Abstract
Aims
To investigate phylogenetic and phenotypic diversity of resident chickpea-nodulating rhizobia from Australian cropping soils.
Methods
Eighty Mesorhizobium strains collected from across Australian cropping regions were analysed in a pot experiment to evaluate nodulation and symbiotic effectiveness (SE%) in chickpea plants. In vitro testing of these strains tolerant to specific stresses (pH, temperature, antibiotics, heavy metals and NaCl) was performed. In addition, phylogenetic analyses were carried out using16S-23S rRNA, atpD, recA, nodC and nifH.
Results
All strains were members of the genus Mesorhizobium based on phylogenies of 16-23S rRNA IGS and core genes. Strains with diverse 16S-23S rRNA IGS carried symbiosis genes that had high similarity to those in chickpea symbionts, suggesting the resident rhizobia in Australian soils may have acquired symbiotic traits from inoculant strains through horizontal gene transfer (HGT). Inoculation of chickpea revealed that variation in SE% among isolated strains was correlated with phylogenetic relatedness to the commercial inoculant strain Mesorhizobium ciceri CC1192. Strain A47 collected from Queensland gave the highest shoot biomass and two strains (A78 and A79) from Western Australia grew under acidic conditions (pH 4.4). In a field experiment, inoculation with four selected strains or strain CC1192 all increased shoot biomass compared with an uninoculated control; chickpea inoculated with strain A47 had the highest nodulation.
Conclusion
Australian cropping soils contain resident chickpea rhizobial genotypes that are genetically and phenotypically diverse, with some genotypes having equal or superior SE compared with the inoculant strain CC1192. This study provides evidence to support HGT of symbiosis genes in Australian soils, and has identified strains adapted to different environmental conditions.
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References
ABARES (2019) Australian crop report, Australian Bureau of Agricultural and Resource Economics and Sciences, Canberra, September. CC BY 4.0. https://doi.org/10.25814/5d71bf5551775
Alexandre A, Laranjo M, Oliveira S (2006) Natural populations of chickpea rhizobia evaluated by antibiotic resistance profiles and molecular methods. Microb Ecol 51:128–136. https://doi.org/10.1007/s00248-005-0085-3
Andrews M, De Meyer S, James EK, Stępkowski T, Hodge S, Simon MF, Young JPW (2018) Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes 9:321. https://doi.org/10.3390/genes9070321
Aserse AA, Räsänen LA, Assefa F, Hailemariam A, Lindström K (2012) Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol 35:120–131. https://doi.org/10.1016/j.syapm.2011.11.005
Bala A, Murphy P, Giller KE (2003) Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Mol Ecol 12:917–929. https://doi.org/10.1046/j.1365-294X.2003.01754.x
Batista JSS, Hungria M, Barcellos FG, Ferreira MC, Mendes IC (2007) Variability in Bradyrhizobium japonicum and B. elkanii seven years after introduction of both the exotic microsymbiont and the soybean host in a Cerrados soil. Microb Ecol 53:270–284. https://doi.org/10.1007/s00248-006-9149-2
Batista L, Tomasco I, Lorite MJ, Sanjuán J, Monza J (2013) Diversity and phylogeny of rhizobial strains isolated from Lotus uliginosus grown in Uruguayan soils. Appl Soil Ecol 66:19–28. https://doi.org/10.1016/j.apsoil.2013.01.009
Benjelloun I, Alami IT, Douira A, Udupa SM (2019) Phenotypic and genotypic diversity among symbiotic and non-symbiotic bacteria present in chickpea nodules in Morocco. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01885
Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I (2003) Stress-induced mutagenesis in bacteria. Science 300:1404–1409. https://doi.org/10.1126/science.1082240
Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton RC, Neto NE, de Fátima LM, De Faria SM, Sprent JI (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52. https://doi.org/10.1111/j.1365-294X.2009.04458.x
Bottomley P (1992) Ecology of Bradyrhizobium and Rhizobium. In: Stacey G, Burris R, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 293–348
Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 174:143–180. https://doi.org/10.1007/BF00032245
Broughton WJ, Perret X (1999) Genealogy of legume-Rhizobium symbioses. Curr Opin Plant Biol 2:305–311. https://doi.org/10.1016/S1369-5266(99)80054-5
Chen L, Figueredo A, Villani H, Michajluk J, Hungria M (2002) Diversity and symbiotic effectiveness of rhizobia isolated from field-grown soybean nodules in Paraguay. Biol Fertil Soils 35:448–457. https://doi.org/10.1007/s00374-002-0493-1
Corbin E, Brockwell J, Gault R (1977) Nodulation studies on chickpea (Cicer arietinum). Aust J Exp Agric 17:126–134. https://doi.org/10.1071/EA9770126
Davey AG, Simpson RJ (1990) Nitrogen fixation by subterranean clover at varying stages of nodule dehydration: I. carbohydrate status and short-term recovery of nodulated root respiration. J Exp Bot 41:1175–1187. https://doi.org/10.1093/jxb/41.9.1175
Degefu T, Wolde-meskel E, Frostegård Å (2011) Multilocus sequence analyses reveal several unnamed Mesorhizobium genospecies nodulating Acacia species and Sesbania sesban trees in Southern regions of Ethiopia. Syst Appl Microbiol 34:216–226. https://doi.org/10.1016/j.syapm.2010.09.006
Dekkiche S, Benguedouar A, Sbabou L, Taha K, Filali-Maltouf A, Béna G (2018) Chickpea (Cicer arietinum) is nodulated by unexpected wide diversity of Mesorhizobium species in Eastern Algeria. Arch Agron Soil Sci 64:285–297. https://doi.org/10.1080/03650340.2017.1346791
Denton MD, Coventry DR, Bellotti WD, Howieson JG (2000) Distribution, abundance and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii from alkaline pasture soils in South Australia. Aust J Exp Agri 40:25–35. https://doi.org/10.1071/EA99035
Denton MD, Coventry DR, Murphy PJ, Howieson JG, Bellotti WD (2002) Competition between inoculated and naturalized Rhizobium leguminosarum bv. trifolii for nodulation of annual clovers in alkaline soil. Aust J Agric Res 53:1019–1026. https://doi.org/10.1071/AR01138
Doignon-Bourcier F, Willems A, Coopman R, Laguerre G, Gillis M, de Lajudie P (2000) Genotypic characterization of Bradyrhizobium strains nodulating small Senegalese legumes by 16S–23S rRNA intergenic gene spacers and amplified fragment length polymorphism fingerprint analyses. Appl Environ Microbiol 66(9):3987–3997. https://doi.org/10.1128/AEM.66.9.3987-3997.2000
Drew EA, Ballard RA (2010) Improving N2 fixation from the plant down: compatibility of Trifolium subterraneum L. cultivars with soil rhizobia can influence symbiotic performance. Plant Soil 327:261–277. https://doi.org/10.1007/s11104-009-0052-8
Eardly BD, Young J, Selander R (1992) Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes. Appl Environ Microbiol 58:1809–1815. https://doi.org/10.1128/AEM.58.6.1809-1815.1992
Elias NV, Herridge DF (2015) Naturalised populations of mesorhizobia in chickpea (Cicer arietinum L.) cropping soils: effects on nodule occupancy and productivity of commercial chickpea. Plant Soil 387:233–249. https://doi.org/10.1007/s11104-014-2298-z
