Abstract
In bacteria, sigma factors are crucial in determining the plasticity of core RNA polymerase (RNAP) while promoter recognition during transcription initiation. This process is modulated through an intricate regulatory network in response to environmental cues. Previously, an extracytoplasmic function (ECF) sigma factor, AlgU, was identified to positively influence the fitness of Pseudomonas aeruginosa PGPR2 during corn root colonization. In this study, we report that the inactivation of the algU gene encoded by PGPR2_23995 hampers the root colonization ability of PGPR2. An insertion mutant in the algU gene was constructed by allele exchange mutagenesis. The mutant strains displayed threefold decreased root colonization efficiency compared with the wild-type strain when inoculated individually and in the competition assay. The mutant strain was more sensitive to osmotic and antibiotic stresses and showed higher resistance to oxidative stress. On the other hand, the mutant strain showed increased biofilm formation on the abiotic surface, and the expression of the pelB and pslA genes involved in the biofilm matrix formation were up-regulated. In contrast, the expression of algD, responsible for alginate production, was significantly down-regulated in the mutant strain, which is directly regulated by the AlgU sigma factor. The mutant strain also displayed altered motility. The expression of RNA binding protein RsmA was also impeded in the mutant strain. Further, the transcript levels of genes associated with the type III secretion system (T3SS) were analyzed, which revealed a significant down-regulation in the mutant strain. These results collectively provide evidence for the regulatory role of the AlgU sigma factor in modulating gene expression during root colonization.
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References
Alm RA, Mattick JS (1995) Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol Microbiol 16:485–496. https://doi.org/10.1111/j.1365-2958.1995.tb02413.x
Alquéres S, Meneses C, Rouws L, Rothballer M, Baldani I, Schmid M, Hartmann A (2013) The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol Plant Microbe Interact 26:937–945. https://doi.org/10.1094/MPMI-12-12-0286-R
Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol 90:109–116. https://doi.org/10.1104/pp.90.1.109
Aspedon A, Palmer K, Whiteley M (2006) Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J Bacteriol 188:2721–2725. https://doi.org/10.1128/JB.188.7.2721-2725.2006
Balasubramanian D, Kong KF, Jayawardena SR, Leal SM, Sautter RT, Mathee K (2011) Co-regulation of beta-lactam resistance, alginate production and quorum sensing in Pseudomonas aeruginosa. J Med Microbiol 60:147–156. https://doi.org/10.1099/jmm.0.021600-0
Bao Z, Wei HL, Ma X, Swingle B (2020) Pseudomonas syringae AlgU downregulates flagellin gene expression, helping evade plant immunity. J Bacteriol 202:e00418-e419. https://doi.org/10.1128/JB.00418-19
Barahona E, Navazo A, Garrido-Sanz D et al (2016) Pseudomonas fluorescens F113 can produce a second flagellar apparatus, which is important for plant root colonization. Front Microbiol 7:1471. https://doi.org/10.3389/fmicb.2016.01471
Bordes P, Lavatine L, Phok K, Barriot R, Boulanger A, Castanie Cornet MP, Dejean G, Lauber E, Becker A, Arlat M, Gutierrez C (2011) Insights into the extracytoplasmic stress response of Xanthomonas campestris pv. campestris: Role and regulation of σE-dependent activity. J Bacteriol 193:246–264. https://doi.org/10.1128/JB.00884-10
Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait Barka E, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clément C, Baillieul F, Dorey S (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603. https://doi.org/10.1093/jxb/erq291
Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72:612–632. https://doi.org/10.1111/j.1365-2958.2009.06670.x
Burrowes E, Baysse C, Adams C, O’Gara F (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiol 152:405–418. https://doi.org/10.1099/mic.0.28324-0
Cheng CY, Shieh SY, Hsu CC, Yang MT (2008) Characterization and transcriptional analysis of an ECF sigma factor from Xanthomonas campestris pv. campestris. FEMS Microbiol Lett 289:250–257. https://doi.org/10.1111/j.1574-6968.2008.01392.x
Chevalier S, Bouffartigues E, Bazire A et al (2019) Extracytoplasmic function sigma factors in Pseudomonas aeruginosa. BBA Gene Regul Mech 1862:706–721. https://doi.org/10.1016/j.bbagrm.2018.04.008
Costerton JW, Lewandowski Z, DeBeer D, Caldwell D, Korber D, James G (1994) Biofilms, the customized microniche. J Bacteriol 176:2137–2142. https://doi.org/10.1128/jb.176.8.2137-2142.1994
da Silva Neto JF, Koide T, Gomes SL, Marques MV (2007) The single extracytoplasmic-function sigma factor of Xylella fastidiosa is involved in the heat shock response and presents an unusual regulatory mechanism. J Bacteriol 189:551–560. https://doi.org/10.1128/JB.00986-06
Damron FH, Goldberg JB (2012) Proteolytic regulation of alginate overproduction in Pseudomonas aeruginosa. Mol Microbiol 84:95–607. https://doi.org/10.1111/j.1365-2958.2012.08049.x
de Lorenzo V, Herrero M, Jakubzik U, Timmis KN (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative Eubacteria. J Bacteriol 172:6568–6572. https://doi.org/10.1128/jb.172.11.6568-6572.1990
del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837. https://doi.org/10.1093/jxb/erv099
Fan B, Carvalhais LC, Becker A, Fedoseyenko D, von Wirén N, Borriss R (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol 12:116. https://doi.org/10.1186/1471-2180-12-116
Ferrara S, Carloni S, Fulco R, Falcone M, Macchi R, Bertoni G (2015) Post-transcriptional regulation of the virulence-associated enzyme AlgC by the σ22-dependent small RNA ErsA of Pseudomonas aeruginosa. Environ Microbiol 17:199–214. https://doi.org/10.1111/1462-2920.12590
Firoved AM, Boucher JC, Deretic V (2002) Global genomic analysis of AlgU (σE)-dependent promoters (sigmulon) in Pseudomonas aeruginosa and implications for inflammatory processes in cystic fibrosis. J Bacteriol 184:1057–1064. https://doi.org/10.1128/jb.184.4.1057-1064.2002
Ghafoor A, Hay ID, Rehm BH (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246. https://doi.org/10.1128/AEM.00637-11
Hajam IA, Dar PA, Shahnawaz I, Jaume JC, Lee JH (2017) Bacterial flagellin-a potent immunomodulatory agent. Exp Mol Med 49:e373. https://doi.org/10.1038/emm.2017.172
Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108. https://doi.org/10.1038/nrmicro821
Helmann JD (2002) The extracytoplasmic function (ECF) sigma factors. Adv Microb Physiol 46:47–110. https://doi.org/10.1016/S0065-2911(02)46002-X
Hershberger CD, Ye RW, Parsek MR, Xie ZD, Chakrabarty AM (1995) The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E). Proc Natl Acad Sci USA 92:7941–7945. https://doi.org/10.1073/pnas.92.17.7941
Hybiske K, Ichikawa JK, Huang V, Lory SJ, Machen TE (2004) Cystic fibrosis airway epithelial cell polarity and bacterial flagellin determine host response to Pseudomonas aeruginosa. Cell Microbiol 6:49–63. https://doi.org/10.1046/j.1462-5822.2003.00342.x
Illakkiam D, Ponraj P, Shankar M, Muthusubramanian S, Rajendhran J, Gunasekaran P (2013) Identification and structure elucidation of a novel antifungal compound produced by Pseudomonas aeruginosa PGPR2 against Macrophomina phaseolina. Appl Biochem Biotechnol 171:2176–2185. https://doi.org/10.1007/s12010-013-0469-7
