenye T, Laevens S, Vandamme P (2001) Burkholderia cepacia Genomovar III is a common plant-associated bacterium. Applied and Environmental Microbiology 67(2), 982-985.
| Crossref | Google Scholar | PubMed |
Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biology and Fertility of Soils 30, 485-491.
| Crossref | Google Scholar |
Barrow NJ (2025) Phosphate solubilizing microorganisms; the modern philosopher’s stone. Plant and Soil 508, 21-28.
| Crossref | Google Scholar |
Bavec M, Bavec F, Varga B, Kovačević V (2002) Relationships among yield, its quality and components, in winter wheat (Triticum aestivum L.) cultivars affected by seeding rates. Die Bodenkultur 53(3), 143-151.
| Google Scholar |
Beavers RL, Hammermeister AM, Frick B, Astatkie T, Martin RC (2008) Spring wheat yield response to variable seeding rates in organic farming systems at different fertility regimes. Canadian Journal of Plant Science 88(1), 43-52.
| Crossref | Google Scholar |
Ben Mahmud M (2008) Effect of Burkholderia as biofertiliser on cereal productivity. PhD Thesis, RMIT University, Melbourne, Vic, Australia. Available at https://research-repository.rmit.edu.au/articles/thesis/Effect_of_Burkholderia_as_biofertiliser_on_cereal_productivity/27340674?file=50728917
Bernabeu PR, García SS, López AC, Vio SA, Carrasco N, Boiardi JL, Luna MF (2018) Assessment of bacterial inoculant formulated with Paraburkholderia tropica to enhance wheat productivity. World Journal of Microbiology and Biotechnology 34, 81.
| Crossref | Google Scholar | PubMed |
Beukes CW, Venter SN, Steenkamp ET (2021) The history and distribution of nodulating Paraburkholderia, a potential inoculum for Fynbos forage species. Grass and Forage Science 76, 10-32.
| Crossref | Google Scholar |
Bezrukova M, Kildibekova A, Shakirova F (2008) WGA reduces the level of oxidative stress in wheat seedlings under salinity. Plant Growth Regulation 54, 195-201.
| Crossref | Google Scholar |
Bohlool BB, Ladha JK, Garrity DP, George T (1992) Biological nitrogen fixation for sustainable agriculture: a perspective. Plant and Soil 141, 1-11.
| Crossref | Google Scholar |
Brown ME (1974) Seed and root bacterization. Annual Review of Phytopathology 12, 181-197.
| Crossref | Google Scholar |
Bulut S (2013a) Evaluation of yield and quality parameters of phosphorous-solubilizing and N-fixing bacteria inoculated in wheat (Triticum aestivum L.). Turkish Journal of Agriculture and Forestry 37(5), 545-554.
| Crossref | Google Scholar |
Bulut S (2013b) Evaluation of efficiency parameters of phosphorous-solubilizing and N-fixing bacteria inoculations in wheat (Triticum aestivum L.). Turkish Journal of Agriculture and Forestry 37(6), 734-743.
| Crossref | Google Scholar |
Bureau of Meteorology (2006) Drought intensifies over eastern and southern Australia as spring rains fail. Available at http://www.bom.gov.au/climate/drought/archive/20061103.shtml [accessed 8 July 2024]
Bureau of Meteorology (2024) Climate data online. Available at http://www.bom.gov.au/climate/data/ [accessed 8 July 2024]
Caballero-Mellado J, Martínez-Aguilar L, Paredes-Valdez G, Estrada-De los Santos P (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. International Journal of Systematic and Evolutionary Microbiology 54(4), 1165-1172.
| Crossref | Google Scholar | PubMed |
Chen S, Xiang X, Ma H, Penttinen P, Zhao J, Li H, Gao R, Zheng T, Fan G (2021) Straw mulching and nitrogen fertilization affect diazotroph communities in wheat rhizosphere. Frontiers in Microbiology 12, 658668.
| Crossref | Google Scholar | PubMed |
Chhetri G, Kim I, Kim J, So Y, Park S, Jung Y, Seo T (2023) Paraburkholderia tagetis sp. nov., a novel species isolated from roots of Tagetes patula enhances the growth and yield of Solanum lycopersicum L. (tomato). Frontiers in Microbiology 14, 1140484.