Ferreira MC, Hungria M (2002) Recovery of soybean inoculant strains from uncropped soils in Brazil. Field Crops Res 79:139–152. https://doi.org/10.1016/S0378-4290(02)00119-3
Furseth BJ, Conley SP, Ané J-M (2012) Soybean response to soil rhizobia and seed-applied rhizobia inoculants in Wisconsin. Crop Sci 52:339–344. https://doi.org/10.2135/cropsci2011.01.0041
Galli-Terasawa LV, Glienke-Blanco C, Hungria M (2003) Diversity of a soybean rhizobial population adapted to a Cerrados soil. World J Microbiol Biotechnol 19:933–939. https://doi.org/10.1023/B:WIBI.0000007324.50022.c0
Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JPW (2001) Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048. https://doi.org/10.1099/00207713-51-6-2037
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57(1):81–91. https://doi.org/10.1099/ijs.0.64483-0
GRDC (2017) Chickpea: GrowNotes southern July 2017, Grains Research and Development Corporation, Canberra, ACT, Australia. Available at https://grdc.com.au/resources-and-publications/grownotes/crop-agronomy/chickpea-southern-region-grownotes, Accessed 3 December 2020
Greenlon A, Chang PL, Damtew ZM, Muleta A, Carrasquilla-Garcia N, Kim D, Nguyen HP, Suryawanshi V, Krieg CP, Yadav SK, Patel JS, Mukherjee A, Udupa S, Benjelloun I, Thami-Alami I, Yasin M, Patil B, Singh S, Sarma BK, von Wettberg EJB, Kahraman A, Bukun B, Assefa F, Tesfaye K, Fikre A, Cook DR (2019) Global-level population genomics reveals differential effects of geography and phylogeny on horizontal gene transfer in soil bacteria. Proc Natl Acad Sci USA 116:15200–15209. https://doi.org/10.1073/pnas.1900056116
Gunnabo A, van Heerwaarden J, Geurts R, Wolde-Meskel E, Degefu T, Giller K (2020) Phylogeography and symbiotic effectiveness of rhizobia nodulating chickpea (Cicer arietinum L.) in Ethiopia. Microb Ecol. https://doi.org/10.1007/s00248-020-01620-8
Hartley E, Gemell L, Slattery J, Howieson J, Herridge D (2005) Age of peat-based lupin and chickpea inoculants in relation to quality and efficacy. Aust J Exp Agric 45:183–188. https://doi.org/10.1071/EA03158
Haskett TL, Terpolilli JJ, Bekuma A, O’Hara GW, Sullivan JT, Wang P, Ronson CW, Ramsay JP (2016) Assembly and transfer of tripartite integrative and conjugative genetic elements. Proc Natl Acad Sci USA 113:12268–12273. https://doi.org/10.1073/pnas.1613358113
Hill Y, Colombi E, Bonello E, Haskett T, Ramsay J, O’Hara G, Terpolilli J (2021) Evolution of diverse effective N2-fixing microsymbionts of Cicer arietinum following horizontal transfer of the Mesorhizobium ciceri CC1192 symbiosis integrative and conjugative element. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02558-20
Howieson JG, Dilworth MJ (2016) Working with rhizobia. Australian Centre for International Agricultural Research (ACIAR). Monograph No. 173, Canberra
Howieson J, Ewing M, D’antuono M (1988) Selection for acid tolerance in Rhizobium meliloti. Plant Soil 105:179–188
Jaiswal SK, Beyan SM, Dakora FD (2016) Distribution, diversity and population composition of soybean-nodulating bradyrhizobia from different agro-climatic regions in Ethiopia. Biol Fertil Soils 52:725–738. https://doi.org/10.1007/s00374-016-1108-6
Kaschuk G, Hungria M, Andrade DS, Campo RJ (2006) Genetic diversity of rhizobia associated with common bean (Phaseolus vulgaris L.) grown under no-tillage and conventional systems in Southern Brazil. Appl Soil Ecol 32:210–220. https://doi.org/10.1016/j.apsoil.2005.06.008
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Laguerre G, Mavingui P, Allard M-R, Charnay M-P, Louvrier P, Mazurier S-I, Rigottier-Gois L, Amarger N (1996) Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl Environ Microbiol 62:2029–2036. https://doi.org/10.1128/AEM.62.6.2029-2036.1996
