Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction

Hoff, G.; Arias, A. A.; Boubsi, Farah; Prsic, Jelena; Meyer, T.; Ibrahim, H. M. M.; Steels, Sébastien; Luzuriaga, P.; Legras, A.; Franzil, L.; Lequart-Pillon, M.; Rayon, C.; Osorio, V.; De Pauw, Edwin; Lara, Yannick; Deboever, Estelle; de Coninck, B.; Jacques, Philippe; Deleu, Magali; Petit, E.; van Wuytswinkel, O.; Ongena, Marc

doi:10.1128/mBio.01774-21

Article (Scientific journals)

Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction

Hoff, G.; Arias, A. A.; Boubsi, Farah et al.

2021 • In MBio, 12 (6)

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/267262

DOI
10.1128/mBio.01774-21

PubMed
34724831

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

mbio.01774-21.pdf

Publisher postprint (3.3 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Lipopeptides; Molecular crosstalk; Plant cell wall polymers; Plant immunity; Plant-microbe interactions; Article; Bacillus amyloliquefaciens; Bacillus pumilus; Bacillus subtilis; Bacillus velezensis; Escherichia coli

Abstract :

[en] Bacillus velezensis is considered as a model species belonging to the so-called Bacillus subtilis complex that evolved typically to dwell in the soil rhizosphere niche and establish an intimate association with plant roots. This bacterium provides protection to its natural host against diseases and represents one of the most promising biocontrol agents. However, the molecular basis of the cross talk that this bacterium establishes with its natural host has been poorly investigated. We show here that these plant-associated bacteria have evolved a polymer-sensing system to perceive their host and that, in response, they increase the production of the surfactin-type lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favored upon growth on root exudates and that this lipopeptide is a key component used by the bacterium to optimize biofilm formation, motility, and early root colonization. In this specific nutritional context, the bacterium also modulates qualitatively the pattern of surfactin homologues coproduced in planta and forms mainly variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. © 2021 Hoff et al.

Disciplines :

Microbiology

Author, co-author :

Hoff, G.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium, Ecology and Biodiversity, Department of Biology, Utrecht University, Utrecht, Netherlands

Arias, A. A.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium

Boubsi, Farah ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies

Prsic, Jelena ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies

Meyer, T.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium, UMR Ecologie Microbienne, University of Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, Villeurbanne, F-69622, France

Ibrahim, H. M. M.; Division of Plant Biotechnics, Department of Biosystems, Faculty of Bioscience Engineering, KU Leuven, Leuven, Belgium

Steels, Sébastien ; Université de Liège - ULiège > Département GxABT > Microbial, food and biobased technologies

Luzuriaga, P.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium

Legras, A.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium

Franzil, L.; Microbial Processes and Interactions, TERRA Teaching and Research Center, BioEcoAgro, Joint Research Unit, UMR transfrontalière 1158, University of Liège-Gembloux Agro-Bio Tech, Gembloux, Belgium

More authors (12 more)

Language :

English

Title :

Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction

Publication date :

2021

Journal title :

MBio

ISSN :

2161-2129

eISSN :

2150-7511

Publisher :

American Society for Microbiology

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Interreg France-Wallonie-Vlaanderen
FEDER - Fonds Européen de Développement Régional
F.R.S.-FNRS - Fonds de la Recherche Scientifique
KU Leuven - Catholic University of Leuven

Available on ORBi :

since 18 January 2022

Statistics

Number of views

161 (27 by ULiège)