| Crossref | Google Scholar | PubMed |
Chun J, Oren A, Ventosa A, Christensen H, Ruiz Arahal D, Da Costa MS, Rooney AP, Yi H, Xu X-W, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. International Journal of Systematic and Evolutionary Microbiology 68(1), 461-466.
| Crossref | Google Scholar | PubMed |
Ciccillo F, Fiore A, Bevivino A, Dalmastri C, Tabacchioni S, Chiarini L (2002) Effects of two different application methods of Burkholderia ambifaria MCI 7 on plant growth and rhizospheric bacterial diversity. Environmental Microbiology 4(4), 238-245.
| Crossref | Google Scholar | PubMed |
Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environmental Microbiology 5(9), 719-729.
| Crossref | Google Scholar | PubMed |
Coenye T, Vandamme P, Govan JRW, LiPuma JJ (2001) Taxonomy and identification of the Burkholderia cepacia complex. Journal of Clinical Microbiology 39(10), 3427-3436.
| Crossref | Google Scholar | PubMed |
Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiology Ecology 63(1), 84-93.
| Crossref | Google Scholar |
Curtis BC (2002) Wheat in the world. In ‘Bread wheat: improvement and production’. (Eds BC Curtis, S Rajaram, H Gomez Macpherson). (Food and Agriculture Organization of the United Nations: Rome, Italy) Available at https://www.fao.org/3/y4011e/y4011e04.htm#bm04
Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Australian Journal of Plant Physiology 28(9), 871-879.
| Crossref | Google Scholar |
Dobritsa AP, Samadpour M. (2016) Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia. International Journal of Systematic and Evolutionary Microbiology 66(8), 2836-2846.
| Crossref | Google Scholar |
Donn S, Kirkegaard JA, Perera G, Richardson AE, Watt M (2015) Evolution of bacterial communities in the wheat crop rhizosphere. Environmental Microbiology 17(3), 610-621.
| Crossref | Google Scholar |
Elliott GN, Chen W-M, Bontemps C, Chou J-H, Young JPW, Sprent JI, James EK (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Annals of Botany 100(7), 1403-1411.
| Crossref | Google Scholar | PubMed |
Esmaeel Q, Miotto L, Rondeau M, Leclère V, Clément C, Jacquard C, Sanchez L, Barka EA (2018) Paraburkholderia phytofirmans PsJN-plants interaction: from perception to the induced mechanisms. Frontiers in Microbiology 9, 2093.
| Crossref | Google Scholar |
Estrada-De Los Santos P, Bustillos-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Applied and Environmental Microbiology 67(6), 2790-2798.
| Crossref | Google Scholar | PubMed |
Eze MO, Thiel V, Hose GC, George SC, Daniel R (2022) Bacteria-plant interactions synergistically enhance biodegradation of diesel fuel hydrocarbons. Communications Earth & Environment 3, 192.
| Crossref | Google Scholar |
Fan X, Hu H, Huang G, Huang F, Li Y, Palta J (2015) Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize. Plant and Soil 390, 337-349.
| Crossref | Google Scholar |
Fautz E, Reichenbach H (1980) A simple test for flexirubin-type pigments. FEMS Microbiology Letters 8(2), 87-91.
| Crossref | Google Scholar |
Fowler DB, Brydon J, Darroch BA, Entz MH, Johnston AM (1990) Environment and genotype influence on grain protein concentration of wheat and rye. Agronomy Journal 82(4), 655-664.
| Crossref | Google Scholar |
Fox AR, Soto G, Valverde C, Russo D, Lagares A, Jr, Zorreguieta Á, Alleva K, Pascuan C, Frare R, Mercado-Blanco J, Dixon R, Ayub ND (2016) Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940. Environmental Microbiology 18(10), 3522-3534.
| Crossref | Google Scholar | PubMed |
Frommel MI, Nowak J, Lazarovits G (1991) Growth enhancement and developmental modifications of in vitro grown potato (Solanum tuberosum spp. tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiology 96(3), 928-936.
| Crossref | Google Scholar | PubMed |
Gallart M, Paungfoo-Lonhienne C, Gonzalez A, Trueman SJ (2021) Nitrogen source influences the effect of plant growth-promoting rhizobacteria (PGPR) on Macadamia integrifolia. Agronomy 11(6), 1064.
| Crossref | Google Scholar |
Gallart M, Paungfoo-Lonhienne C, Trueman SJ (2022) Effects of a growth-promoting Paraburkholderia species on nitrogen acquisition by avocado seedlings. Scientia Horticulturae 295, 110767.