Laguerre G, Louvrier P, Allard M-R, Amarger N (2003) Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Appl Environ Microbiol 69:2276–2283. https://doi.org/10.1128/AEM.69.4.2276-2283.2003
Laranjo M, Machado J, Young JPW, Oliveira S (2004) High diversity of chickpea Mesorhizobium species isolated in a Portuguese agricultural region. FEMS Microbiol Ecol 48:101–107. https://doi.org/10.1016/j.femsec.2003.12.015
Laranjo M, Alexandre A, Rivas R, Velázquez E, Young JPW, Oliveira S (2008) Chickpea rhizobia symbiosis genes are highly conserved across multiple Mesorhizobium species. FEMS Microbiol Ecol 66:391–400. https://doi.org/10.1111/j.1574-6941.2008.00584.x
Laranjo M, Young J, Oliveira S (2012) Multilocus sequence analysis reveals multiple symbiovars within Mesorhizobium species. Syst Appl Microbiol 35:359–367. https://doi.org/10.1016/j.syapm.2012.06.002
Lauter DJ, Munns DN, Clarkin KL (1981) Salt response of chickpea as influenced by N supply 1. Agron J 73:961–966. https://doi.org/10.2134/agronj1981.00021962007300060013x
Lemaire B, Dlodlo O, Chimphango S, Stirton C, Schrire B, Boatwright S, Honnay O, Smets E, Sprent J, James E (2015) Symbiotic diversity, specificity and distribution of rhizobia in native legumes of the Core Cape Subregion (South Africa). FEMS Microbiol Ecol 91:2–17. https://doi.org/10.1093/femsec/fiu024
López-Bellido RJ, López-Bellido L, Benítez-Vega J, Muñoz-Romero V, López-Bellido FJ, Redondo R (2011) Chickpea and faba bean nitrogen fixation in a Mediterranean rainfed vertisol: effect of the tillage system. Eur J Agron 34:222–230. https://doi.org/10.1016/j.eja.2011.01.005
Maatallah J, Berraho EB, Munoz S, Sanjuan J, Lluch C (2002) Phenotypic and molecular characterization of chickpea rhizobia isolated from different areas of Morocco. J Appl Microbiol 93:531–540. https://doi.org/10.1046/j.1365-2672.2002.01718.x
Martens M, Dawyndt P, Coopman R, Gillis M, De Vos P, Willems A (2008) Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int J Syst Evol Microbiol 58:200–214
McKnight T (1949) Efficiency of isolates of Rhizobium in the cowpea (Vigna unguiculata) group, with proposed additions to this group. Division of plant industry. Qld J Agric Sci 6:61–76
Mothapo NV, Grossman JM, Sooksa-Nguan T, Maul J, Bräuer SL, Shi W (2013) Cropping history affects nodulation and symbiotic efficiency of distinct hairy vetch (Vicia villosa Roth.) genotypes with resident soil rhizobia. Biol Fertil Soils 49:871–879. https://doi.org/10.1007/s00374-013-0781-y
Naamala J, Jaiswal SK, Dakora FD (2016) Antibiotics resistance in Rhizobium: type, process, mechanism and benefit for agriculture. Curr Microbiol 72:804–816. https://doi.org/10.1007/s00284-016-1005-0
Nandasena KG, O’Hara GW, Tiwari RP, Howieson JG (2006) Rapid in situ evolution of nodulating strains for Biserrula pelecinus L. through lateral transfer of a symbiosis island from the original mesorhizobial inoculant. Appl Environ Microbiol 72:7365–7367. https://doi.org/10.1128/AEM.00889-06
Nandasena KG, O’hara GW, Tiwari RP, Sezmiş E, Howieson JG (2007) In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ Microbiol 9:2496–2511. https://doi.org/10.1111/j.1462-2920.2007.01368.x
Ndungu SM, Messmer MM, Ziegler D, Gamper HA, Mészáros É, Thuita M, Vanlauwe B, Frossard E, Thonar C (2018) Cowpea (Vigna unguiculata L. Walp) hosts several widespread bradyrhizobial root nodule symbionts across contrasting agro-ecological production areas in Kenya. Agric Ecosyst Environ 261:161–171. https://doi.org/10.1016/j.agee.2017.12.014