Intile PJ, Diaz MR, Urbanowski ML, Wolfgang MC, Yahr TL (2014) The AlgZR two-component system recalibrates the RsmAYZ posttranscriptional regulatory system to inhibit expression of the Pseudomonas aeruginosa type III secretion system. J Bacteriol 196:357–366. https://doi.org/10.1128/JB.01199-13
Keith LMW, Bender CL (1999) AlgT (σ22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181:7176–7184. https://doi.org/10.1128/JB.181.23.7176-7184.1999
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lyczak JB, Cannon CL, Pier GB (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194–222. https://doi.org/10.1128/cmr.15.2.194-222.2002
Martin DW, Holloway BW, Deretic V (1993) Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J Bacteriol 175:1153–1164. https://doi.org/10.1128/jb.175.4.1153-1164.1993
Martínez-Bueno MA, Tobes R, Rey M, Ramos JL (2002) Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PA01. Environ Microbiol 4:842–855. https://doi.org/10.1046/j.1462-2920.2002.00371.x
Martinez-Granero F, Navazo A, Barahona E, Redondo-Nieto M, Rivilla R, Martin M (2012) The Gac-Rsm and SadB signal transduction pathways converge on AlgU to downregulate motility in Pseudomonas fluorescens. PLoS ONE 7:e31765. https://doi.org/10.1371/journal.pone.0031765
Mavrodi DV, Joe A, Mavrodi OV et al (2011) Structural and functional analysis of the type III secretion system from Pseudomonas fluorescens Q8r1–96. J Bacteriol 193:177–189. https://doi.org/10.1128/JB.00895-10
Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136. https://doi.org/10.1146/annurev.micro.50.1.101
Murray TS, Kazmierczak BI (2006) FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J Bacteriol 188:6995–7004. https://doi.org/10.1128/JB.00790-06
Muriel C, Blanco-Romero E, Trampari E, Arrebola E, Dur´an D, Redondo-Nieto M, Malone JG, Mart´ın M, Rivilla R (2019) The diguanylate cyclase AdrA regulates flagellar biosynthesis in Pseudomonas fluorescens F113 through SadB. Sci Rep 9:8096. https://doi.org/10.1038/s41598-019-44554-z
Müsken M, Di Fiore S, Römling U, Häussler S (2010) A 96-well-plate-based optical method for the quantitative and qualitative evaluation of Pseudomonas aeruginosa biofilm formation and its application to susceptibility testing. Nat Protoc 5:1460. https://doi.org/10.1038/nprot.2010.110
Nelson KE, Weinel C, Paulsen IT et al (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808. https://doi.org/10.1046/j.1462-2920.2002.00366.x
Nithya C, Devi MG, Karutha Pandian S (2011) A novel compound from the marine bacterium Bacillus pumilus S6–15 inhibits biofilm formation in gram-positive and gram-negative species. Biofouling 27:519–528. https://doi.org/10.1080/08927014.2011.586127
Paget MS, Helmann JD (2003) The σ70 family of sigma factors. Genome Biol 4:203. https://doi.org/10.1186/gb-2003-4-1-203
Park SH, Bao Z, Butcher BG et al (2014) Analysis of the small RNA spf in the plant pathogen Pseudomonas syringae pv. tomato strain DC3000. Microbiol 160:941–953. https://doi.org/10.1099/mic.0.076497-0
Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Meth 72:157–165. https://doi.org/10.1016/j.mimet.2007.11.010
Pfeilmeier S, Saur IM, Rathjen JP, Zipfel C, Malone JG (2016) High levels of cyclic-di-GMP in plant-associated Pseudomonas correlate with evasion of plant immunity. Mol Plant Pathol 17:521–531. https://doi.org/10.1111/mpp.12297
Piromyou P, Songwattana P, Greetatorn T et al (2015) The type III secretion system (T3SS) is a determinant for rice-endophyte colonization by non-photosynthetic Bradyrhizobium. Microbes Environ 30:291–300. https://doi.org/10.1264/jsme2.ME15080
Potvin E, Sanschagrin F, Levesque R (2008) Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev 32:38–55. https://doi.org/10.1111/j.1574-6976.2007.00092.x
Qiu D, Eisinger VM, Rowen DW, Hongwei DY (2007) Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. P Natl Acad Sci USA 104:8107–8112. https://doi.org/10.1073/pnas.0702660104