| Crossref | Google Scholar |
Gao Z-H, Ruan S-L, Huang Y-X, Lv Y-Y, Qiu L-H (2019) Paraburkholderia phosphatilytica sp. nov., a phosphate-solubilizing bacterium isolated from forest soil. International Journal of Systematic and Evolutionary Microbiology 69(1), 196-202.
| Crossref | Google Scholar | PubMed |
Ghimire D, Das S, Mueller ND, Creech CF, Santra D, Beanziger PS, Easterly AC, Mausti B, Maharjani B (2021) Effects of cultivars and nitrogen management on wheat grain yield and protein. Agronomy Journal 113(5), 4348-4368.
| Crossref | Google Scholar |
Giller KE, James EK, Ardley J, Unkovich MJ (2024) Science losing its way: examples from the realm of microbial N2-fixation in cereals and other non-legumes. Plant Soil 2024,.
| Crossref | Google Scholar |
Gillis M, Tran Van V, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. International Journal of Systematic and Evolutionary Microbiology 45(2), 274-289.
| Crossref | Google Scholar |
Gopalkrishnan S, Srinivas V, Vemula A, Samineni S, Rathore A (2018) Influence of diazotrophic bacteria on nodulation, nitrogen fixation, growth promotion and yield traits in five cultivars of chickpea. Biocatalysis and Agricultural Biotechnology 15, 35-42.
| Crossref | Google Scholar |
GrainCorp Ltd (2021) Wheat standards 2021–2022. Available at https://grains.graincorp.com.au/wp-content/uploads/2021/08/Wheat-Standards-2021-2022.pdf [accessed 8 July 2024]
Grains Australia (2023) 2024-2025 Wheat Variety Master List. Available at https://grainsaustralia.com.au/master-lists/wheat-variety-list#wheat-master-list/?view_4_page=1&view_4_filters=%5B%7B%22field%22%3A%22field_94%22%2C%22operator%22%3A%22in%22%2C%22value%22%3A%5B%22AH%22%5D%7D%2C%7B%22field%22%3A%22field_95%22%2C%22operator%22%3A%22in%22%2C%22value%22%3A%5B%22AH%22%5D%7D%2C%7B%22field%22%3A%22field_310%22%2C%22operator%22%3A%22in%22%2C%22value%22%3A%5B%22all%22%5D%7D%5D [accessed 6 June 2025]
Guimarães SL, Silva RA, Baldani JI, Baldani VLD, Döbereiner J (2000) Effects of the inoculation of endophytic diazotrophic bacteria on grain yield of two rice varieties (Guarani and CNA 8305) grown under field conditions. In ‘Nitrogen fixation: from molecules to crop productivity’. (Eds FO Pedrosa, M Hungria, G Yates, WE Newton) p. 431. (Kluwer: Dordrecht)
Gupta VVSR, Roper MM, Roget DK (2006) Potential for non-symbiotic N2-fixation in different agroecological zones of southern Australia. Australian Journal of Soil Research 44, 343-354.
| Crossref | Google Scholar |
Haahtela K, Laakso T, Nurmiaho-Lassila E-L, Korhonen TK (1988) Effects of inoculation of Poa pratensis and Triticum aestivum with root-associated, N2-fixing Klebsiella, Enterobacter and Azospirillum. Plant and Soil 106, 239-248.
| Crossref | Google Scholar |
Harvey RWS, Price TH (1967) The isolation of salmonellas from animal feedingstuffs. Journal of Hygiene 65(2), 237-244.
| Crossref | Google Scholar | PubMed |
Hasan N, Zainal Abidina NH (2024) Plant growth-promoting rhizobacteria and sustainable agriculture. In ‘Soil bacteria’. (Eds S Dheeman, MT Islam, D Egamberdieva, MN Siddiqui) pp. 253–287. (Springer: Singapore). 10.1007/978-981-97-3473-3_9
Hayes RC, Gupta VVSR, Li GD, Peoples MB, Rawnsley RP, Pembleton KG (2021) Contrasting soil microbial abundance and diversity on and between pasture drill rows in the third growing season after sowing. Renewable Agriculture and Food Systems 36(2), 163-172.
| Crossref | Google Scholar |
Hecht-Buchholz C (1998) The apoplast-habitat of endophytic dinitrogen-fixing bacteria and their significance for the nitrogen nutrition of nonleguminous plants. Zeitschrift fur Pflanzenernahrung und Bodenkunde 161(5), 509-520.