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecol Packag 10:719
Peoples MB, Giller KE, Herridge DF, Vessey JK (2002) Limitations to biological nitrogen fixation as a renewable source of nitrogen for agriculture. In: Nitrogen Fixation: global Perspectives, TM Finan, MR O'Brian, DB Layzell, JK Vessey and W Newton (eds) CABI Publishing: Proceedings of 13th International Congress of nitrogen fixation, July 2–4, 2001 Hamilton, Canada, p 356–360 https://doi.org/10.1079/9780851995915.0356
Pérez-Yépez J, Armas-Capote N, Velázquez E, Pérez-Galdona R, Rivas R, León-Barrios M (2014) Evaluation of seven housekeeping genes for multilocus sequence analysis of the genus Mesorhizobium: resolving the taxonomic affiliation of the Cicer canariense rhizobia. Syst Appl Microbiol 37:553–559. https://doi.org/10.1016/j.syapm.2014.10.003
Rai R, Dash PK, Mohapatra T, Singh A (2012) Phenotypic and molecular characterization of indigenous rhizobia nodulating chickpea in India. Indian J Exp Biol 50(5):340–350
Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW (2006) Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62:723–734. https://doi.org/10.1111/j.1365-2958.2006.05396.x
Rayment GE, Lyons DJ (2011) Soil chemical methods: Australasia. CSIRO publishing, Clayton
Reeve W, Sullivan J, Ronson C, Tian R, Bräu L, Davenport K, Goodwin L, Chain P, Woyke T, Lobos E, Huntemann M, Pati A, Mavromatis K, Markowitz V, Ivanova N, Kyrpides N (2014) Genome sequence of the Lotus corniculatus microsymbiont Mesorhizobium loti strain R88B. Stand Genomic Sci 9:3. https://doi.org/10.1186/1944-3277-9-3
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
Rivas R, Laranjo M, Mateos P, Oliveira S, Martínez-Molina E, Velázquez E (2007) Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett Appl Microbiol 44:412–418. https://doi.org/10.1111/j.1472-765X.2006.02086.x
Santos MA, Vargas MA, Hungria M (1999) Characterization of soybean Bradyrhizobium strains adapted to the Brazilian savannas. FEMS Microbiol Ecol 30:261–272. https://doi.org/10.1016/S0168-6496(99)00065-3
Sawada H, Kuykendall LD, Young JM (2003) Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J Gen Appl Microbiol 49:155–179. https://doi.org/10.2323/jgam.49.155
Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50:11–16. https://doi.org/10.1007/s00284-004-4391-7
Slattery JF, Coventry DR, Slattery WJ (2001) Rhizobial ecology as affected by the soil environment. Aust J Exp Agric 41:289–298. https://doi.org/10.1071/EA99159
Slattery JF, Pearce DJ, Slattery WJ (2004) Effects of resident rhizobial communities and soil type on the effective nodulation of pulse legumes. Soil Biol Biochem 36:1339–1346. https://doi.org/10.1016/j.soilbio.2004.04.015
Sullivan JT, Ronson CW (1998) Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95:5145–5149. https://doi.org/10.1073/pnas.95.9.5145
Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW (1995) Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92:8985–8989. https://doi.org/10.1073/pnas.92.19.8985
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Tena W, Wolde-Meskel E, Degefu T, Walley F (2017) Genetic and phenotypic diversity of rhizobia nodulating chickpea (Cicer arietinum L.) in soils from southern and central Ethiopia. Can J Microbiol. https://doi.org/10.1139/cjm-2016-0776
Thies JE, Bohlool BB, Singleton PW (1992) Environmental effects on competition for nodule occupancy between introduced and indigenous rhizobia and among introduced strains. Can J Microbiol 38:493–500. https://doi.org/10.1139/m92-081
