Pectic homogalacturonan sensed by Bacillus acts as host associated cue to promote establishment and persistence in the rhizosphere.

Boubsi, Farah; Hoff, Grégory; Arguelles Arias, Anthony; Steels, Sébastien; Andric, Sofija; Anckaert, Adrien; Roulard, Romain; Rigolet, Augustin; van Wuytswinkel, Olivier; Ongena, Marc

doi:10.1016/j.isci.2023.107925

Article (Scientific journals)

Pectic homogalacturonan sensed by Bacillus acts as host associated cue to promote establishment and persistence in the rhizosphere.

Boubsi, Farah; Hoff, Grégory; Arguelles Arias, Anthony et al.

2023 • In iScience, 26 (10), p. 107925

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/313873

DOI
10.1016/j.isci.2023.107925

PubMed
37790276

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Boubsi et al iScience 2023.pdf

Author postprint (5.18 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Plant biology; Plant development; Process in plant; Multidisciplinary

Abstract :

[en] Bacillus velezensis isolates are among the most promising plant-associated beneficial bacteria used as biocontrol agents. However, various aspects of the chemical communication between the plant and these beneficials, determining root colonization ability, remain poorly described. Here we investigated the molecular basis of such interkingdom interaction occurring upon contact between Bacillus velezensis and its host via the sensing of pectin backbone homogalacturonan (HG). We showed that B. velezensis stimulates key developmental traits via a dynamic process involving two conserved pectinolytic enzymes. This response integrates transcriptional changes leading to the switch from planktonic to sessile cells, a strong increase in biofilm formation, and an accelerated sporulation dynamics while conserving the potential to efficiently produce specialized secondary metabolites. As a whole, we anticipate that this response of Bacillus to cell wall-derived host cues contributes to its establishment and persistence in the competitive rhizosphere niche and ipso facto to its activity as biocontrol agent.

Disciplines :

Microbiology

Author, co-author :

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

Hoff, Grégory ; Université de Liège - ULiège > Département GxABT > Microbial technologies

Arguelles Arias, Anthony; Microbial Processes and Interactions, TERRA Teaching and Research Center, University of Liège - Gembloux Agro-Bio Tech, 5030 Gembloux, Belgium

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

Andric, Sofija ; Université de Liège - ULiège > Département GxABT > Microbial technologies

Anckaert, Adrien ; Université de Liège - ULiège > TERRA Research Centre

Roulard, Romain; UMRT INRAe 1158 Plant Biology and Innovation, University of Picardie Jules Verne, UFR des Sciences, 80039 Amiens, France

Rigolet, Augustin ; Université de Liège - ULiège > Département GxABT > Microbial technologies

van Wuytswinkel, Olivier; UMRT INRAe 1158 Plant Biology and Innovation, University of Picardie Jules Verne, UFR des Sciences, 80039 Amiens, France

Ongena, Marc ; Université de Liège - ULiège > Département GxABT

Language :

English

Title :

Pectic homogalacturonan sensed by Bacillus acts as host associated cue to promote establishment and persistence in the rhizosphere.

Publication date :

20 October 2023

Journal title :

iScience

eISSN :

2589-0042

Publisher :

Elsevier Inc., United States

Volume :

Issue :

Pages :

107925

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S2589004223020023?httpAccept=text/xml

Funding text :

This work was supported by the PDR research project ID 26084552 from the F.R.S.-FNRS (National fund for Scientific Research in Belgium) and by the EOS project ID 30650620 from the FWO/F.R.S.-FNRS. F.B. A.A. and A.R. are recipient of an F.R.I.A. fellowship (F.R.S.-FNRS) and MO is Research Director at the F.R.S.-FNRS. We gratefully acknowledge Emmanuel Petit for providing the oligogalacturonides of high polymerization degree and Catherine Helmus for technical help. F.B. and M.O. conceived, designed, and coordinated the project. F.B. G.H. A.A.A. S.S. S.A. A.A. R.R. A.R. and O.V.W. generated materials, performed experiments, and/or analyzed data. F.B. and M.O. wrote the manuscript. O.V.W. A.A. and G.H. revised the manuscript. O.V.W. and G.H. were involved in the discussion of the work. The authors declare no competing interests.This work was supported by the PDR research project ID 26084552 from the F.R.S.- FNRS ( National fund for Scientific Research in Belgium ) and by the EOS project ID 30650620 from the FWO/F.R.S.- FNRS . F.B., A.A., and A.R. are recipient of an F.R.I.A. fellowship (F.R.S.- FNRS ) and MO is Research Director at the F.R.S.- FNRS . We gratefully acknowledge Emmanuel Petit for providing the oligogalacturonides of high polymerization degree and Catherine Helmus for technical help.