Number of downloads

23 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Andrews JH, Harris RF. 2000. The ecology and biogeography of micoroorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180. https://doi.org/10.1146/annurev.phyto.38.1.145.
Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, Cho H, Karaoz U, Loqué D, Bowen BP, Firestone MK, Northen TR, Brodie EL. 2018. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480. https://doi.org/10.1038/s41564-018-0129-3.
Vieira S, Sikorski J, Dietz S, Herz K, Schrumpf M, Bruelheide H, Scheel D, Friedrich MW, Overmann J. 2020. Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands. ISME J 14: 463–475. https://doi.org/10.1038/s41396-019-0543-4.
Vacheron J, Desbrosses G, Bouffaud M-L, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C. 2013. Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. https://doi.org/10.3389/fpls.2013.00356.
Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL. 2018. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of bio-stimulants for sustainable agriculture. Front Plant Sci 9:1473. https://doi.org/10.3389/fpls.2018.01473.
Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM. 2014. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto -082712-102340.
Köhl J, Kolnaar R, Ravensberg WJ. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845. https://doi.org/10.3389/fpls.2019.00845.
van Loon LC, Bakker PAHM, Pieterse CMJ. 1998. Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. https://doi.org/10.1146/annurev.phyto.36.1.453.
Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B, Arpigny JL, Thonart P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9: 1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x.
Ongena M, Jacques P. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009.
Wu K, Fang Z, Guo R, Pan B, Shi W, Yuan S, Guan H, Gong M, Shen B, Shen Q. 2015. Pectin enhances bio-control efficacy by inducing colonization and secretion of secondary metabolites by Bacillus amyloliquefaciens SQY 162 in the rhizosphere of tobacco. PLoS One 10:e0127418. https://doi.org/10.1371/journal.pone.0127418.
Saxena AK, Kumar M, Chakdar H, Anuroopa N, Bagyaraj DJ. 2020. Bacillus species in soil as a natural resource for plant health and nutrition. J Appl Microbiol 128:1583–1594. https://doi.org/10.1111/jam.14506.
Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Süssmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R. 2007. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014. https://doi.org/10.1038/nbt1325.
Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R. 2009. Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140: 27–37. https://doi.org/10.1016/j.jbiotec.2008.10.011.
Molinatto G, Puopolo G, Sonego P, Moretto M, Engelen K, Viti C, Ongena M, Pertot I. 2016. Complete genome sequence of Bacillus amyloliquefaciens subsp. plantarum S499, a rhizobacterium that triggers plant defences and inhibits fungal phytopathogens. J Biotechnol 238:56–59. https://doi.org/10.1016/j.jbiotec.2016.09.013.
van Gestel J, Vlamakis H, Kolter R. 2015. From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol 13: e1002141. https://doi.org/10.1371/journal.pbio.1002141.
López D, Vlamakis H, Losick R, Kolter R. 2009. Paracrine signaling in a bacterium. Genes Dev 23:1631–1638. https://doi.org/10.1101/gad.1813709.
Aleti G, Lehner S, Bacher M, Compant S, Nikolic B, Plesko M, Schuhmacher R, Sessitsch A, Brader G. 2016. Surfactin variants mediate species-specific biofilm formation and root colonization in Bacillus. Environ Microbiol 18: 2634–2645. https://doi.org/10.1111/1462-2920.13405.
Pršic J, Ongena M. 2020. Elicitors of plant immunity triggered by beneficial bacteria. Front Plant Sci 11:594530. https://doi.org/10.3389/fpls.2020.594530.
Debois D, Fernandez O, Franzil L, Jourdan E, de Brogniez A, Willems L, Clément C, Dorey S, De Pauw E, Ongena M. 2015. Plant polysaccharides initiate underground crosstalk with bacilli by inducing synthesis of the immunogenic lipopeptide surfactin. Environ Microbiol Rep 7:570–582. https://doi.org/10.1111/1758-2229.12286.
Gage DJ. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300. https://doi.org/10.1128/MMBR.68.2.280-300.2004.
Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R. 2013. Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci U S A 110:E1621–E1630. https://doi.org/10.1073/pnas.1218984110.
Fan B, Wang C, Song X, Ding X, Wu L, Wu H, Gao X, Borriss R. 2018. Bacillus velezensis FZB42 in 2018: the gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol 9:2491. https://doi.org/10.3389/fmicb.2018.02491.
Mohnen D. 2008. Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277. https://doi.org/10.1016/j.pbi.2008.03.006.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:490–495. https://doi.org/10.1093/nar/gkt1178.
Fan B, Blom J, Klenk HP, Borriss R. 2017. Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis Form an “Operational Group B. amyloliquefaciens” within the B. subtilis species complex. Front Microbiol 8: 22. https://doi.org/10.3389/fmicb.2017.00022.
Nihorimbere V, Cawoy H, Seyer A, Brunelle A, Thonart P, Ongena M. 2012. Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79:176–191. https://doi.org/10.1111/j.1574-6941.2011.01208.x.
Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo JH. 2013. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15:848–864. https://doi.org/10.1111/j.1462-2920.2012.02860.x.
Grau RR, De Oña P, Kunert M, Leñini C, Gallegos-Monterrosa R, Mhatre E, Vileta D, Donato V, Hölscher T, Boland W, Kuipers OP, Kovács ÁT. 2015. A duo of potassium-responsive histidine kinases govern the multicellular destiny of Bacillus subtilis. mBio 6:e00581-15. https://doi.org/10.1128/mBio.00581-15.
Thérien M, Kiesewalter HT, Auria E, Charron-Lamoureux V, Wibowo M, Maróti G, Kovács ÁT, Beauregard PB. 2020. Surfactin production is not essential for pellicle and root-associated biofilm development of Bacillus subtilis. Biofilm 2:100021. https://doi.org/10.1016/j.bioflm.2020.100021.
Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11: 157–168. https://doi.org/10.1038/nrmicro2960.
Caramori T, Barillà D, Nessi C, Sacchi L, Galizzi A. 1996. Role of FlgM in sD-dependent gene expression in Bacillus subtilis. J Bacteriol 178:3113–3118. https://doi.org/10.1128/jb.178.11.3113-3118.1996.
Strieker M, Tanovic A, Marahiel MA. 2010. Nonribosomal peptide synthetases: structures and dynamics. Curr Opin Struct Biol 20:234–240. https://doi.org/10.1016/j.sbi.2010.01.009.
Süssmuth RD, Mainz A. 2017. Nonribosomal peptide synthesis—principles and prospects. Angew Chem Int Ed Engl 56:3770–3821. https://doi.org/10.1002/anie.201609079.
Diomandé SE, Nguyen-The C, Guinebretière MH, Broussolle V, Brillard J. 2015. Role of fatty acids in Bacillus environmental adaptation. Front Microbiol 6:813. https://doi.org/10.3389/fmicb.2015.00813.
Serror P, Sonenshein AL. 1996. CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol 178:5910–5915. https://doi.org/10.1128/jb.178.20.5910-5915.1996.
Dhali D, Coutte F, Arias AA, Auger S, Bidnenko V, Chataigné G, Lalk M, Niehren J, de Sousa J, Versari C, Jacques P. 2017. Genetic engineering of the branched fatty acid metabolic pathway of Bacillus subtilis for the overproduction of surfactin C14 isoform. Biotechnol J 12:1–10. https://doi .org/10.1002/biot.201600574.
Brinsmade SR, Kleijn RJ, Sauer U, Sonenshein AL. 2010. Regulation of CodY activity through modulation of intracellular branched-chain amino acid pools. J Bacteriol 192:6357–6368. https://doi.org/10.1128/JB.00937-10.
Cawoy H, Mariutto M, Henry G, Fisher C, Vasilyeva N, Thonart P, Dommes J, Ongena M. 2014. Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol Plant Microbe Interact 27:87–100. https://doi.org/10.1094/MPMI-09-13-0262-R.
Saijo Y, Po-iian Loo EP, Yasuda S. 2018. Pattern recognition receptors and signaling in plant–microbe interactions. Plant J 93:592–613. https://doi.org/10.1111/tpj.13808.
Waszczak C, Carmody M, Kangasjärvi J. 2018. Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236. https://doi.org/10.1146/ annurev-arplant-042817-040322.
Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosche M, Van Breusegem F, Kangasjärvi J. 2016. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67:3831–3844. https://doi.org/10.1093/jxb/erw080.