| Crossref | Google Scholar |
Hermenau R, Ishida K, Gama S, Hoffmann B, Pfeifer-Leeg M, Plass W, Mohr JF, Wichard T, Saluz H-P, Hertweck C (2018) Gramibactin is a bacterial siderophore with a diazeniumdiolate ligand system. Nature Chemical Biology 14, 841-843.
| Crossref | Google Scholar | PubMed |
Hermenau R, Mehl JL, Ishida K, Dose B, Pidot SJ, Stinear TP, Hertweck C (2019) Genomics-driven discovery of NO-donating diazeniumdiolate siderophores in diverse plant-associated bacteria. Angewandte Chemie International Edition 58(37), 13024-13029.
| Crossref | Google Scholar | PubMed |
Herridge DF, Giller KE, Jensen ES, Peoples MB (2022) Quantifying country-to-global scale nitrogen fixation for grain legumes II. Coefficients, templates and estimates for soybean, groundnut and pulses. Plant and Soil 474, 1-15.
| Crossref | Google Scholar |
Holford ICR, Doyle AD, Leckie CC (1992) Nitrogen response characteristics of wheat protein in relation to yield responses and their interactions with phosphorus. Australian Journal of Agricultural Research 43(5), 969-986.
| Crossref | Google Scholar |
Hoque MS, Broadhurst LM, Thrall PH (2011) Genetic characterization of root-nodule bacteria associated with Acacia salicina and A. stenophylla (Mimosaceae) across south-eastern Australia. International Journal of Systematic and Evolutionary Microbiology 61(2), 299-309.
| Crossref | Google Scholar | PubMed |
Hussain M, Asgheri Z, Tahir M, Ijaz M, Shahid M, Ali H, Sattar A (2016) Bacteria in combination with fertilizers improve growth, productivity and net returns of wheat (Triticum aestivum L.). Pakistan Journal of Agricultural Science 53(3), 633-645.
| Crossref | Google Scholar |
Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by microorganisms isolated from forest soils. Soil Biology and Biochemistry 24(4), 389-395.
| Crossref | Google Scholar |
Iwaki H, Hasegawa Y (2007) Degradation of 2-nitrobenzoate by Burkholderia terrae strain KU-15. Bioscience, Biotechnology, and Biochemistry 71(1), 145-151.
| Crossref | Google Scholar | PubMed |
Kapulnik Y, Okon Y, Henis Y (1985) Changes in root morphology of wheat caused by Azospirillum inoculation. Canadian Journal of Microbiology 31(10), 881-887.
| Crossref | Google Scholar |
Kaur C, Selvakumar G, Ganeshamurthy AN (2017) Burkholderia to Paraburkholderia: the journey of a plant-beneficial-environmental bacterium. In ‘Recent advances in applied microbiology’. (Ed P Shukla) pp. 213–228. (Springer Nature: Singapore) 10.1007/978-981-10-5275-0_10
Kennedy IR (2003) Symposium summary and future perspectives. Symbiosis 35(1–3), 271-278.
| Google Scholar |
Kennedy IR, Islam N (2001) The current and potential contribution of asymbiotic nitrogen fixation to nitrogen requirements on farms: a review. Australian Journal of Experimental Agriculture 41(3), 447-457.
| Crossref | Google Scholar |
Kennedy IR, Choudhury ATMA, Kecskés ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biology and Biochemistry 36(8), 1229-1244.
| Crossref | Google Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7), 1870-1874.
| Crossref | Google Scholar | PubMed |
Ladha JK, Tirol-Padre A, Reddy CK, Cassman KG, Verma S, Powlson DA, van Kessel C, Richter DdB, Chakraborty D, Pathak H (2016) Global nitrogen budgets in cereals: a 50-year assessment for maize, rice and wheat production systems. Scientific Reports 6, 19355.
| Crossref | Google Scholar | PubMed |
Lemon J (2007) Nitrogen management for wheat protein and yield in the Esperance port zone. Department of Agriculture and Food Bulletin 4707, Western Australia, Perth. Available at https://researchlibrary.agric.wa.gov.au/bulletins
Lin T-F, Huang H-I, Shen F-T, Young C-C (2006) The protons of gluconic acid are the major factor responsible for the dissolution of tricalcium phosphate by Burkholderia cepacia CC-A174. Bioresource Technology 97(7), 957-960.