Available on ORBi :

since 03 March 2024

Statistics

Number of views

7 (3 by ULiège)

Number of downloads

4 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

Bibliography

Prashar, P., Kapoor, N., Sachdeva, S., Rhizosphere: Its structure, bacterial diversity and significance. Rev. Environ. Sci. Biotechnol. 13 (2014), 63–77, 10.1007/S11157-013-9317-Z.
Mendes, R., Garbeva, P., Raaijmakers, J.M., The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37 (2013), 634–663, 10.1111/1574-6976.12028.
Müller, D.B., Vogel, C., Bai, Y., Vorholt, J.A., The Plant Microbiota: Systems-Level Insights and Perspectives. Annu. Rev. Genet. 50 (2016), 211–234, 10.1146/annurev-genet-120215-034952.
Vives-Peris, V., de Ollas, C., Gómez-Cadenas, A., Pérez-Clemente, R.M., Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep. 39 (2020), 3–17, 10.1007/s00299-019-02447-5.
Wang, N., Wang, L., Zhu, K., Hou, S., Chen, L., Mi, D., Gui, Y., Qi, Y., Jiang, C., Guo, J.-H., Plant Root Exudates Are Involved in Bacillus cereus AR156 Mediated Biocontrol Against Ralstonia solanacearum. Front. Microbiol., 10, 2019, 98, 10.3389/fmicb.2019.00098.
Xie, S., Jiang, L., Wu, Q., Wan, W., Gan, Y., Zhao, L., Wen, J., Maize Root Exudates Recruit Bacillus amyloliquefaciens OR2-30 to Inhibit Fusarium graminearum Infection. Phytopathology 112 (2022), 1886–1893, 10.1094/PHYTO-01-22-0028-R.
Xiong, Y.-W., Li, X.-W., Wang, T.-T., Gong, Y., Zhang, C.-M., Xing, K., Qin, S., Root exudates-driven rhizosphere recruitment of the plant growth-promoting rhizobacterium Bacillus flexus KLBMP 4941 and its growth-promoting effect on the coastal halophyte Limonium sinense under salt stress. Ecotoxicol. Environ. Saf., 194, 2020, 110374, 10.1016/j.ecoenv.2020.110374.
Tian, B., Zhang, C., Ye, Y., Wen, J., Wu, Y., Wang, H., Li, H., Cai, S., Cai, W., Cheng, Z., et al. Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agric. Ecosyst. Environ. 247 (2017), 149–156, 10.1016/j.agee.2017.06.041.
Torres-Cortés, G., Bonneau, S., Bouchez, O., Genthon, C., Briand, M., Jacques, M.-A., Barret, M., Functional Microbial Features Driving Community Assembly During Seed Germination and Emergence. Front. Plant Sci., 9, 2018, 902, 10.3389/fpls.2018.00902.
Knief, C., Delmotte, N., Chaffron, S., Stark, M., Innerebner, G., Wassmann, R., von Mering, C., Vorholt, J.A., Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6 (2012), 1378–1390, 10.1038/ismej.2011.192.
Levy, A., Salas Gonzalez, I., Mittelviefhaus, M., Clingenpeel, S., Herrera Paredes, S., Miao, J., Wang, K., Devescovi, G., Stillman, K., Monteiro, F., et al. Genomic features of bacterial adaptation to plants. Nat. Genet. 50 (2017), 138–150, 10.1038/s41588-017-0012-9.
Anckaert, A., Argüelles Arias, A., Hoff, G., Calonne-Salmon, M., Declerck, S., Ongena, M., The use of Bacillus spp. as bacterial biocontrol agents to control plant diseases. Köhl, J., Ravensberg, W., (eds.) Microbial bioprotectants for plant disease management, 2021, Burleigh Dodds Science Publishing), 1–54.
Miljaković, D., Marinković, J., Balešević-Tubić, S., The Significance of Bacillus spp. in Disease Suppression and Growth Promotion of Field and Vegetable Crops. Microorganisms, 8, 2020, 1037, 10.3390/microorganisms8071037.