Torabian S, Farhangi-Abriz S, Denton MD (2019) Do tillage systems influence nitrogen fixation in legumes? A review. Soil Tillage Res 185:113–121
Turpin PE, Dhir VK, Maycroft KA, Rowlands C, Wellington EM (1992) The effect of Streptomyces species on the survival of Salmonella in soil. FEMS Microbiol Lett 101:271–280. https://doi.org/10.1016/0378-1097(92)90824-8
Unkovich MJ, Pate JS, Sanford P (1997) Nitrogen fixation by annual legumes in Australian Mediterranean agriculture. Aust J Agric Res 48:267–293. https://doi.org/10.1071/A96099
Unkovich M, Herridge D, Peoples M, Cadisch G, Boddey B, Giller K, Alves B, Chalk P (2008) Measuring plant-associated nitrogen fixation in agricultural systems. Australian Centre for International Agricultural Research (ACIAR), Canberra
Unkovich MJ, Baldock J, Peoples MB (2010) Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes. Plant Soil 329:75–89. https://doi.org/10.1007/s11104-009-0136-5
USDA N (2007) Statistix 8.0 user guide for the plant materials program. United State Department of Agriculture and National Resources Conservation Service
van Berkum P, Fuhrmann JJ (2000) Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 50(6):2165–2172. https://doi.org/10.1099/00207713-50-6-2165
Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197. https://doi.org/10.1023/A:1022367312851
Wielgoss S, Barrick JE, Tenaillon O, Cruveiller S, Chane-Woon-Ming B, Médigue C, Lenski RE, Schneider D (2011) Mutation rate inferred from synonymous substitutions in a long-term evolution experiment with Escherichia coli. G3:Genes, Genomes, Genetics 1:183–186. https://doi.org/10.1534/g3.111.000406
Willems A, Coopman R, Gillis M (2001) Comparison of sequence analysis of 16S–23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51:623–632. https://doi.org/10.1099/00207713-51-2-623
Yoon S-H, Ha S-m, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zahran HH, Abdel-Fattah M, Ahmad MS, Zaky AY (2003) Polyphasic taxonomy of symbiotic rhizobia from wild leguminous plants growing in Egypt. Folia Microbiol 48:510–520. https://doi.org/10.1007/BF02931333
Zhang J, Yang X, Guo C, de Lajudie P, Singh RP, Wang E, Chen W (2017) Mesorhizobium muleiense and Mesorhizobium gsp. Nov. are symbionts of Cicer arietinum L. in alkaline soils of Gansu. Northwest China Plant Soil 410:103–112. https://doi.org/10.1007/s11104-016-2987-x
Acknowledgements
This study was conducted under the support of Australia Awards John Allwright Fellowship Scholarship provided by Australian Centre for International Agricultural Research (ACIAR) project SMCN/2011/047. We acknowledge Dr Ian Riley for his insightful advice on scientific writing on improving our manuscript, Dr Jenna Malone and Dr Tijana Petrovic from the Weed Science Research Group, University of Adelaide for assisting in working with DNA samples for molecular analysis. We are grateful to anonymous reviewers for their constructive feedback, comments and suggestions.
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Financial support was obtained from Australia Awards John Allwright Fellowship Scholarship provided by Australian Centre for International Agricultural Research (project number SMCN/2011/047).
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Zaw, M., Rathjen, J.R., Zhou, Y. et al. Symbiotic effectiveness, ecological adaptation and phylogenetic diversity of chickpea rhizobia isolated from a large-scale Australian soil collection. Plant Soil 469, 49–71 (2021). https://doi.org/10.1007/s11104-021-05119-0
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DOI: https://doi.org/10.1007/s11104-021-05119-0