Ashtamker C, Kiss V, Sagi M, Davydov O, Fluhr R. 2007. Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco bright yellow-2 cells. Plant Physiol 143:1817–1826. https://doi.org/10.1104/pp.106.090902.
Bigeard J, Colcombet J, Hirt H. 2015. Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539. https://doi.org/10.1016/j.molp.2014.12.022.
Jourdan E, Henry G, Duby F, Dommes J, Barthélemy JP, Thonart P, Ongena M. 2009. Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact 22:456–468. https://doi.org/10.1094/MPMI-22-4-0456.
Henry G, Deleu M, Jourdan E, Thonart P, Ongena M. 2011. The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell Microbiol 13: 1824–1837. https://doi.org/10.1111/j.1462-5822.2011.01664.x.
Zipfel C, Oldroyd GED. 2017. Plant signalling in symbiosis and immunity. Nature 543:328–336. https://doi.org/10.1038/nature22009.
Schellenberger R, Touchard M, Clément C, Baillieul F, Cordelier S, Crouzet J, Dorey S. 2019. Apoplastic invasion patterns triggering plant immunity: plasma membrane sensing at the frontline. Mol Plant Pathol 20: 1602–1616. https://doi.org/10.1111/mpp.12857.
Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse CMJ, Pozo MJ, Ton J, van Dam NM, Conrath U. 2016. Recognizing plant defense priming. Trends Plant Sci 21:818–822. https://doi.org/10.1016/j.tplants.2016.07.009.
Levy A, Salas Gonzalez I, Mittelviefhaus M, Clingenpeel S, Herrera Paredes S, Miao J, Wang K, Devescovi G, Stillman K, Monteiro F, Rangel Alvarez B, Lundberg DS, Lu TY, Lebeis S, Jin Z, McDonald M, Klein AP, Feltcher ME, Rio TG, Grant SR, Doty SL, Ley RE, Zhao B, Venturi V, Pelletier DA, Vorholt JA, Tringe SG, Woyke T, Dangl JL. 2017. Genomic features of bacterial adaptation to plants. Nat Genet 50:138–150. https://doi.org/10.1038/s41588 -017-0012-9.
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.
Feng H, Zhang N, Du W, Zhang H, Liu Y, Fu R, Shao J, Zhang G, Shen Q, Zhang R. 2018. Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria bacillus amyloliquefaciens SQR9. Mol Plant Microbe Interact 31: 995–1005. https://doi.org/10.1094/MPMI-01-18-0003-R.
Zhang N, Yang D, Wang D, Miao Y, Shao J, Zhou X, Xu Z, Li Q, Feng H, Li S, Shen Q, Zhang R. 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.
Raaijmakers JM, de Bruijn I, Nybroe O, Ongena M. 2010. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. https://doi.org/10.1111/j.1574-6976.2010.00221.x.
Hayashi K, Ohsawa T, Kobayashi K, Ogasawara N, Ogura M. 2005. The H2O2 stress-responsive regulator PerR positively regulates srfA Expression in Bacillus subtilis. J Bacteriol 187:6659–6667. https://doi.org/10.1128/JB.187.19.6659-6667.2005.
Wolf D, Rippa V, Mobarec JC, Sauer P, Adlung L, Kolb P, Bischofs IB. 2016. The quorum-sensing regulator ComA from Bacillus subtilis activates transcription using topologically distinct DNA motifs. Nucleic Acids Res 44: 2160–2172. https://doi.org/10.1093/nar/gkv1242.
Mariappan A, Makarewicz O, Chen XH, Borriss R. 2012. Two-component response regulator DegU controls the expression of bacilysin in plant-growth-promoting bacterium bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol 22:114–125. https://doi.org/10.1159/000338804.
Zhi Y, Wu Q, Xu Y. 2017. Genome and transcriptome analysis of surfactin biosynthesis in Bacillus amyloliquefaciens MT45. Sci Rep 7:40976. https://doi.org/10.1038/srep40976.
Koumoutsi A, Chen XH, Vater J, Borriss R. 2007. DegU and YczE positively regulate the synthesis of bacillomycin D by Bacillus amyloliquefaciens strain FZB42. Appl Environ Microbiol 73:6953–6964. https://doi.org/10.1128/AEM.00565-07.
Konishi H, Hio M, Kobayashi M, Takase R, Hashimoto W. 2020. Bacterial chemotaxis towards polysaccharide pectin by pectin-binding protein. Sci Rep 10:3977. https://doi.org/10.1038/s41598-020-60274-1.
Muller DB, Schubert OT, Rost H, Aebersold R, Vorholt JA. 2016. Systems-level proteomics of two ubiquitous leaf commensals reveals complementary adaptive traits for phyllosphere colonization. Mol Cell Proteomics 15: 3256–3269. https://doi.org/10.1074/mcp.M116.058164.