Rainey PB (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1:243–257. https://doi.org/10.1046/j.1462-2920.1999.00040.x
Ramsey DM, Wozniak DJ (2005) Understanding the control of Pseudomonas aeruginosa alginate synthesis and the prospects for management of chronic infections in cystic fibrosis. Mol Microbiol 56:309–322. https://doi.org/10.1111/j.1365-2958.2005.04552.x
Rezzonico F, Binder C, Défago G, Moënne-Loccoz Y (2005) The type III secretion system of biocontrol Pseudomonas fluorescens KD targets the phytopathogenic Chromista Pythium ultimum and promotes cucumber protection. Mol Plant Microbe in 18:991–1001. https://doi.org/10.1094/MPMI-18-0991
Ruer S, Stender S, Filloux A, de Bentzmann S (2007) Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J Bacteriol 189:3547–3555. https://doi.org/10.1128/JB.00093-07
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Santos R, Hérouart D, Sigaud S, Touati D, Puppo A (2001) Oxidative burst in alfalfa Sinorhizobium meliloti symbiotic interaction. Mol Plant-Microbe in 14:86–89. https://doi.org/10.1094/MPMI.2001.14.1.86
Sarniguet A, Kraus J, Henkels MD, Muehlchen AM, Loper JE (1995) The sigma factor sigma s affects antibiotic production and biological control activity of Pseudomonas fluorescens Pf-5. Proc Natl Acad Sci USA 92:12255–12259. https://doi.org/10.1073/pnas.92.26.12255
Schmidt MA, Balsanelli E, Faoro H et al (2012) The type III secretion system is necessary for the development of a pathogenic and endophytic interaction between Herbaspirillum rubrisubalbicans and Poaceae. BMC Microbial 12:98. https://doi.org/10.1186/1471-2180-12-98
Schnider-Keel U, Lejbølle KB, Baehler E, Haas D, Keel C (2001) The Sigma Factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHA0. Appl Environ Microbiol 67:5683–5693. https://doi.org/10.1128/AEM.67.12.5683-5693.2001
Schreiber KJ, Desveaux D (2011) AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol Microbiol 80:364–377. https://doi.org/10.1111/j.1365-2958.2011.07571.x
Schurr MJ, Martin DW, Mudd MH, Deretic V (1994) Gene cluster controlling conversion to alginate-overproducing phenotype in Pseudomonas aeruginosa: functional analysis in a heterologous host and role in the instability of mucoidy. J Bacteriol 176:3375–3382. https://doi.org/10.1128/jb.176.11.3375-3382.1994
Schurr MJ, Yu H, Martinez-Salazar JM, Boucher JC, Deretic V (1996) Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol 178:4997–5004. https://doi.org/10.1128/jb.178.16.4997-5004.1996
Semmler AB, Whitchurch CB, Mattick JS (1999) A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145:2863–2873. https://doi.org/10.1099/00221287-145-10-2863
Shi XY, Dumenyo CK, Hernandez-Martinez R, Azad H, Cooksey DA (2007) Characterization of regulatory pathways in Xylella fastidiosa: Genes and phenotypes controlled by algU. Appl Environ Microbiol 73:6748–6756. https://doi.org/10.1128/AEM.01232-07
Shidore T, Dinse T, Öhrlein J, Becker A, Reinhold-Hurek B (2012) Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Enviro Microbiol 14:2775–2787. https://doi.org/10.1111/j.1462-2920.2012.02777.x
Sivakumar R, Ranjani J, Vishnu US et al (2019) Evaluation of INSeq to identify genes essential for Pseudomonas aeruginosa PGPR2 corn root colonization. G3. Genes Genom Genet 9:651–661. https://doi.org/10.1534/g3.118.200928
Songwattana P, Noisangiam R, Teamtisong K et al (2017) Type 3 secretion system (T3SS) of Bradyrhizobium sp. DOA9 and its roles in legume symbiosis and rice endophytic association. Front Microbiol 8:1810. doi:https://doi.org/10.3389/fmicb.2017.01810
Stacey SD, Pritchett CL (2016) Pseudomonas aeruginosa AlgU contributes to post-transcriptional activity by increasing rsmA expression in a mucA22 strain. J Bacteriol 198:1812–1826. https://doi.org/10.1128/JB.00133-16