| Crossref | Google Scholar | PubMed |
Liu M, Philp J, Wang Y, Hu J, Wei Y, Li J, Ryder M, Toh R, Zhou Y, Denton MD, Wu Y, Yang H (2022) Plant growth-promoting rhizobacteria Burkholderia vietnamiensis B418 inhibits root-knot nematode on watermelon by modifying the rhizosphere microbial community. Scientific Reports 12, 8381.
| Crossref | Google Scholar | PubMed |
Mahenthiralingam E, Bischof J, Byrne SK, Radomski C, Davies JE, Av-Gay Y, Vandamme P (2000) DNA-based diagnostic approaches for identification of Burkholderia cepacia complex, Burkholderia vietnamiensis, Burkholderia multivorans, Burkholderia stabilis, and Burkholderia cepacia genomovars I and III. Journal of Clinical Microbiology 38(9), 3165-3173.
| Crossref | Google Scholar | PubMed |
Martínez-Aguilar L, Salazar-Salazar C, Méndez RD, Caballero-Mellado J, Hirsch AM, Vásquez-Murrieta MS, Estrada-De Los Santos P (2013) Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Antonie van Leeuwenhoek 104, 1063-1071.
| Crossref | Google Scholar |
Martínez-Toledo MV, Gonzalez-Lopez J, de la Rubia T, Ramos-Cormenzana A (1985) Isolation and characterization of Azotobacter chroococcum from the roots of Zea mays. FEMS Microbiology Ecology 1(4), 197-203.
| Crossref | Google Scholar |
Moreno-Ramos OH, Rodriguez-Casas J, Johnson D, Thompson TL (2004) Wheat response to population density and bed spacing in northwest Mexico. Cereal Research Communications 32, 273-279.
| Crossref | Google Scholar |
Mullins AJ, Mahenthiralingam E (2021) The hidden genomic diversity, specialized metabolite capacity, and revised taxonomy of Burkholderia sensu lato. Frontiers in Microbiology 12, 726847.
| Crossref | Google Scholar | PubMed |
Nakata PA (2002) The generation of a transposon-mutagenized Burkeholderia glumae library to isolate novel mutants. Plant Science 162(2), 267-271.
| Crossref | Google Scholar |
Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regulation 73, 121-131.
| Crossref | Google Scholar |
Nelson DR, Mele PM (2006) The impact of crop residue amendments and lime on microbial community structure and nitrogen-fixing bacteria in the wheat rhizosphere. Australian Journal of Soil Research 44(4), 319-329.
| Crossref | Google Scholar |
Omar MNA, Berge O, Hassanein EE, Shalan SN (1992) In vitro and in situ effects of herbicide thiobencarb on rice-Azospirillum association. Symbiosis 13, 55-63.
| Google Scholar |
Oren A, Garrity GM (2015) List of new names and new combinations previously effectively, but not validly, published. International Journal of Systematic and Evolutionary Microbiology 65, 2017-2025.
| Crossref | Google Scholar |
O’Connell PF (1992) Sustainable agriculture-a valid alternative. Outlook on Agriculture 21(1), 5-12.
| Crossref | Google Scholar |
Parker MA, Wurtz AK, Paynter Q (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biological Invasions 9, 127-138.
| Crossref | Google Scholar |
Parr JR, Papendick RI (1965) Retention of ammonia in soils. In ‘Agricultural anhydrous ammonia technology and use’. (Eds MH McVicker, WP Martin, IE Miles, HH Tucker) pp. 213–236. (Agricultural Ammonia Institute: Memphis, American Society of Agronomy: Madison, Soil Science Society of America: Madison) 10.2134/1966.nh3agricultural
Paulitsch F, Bueno dos Reis F, Jr, Hungria M (2021) Twenty years of paradigm-breaking studies of taxonomy and symbiotic nitrogen fixation by beta-rhizobia, and indication of Brazil as a hotspot of Paraburkholderia diversity. Archives of Microbiology 203, 4785-4803.
| Crossref | Google Scholar | PubMed |
Paungfoo-Lonhienne C, Lonhienne TGA, Yeoh YK, Webb RI, Lakshmanan P, Chan CX, Lim PE, Ragan MA, Schmidt S, Hugenholtz P (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microbial Biotechnology 7(2), 142-154.