Hossain MJ, Ran C, Liu K, Ryu C-MM, Rasmussen-Ivey CR, Williams MA, Hassan MK, Choi S-KK, Jeong H, Newman M, Kloepper JW, Liles MR. 2015. Deciphering the conserved genetic loci implicated in plant disease control through comparative genomics of Bacillus amyloliquefaciens subsp. Plantarum. Front Plant Sci 6:631. https://doi.org/10.3389/fpls.2015.00631.
Birkenbihl RP, Liu S, Somssich IE. 2017. Transcriptional events defining plant immune responses. Curr Opin Plant Biol 38:1–9. https://doi.org/10.1016/j.pbi.2017.04.004.
Huot B, Yao J, Montgomery BL, He SY. 2014. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287. https://doi.org/10.1093/mp/ssu049.
Trauth S, Bischofs IB. 2014. Ectopic integration vectors for generating fluorescent promoter fusions in Bacillus subtilis with minimal dark noise. PLoS One 9:e98360. https://doi.org/10.1371/journal.pone.0098360.
Bryksin AV, Matsumura I. 2010. Overlap extension PCR cloning: a simple and reliable way to create recombinant plasmids. Biotechniques 48: 463–465. https://doi.org/10.2144/000113418.
Jarmer H, Berka R, Knudsen S, Saxild HH. 2002. Transcriptome analysis documents induced competence of Bacillus subtilis during nitrogen limiting conditions. FEMS Microbiol Lett 206:197–200. https://doi.org/10.1111/j.1574-6968.2002.tb11009.x.
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021.
De Coster W, D'Hert S, Schultz DT, Cruts M, Van Broeckhoven C. 2018. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics 34:2666–2669. https://doi.org/10.1093/bioinformatics/bty149.
Antipov D, Korobeynikov A, McLean JS, Pevzner PA. 2016. HybridSPAdes: an algorithm for hybrid assembly of short and long reads. Bioinformatics 32:1009–1015. https://doi.org/10.1093/bioinformatics/btv688.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352.
Anders S, Pyl PT, Huber W. 2015. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169. https://doi.org/10.1093/bioinformatics/btu638.
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8.
Molinatto G, Franzil L, Steels S, Puopolo G, Pertot I, Ongena M. 2017. Key impact of an uncommon plasmid on bacillus amyloliquefaciens subsp. plantarum S499 developmental traits and lipopeptide production. Front Microbiol 8:17. https://doi.org/10.3389/fmicb.2017.00017.
Debois D, Ongena M, Cawoy H, De Pauw E. 2013. MALDI-FTICR MS imaging as a powerful tool to identify paenibacillus antibiotics involved in the inhibition of plant pathogens. J Am Soc Mass Spectrom 24:1202–1213. https://doi.org/10.1007/s13361-013-0620-2.
Carpita NC. 1984. Cell wall development in maize coleoptiles. Plant Physiol 76:205–212. https://doi.org/10.1104/pp.76.1.205.
Silva GB, Ionashiro M, Carrara TB, Crivellari AC, Tiné MAS, Prado J, Carpita NC, Buckeridge MS. 2011. Cell wall polysaccharides from fern leaves: evidence for a mannan-rich Type III cell wall in Adiantum raddianum. Phytochemistry 72:2352–2360. https://doi.org/10.1016/j.phytochem.2011.08.020.
Bisceglia N, Gravino M, Savatin D. 2015. Luminol-based assay for detection of immunity elicitor-induced hydrogen peroxide production in Arabidopsis thaliana leaves. Bio-Protocol 5:e1685. https://doi.org/10.21769/BioProtoc.1685.
Heerklotz H, Seelig J. 2000. Titration calorimetry of surfactant-membrane partitioning and membrane solubilization. Biochim Biophys Acta 1508: 69–85. https://doi.org/10.1016/S0304-4157(00)00009-5.
Van Bambeke F, Kerkhofs A, Schanck A, Remacle C, Sonveaux E, Tulkens PM, Mingeot-Leclercq M-P. 2000. Biophysical studies and intracellular destabilization of pH-sensitive liposomes. Lipids 35:213–223. https://doi.org/10.1007/BF02664772.
Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P. 2009. Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8:63. https://doi.org/10.1186/1475-2859-8-63.
Pandin C, Le Coq D, Deschamps J, Védie R, Rousseau T, Aymerich S, Briandet R. 2018. Complete genome sequence of Bacillus velezensis QST713: a biocontrol agent that protects Agaricus bisporus crops against the green mould disease. J Biotechnol 278:10–19. https://doi.org/10.1016/j.jbiotec.2018.04.014.
Serrano L, Manker D, Brandi F, Cali T. 2013. The use of Bacillus subtilis QST 713 and Bacillus pumilus QST 2808 as protectant fungicides in conventional application programs for black leaf streak control. Acta Hortic 986: 149–156. https://doi.org/10.17660/ActaHortic.2013.986.15.