Staroń A, Sofia HJ, Dietrich S, Ulrich LE, Liesegang H, Mascher T (2009) The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family. Mol Microbiol 74:557–581. https://doi.org/10.1111/j.1365-2958.2009.06870.x
Stover CK, Pham XQ, Erwin AL et al (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959. https://doi.org/10.1038/35023079
Vakulskas CA, Potts AH, Babitzke P, Ahmer BM, Romeo T (2015) Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev 79:193–224. https://doi.org/10.1128/MMBR.00052-14
Verhagen BWM, Trotel-Aziz P, Couderchet M, Höfte M, Aziz A (2010) Pseudomonas spp. induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260. https://doi.org/10.1093/jxb/erp295
West SEH, Schweizer HP, Dall C, Sample AK, Runyen-Janecky LJ (1994) Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148:81–86. https://doi.org/10.1016/0378-1119(94)90237-2
Wood LF, Leech AJ, Ohman DE (2006) Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: roles of σ22 (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62:412–426. https://doi.org/10.1111/j.1365-2958.2006.05390.x
Wood LF, Ohman DE (2009) Use of cell wall stress to characterize σ22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Mol Microbiol 72:183–201. https://doi.org/10.1111/j.1365-2958.2009.06635.x
Wu W, Badrane H, Arora S, Baker HV, Jin S (2004) MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J Bacteriol 186:7575–7585. https://doi.org/10.1128/JB.186.22.7575-7585.2004
Xie ZD, Hershberger CD, Shankar S, Ye RW, Chakrabarty AM (1996) Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J Bacteriol 178:4990–4996. https://doi.org/10.1128/jb.178.16.4990-4996.1996
Yang LY, Yang LC, Gan YL, Wang L, Zhao WZ, He YQ, Jiang W, Jiang BL, Tang JL (2018) Systematic functional analysis of sigma (s) factors in the phytopathogen Xanthomonas campestris reveals novel roles in the regulation of virulence and viability. Front Microbiol 9:1749. https://doi.org/10.3389/fmicb.2018.01749
Yi Y, de Jong A, Frenzel E, Kuipers OP (2017) Comparative transcriptomics of Bacillus mycoides strains in response to potato-root exudates reveals different genetic adaptation of endophytic and soil isolates. Front Microbial 8:1487. https://doi.org/10.3389/fmicb.2017.01487
Yu J, Peñaloza-Vázquez A, Chakrabarty AM, Bender CL (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33:712–720. https://doi.org/10.1046/j.1365-2958.1999.01516.x
Yu X, Lund SP, Greenwald JW et al (2014) Transcriptional analysis of the global regulatory networks active in Pseudomonas syringae during leaf colonization. Mbio 5:e01683-e1714. https://doi.org/10.1128/mBio.01683-14
Zhang N, Yang D, Wang D et al (2015) Whole transcriptomic analysis of the plant-beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 during enhanced biofilm formation regulated by maize root exudates. BMC Genomics 16:685. https://doi.org/10.1186/s12864-015-1825-5
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
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RS acknowledges the Council of Scientific and Industrial Research (CSIR) for providing Senior Research Fellowship (09/201/0416/2016-EMR-I). The UGC-CAS, NRCBS, DBT-IPLS, DST-PURSE, DST-FIST Programs of the School of Biological Sciences, Madurai Kamaraj University is gratefully acknowledged.
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Sivakumar, R., Gunasekaran, P. & Rajendhran, J. Extracytoplasmic sigma factor AlgU contributes to fitness of Pseudomonas aeruginosa PGPR2 during corn root colonization. Mol Genet Genomics 297, 1537–1552 (2022). https://doi.org/10.1007/s00438-022-01938-7
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DOI: https://doi.org/10.1007/s00438-022-01938-7