| Crossref | Google Scholar | PubMed |
Paungfoo-Lonhienne C, Redding M, Pratt C, Wang W (2019) Plant growth promoting rhizobacteria increase the efficiency of fertilisers while reducing nitrogen loss. Journal of Environmental Management 233, 337-341.
| Crossref | Google Scholar | PubMed |
Peoples MB, Herridge DF, Ladha JK (1995) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant and Soil 174, 3-28.
| Crossref | Google Scholar |
Pereg Gerk L, Gilchrist K, Kennedy IR (2000) Mutants with enhanced nitrogenase activity in hydroponic Azospirillum brasilense-wheat associations. Applied and Environmental Microbiology 66(5), 2175-2184.
| Crossref | Google Scholar | PubMed |
Poonguzhali S, Madhaiyan M, Sa T (2007) Quorum-sensing signals produced by plant-growth promoting Burkholderia strains under in vitro and in planta conditions. Research in Microbiology 158(3), 287-294.
| Crossref | Google Scholar | PubMed |
Reis VM, Baldani JI, Baldani VLD, Döbereiner J (2000) Biological dinitrogen fixation in Gramineae and palm trees. Critical Reviews in Plant Science 19(3), 227-247.
| Crossref | Google Scholar |
Reis VM, Estrada-De los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VLD, Schmid M, Baldani JI, Balandreau J, Hartmann A, Cabellero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. International Journal of Systematic and Evolutionary Microbiology 54(6), 2155-2162.
| Crossref | Google Scholar |
Rojas-Rojas FU, Tapia-García EY, Maymon M, Humm E, Huntemann M, Clum A, Pillay M, Palaniappan K, Varghese N, Mikhailova N, Stamatis D, Reddy TBK, Markowitz V, Ivanova N, Kyrpides N, Woyke T, Shapiro N, Hirsch AM, Estrada-De los Santos P (2017) Draft genome of Paraburkholderia caballeronis TNe-841T, a free-living, nitrogen-fixing, tomato plant-associated bacterium. Standards in Genomic Sciences 12, 80.
| Crossref | Google Scholar | PubMed |
Rojas-Rojas FU, Gómez-Vázquez IM, Estrada de los Santos P, Shimade-Beltrán H, Vega-Arreguín JC (2025) The potential of Paraburkholderia species to enhance crop growth. World Journal of Microbiology and Biotechnology 41, 62.
| Crossref | Google Scholar | PubMed |
Sakai Y, Ogawa N, Fujii T, Sugahara K, Miyashihta K, Hasebe A (2007) 2,4-dichrolophenoxyacetic acid-degrading genes from bacteria isolated from soil in Japan: spread of Burkholderia cepacia RASC-type degrading genes harbored on large plasmids. Microbes and Environments 22(2), 145-156.
| Crossref | Google Scholar |
Salles JF, De Souza FA, Van Elsas JD (2002) Molecular method to assess the diversity of Burkholderia species in environmental samples. Applied and Environmental Microbiology 68(4), 1595-1603.
| Crossref | Google Scholar | PubMed |
Sarita S, Priefer UB, Prell J, Sharma PK (2008) Diversity of nifH gene amplified from rhizosphere soil DNA. Current Science 94(1), 109-115 Available at https://eurekamag.com/research/018/767/018767147.php.
| Google Scholar |
Sawana A, Adeolu M, Gupta RS (2014) 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. Frontiers in Genetics 5, 429.
| Crossref | Google Scholar | PubMed |
Sessitsch A, Coenye T, Sturz AV, Vandamme P, Ait Barka E, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. International Journal of Systematic and Evolutionary Microbiology 55(3), 1187-1192.
| Crossref | Google Scholar | PubMed |
Shaharoona B, Jamro GM, Zahir ZA, Arshad M, Memon KS (2007) Effectiveness of various Pseudomonas spp. and Burkholderia caryophylli containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.). Journal of Microbiology and Biotechnology 17(8), 1300-1307.
| Google Scholar | PubMed |
Singh AA, Singh AK (2025) Role of bacterial quorum sensing in plant growth promotion. World Journal of Microbiology and Biotechnology 41, 18.
| Crossref | Google Scholar |
Tago K, Sekiya E, Kiho A, Katsuyama C, Hosshito Y, Yamada N, Hirano K, Sawada H, Hayatsu M (2006) Diversity of fenitrothion-degrading bacteria in soils from distant geographical areas. Microbes and Environments 21(1), 58-64.
| Crossref | Google Scholar |
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10(3), 512-526.
| Crossref | Google Scholar | PubMed |
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22(22), 4673-4680.
| Crossref | Google Scholar | PubMed |
Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Applied and Environmental Microbiology 37(5), 1016-1024.
| Crossref | Google Scholar | PubMed |
Timofeeva AM, Galyamova MR, Sedykh SE (2023) Plant growth-promoting soil bacteria: nitrogen fixation, phosphate solubilization, siderophore production, and other biological activities. Plants 12(24), 4074.
| Crossref | Google Scholar | PubMed |
Too CC, Ong KS, Yule CM, Keller A (2021) Putative roles of bacteria in the carbon and nitrogen cycles in a tropical peat swamp forest. Basic and Applied Ecology 52, 109-123.
| Crossref | Google Scholar |
Trân Van V, Berge O, Balandreau J, Heulin T, Ngô Kê S (1996) Isolation and nitrogenase activity of Burkholderia vietnamiensis, a nitrogen-fixing bacterium associated with rice (Oryza sativa L.) on an acid sulphate soil of Vietnam. Agronomie 16(8), 479-491.
| Crossref | Google Scholar |
Trân Van V, Berge O, Ngô Kê S, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensison early and late yield components in low fertility sulphate acid soils of Vietnam. Plant and Soil 218, 273-284.
| Crossref | Google Scholar |
Ulrich RL (2004) Quorum quenching: enzymatic disruption of N-acylhomoserine lactone-mediated bacterial communication in Burkholderia thailandensis. Applied and Environmental Microbiology 70(10), 6173-6180.
| Crossref | Google Scholar | PubMed |
Unkovich M, Herridge D, James EK, Giller K, Peoples MB (2020) Reliable quantification of N2 fixation by non-legumes remains problematic. Nutrient Cycling in Agroecosystems 118, 223-225.
| Crossref | Google Scholar |
Vance CP (1997) Enhanced agricultural sustainability through biological nitrogen fixation. In ‘Biological fixation of nitrogen for ecology and sustainable agriculture’. NATO ASI Series, Vol. 39. (Eds A Legocki, H Bothe, A Puhler) pp. 179–185. (Springer-Verlag: Berlin, Germany) Available at https://link.springer.com/chapter/10.1007/978-3-642-59112-9_36
Vandamme P, Goris J, Chen W-M, Vos PD, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Systematic and Applied Microbiology 25(4), 507-512.
| Crossref | Google Scholar |
Viallard V, Poirier I, Cournoyer B, Haurat J, Wiebkin S, Ophel-Keller K, Balandreau J (1998) Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia. International Journal of Systematic and Evolutionary Microbiology 48, 549-563.
| Crossref | Google Scholar | PubMed |
Walley FL, Germida JJ (1997) Response of spring wheat (Triticum aestivum) to interactions between Pseudomonas species and Glomus clarum NT4. Biology and Fertility of Soils 24, 365-371.
| Crossref | Google Scholar |
Walsh OS, Torrion JA, Liang X, Shafian S, Yang R, Belmont KM, McClintick-Chess JR (2020) Grain yield, quality, and spectral characteristics of wheat grown under varied nitrogen and irrigation. Agrosystems, Geosciences & Environment 3(1), e20104.
| Crossref | Google Scholar |
Weisburg WG, Barns SM, Pelletier DA, Lae DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173(2), 697-703.
| Crossref | Google Scholar | PubMed |
Wilson MS, Herrick JB, Jeon CO, Hinman DE, Madsen EL (2003) Horizontal transfer of phnAc dioxygenase genes within one of two phenotypically and genotypically distinctive naphthalene-degrading guilds from adjacent soil environments. Applied and Environmental Microbiology 69(4), 2172-2181.
| Crossref | Google Scholar | PubMed |
Yates IE, Sparks D (2008) Fusarium verticillioides dissemination among maize ears of field-grown plants. Crop Protection 27(3–5), 606-613.
| Crossref | Google Scholar |
Yegorenkova IV, Tregubova KV, Burygin GL, Matora LY, Ignatov VV (2016) Assessing the efficacy of co-inoculation of wheat seedlings with the associative bacteria Paenibacillus polymyxa 1465 and Azospirillum brasilense Sp245. Canadian Journal of Microbiology 62(3), 279-285.
| Crossref | Google Scholar | PubMed |