Fan, B., Wang, C., Song, X., Ding, X., Wu, L., Wu, H., Gao, X., Borriss, R., Bacillus velezensis FZB42 in 2018: The Gram-Positive Model Strain for Plant Growth Promotion and Biocontrol. Front. Microbiol., 9, 2018, 2491, 10.3389/fmicb.2018.02491.
Rabbee, M.F., Ali, M.S., Choi, J., Hwang, B.S., Jeong, S.C., Baek, K.H., Bacillus velezensis: A Valuable Member of Bioactive Molecules within Plant Microbiomes. Molecules, 24, 2019, 1046, 10.3390/molecules24061046.
Ye, M., Tang, X., Yang, R., Zhang, H., Li, F., Tao, F., Li, F., Wang, Z., Characteristics and Application of a Novel Species of Bacillus: Bacillus velezensis. ACS Chem. Biol. 13 (2018), 500–505, 10.1021/acschembio.7b00874.
Pandin, C., Le Coq, D., Deschamps, J., Védie, R., Rousseau, T., Aymerich, S., Briandet, R., Complete genome sequence of Bacillus velezensis QST713: A biocontrol agent that protects Agaricus bisporus crops against the green mould disease. J. Biotechnol. 278 (2018), 10–19, 10.1016/j.jbiotec.2018.04.014.
Köhl, J., Kolnaar, R., Ravensberg, W.J., Mode of Action of Microbial Biological Control Agents Against Plant Diseases: Relevance Beyond Efficacy. Front. Plant Sci., 10, 2019, 845, 10.3389/fpls.2019.00845.
Andrić, S., Meyer, T., Ongena, M., Bacillus Responses to Plant-Associated Fungal and Bacterial Communities. Front. Microbiol., 11, 2020, 1350, 10.3389/fmicb.2020.01350.
Harwood, C.R., Mouillon, J.-M., Pohl, S., Arnau, J., Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol. Rev. 42 (2018), 721–738, 10.1093/femsre/fuy028.
Andrić, S., Rigolet, A., Argüelles Arias, A., Steels, S., Hoff, G., Balleux, G., Ongena, L., Höfte, M., Meyer, T., Ongena, M., Plant-associated Bacillus mobilizes its secondary metabolites upon perception of the siderophore pyochelin produced by a Pseudomonas competitor. ISME J. 17 (2023), 263–275, 10.1038/s41396-022-01337-1.
López, D., Fischbach, M.A., Chu, F., Losick, R., Kolter, R., Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 106 (2009), 280–285, 10.1073/pnas.0810940106.
Townsley, L., Shank, E.A., Natural-Product Antibiotics: Cues for Modulating Bacterial Biofilm Formation. Trends Microbiol. 25 (2017), 1016–1026, 10.1016/j.tim.2017.06.003.
Bleich, R., Watrous, J.D., Dorrestein, P.C., Bowers, A.A., Shank, E.A., Thiopeptide antibiotics stimulate biofilm formation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 112 (2015), 3086–3091, 10.1073/pnas.1414272112.
Arnaouteli, S., Bamford, N.C., Stanley-Wall, N.R., Kovács, Á.T., Bacillus subtilis biofilm formation and social interactions. Nat. Rev. Microbiol. 19 (2021), 600–614, 10.1038/s41579-021-00540-9.
Feng, H., Zhang, N., Du, W., Zhang, H., Liu, Y., Fu, R., Shao, J., Zhang, G., Shen, Q., Zhang, R., Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol. Plant Microbe Interact. 31 (2018), 995–1005, 10.1094/MPMI-01-18-0003-R.
Liu, Y., Feng, H., Fu, R., Zhang, N., Du, W., Shen, Q., Zhang, R., Induced root-secreted d-galactose functions as a chemoattractant and enhances the biofilm formation of Bacillus velezensis SQR9 in an McpA-dependent manner. Appl. Microbiol. Biotechnol. 104 (2020), 785–797, 10.1007/S00253-019-10265-8.
Yuan, J., Zhang, N., Huang, Q., Raza, W., Li, R., Vivanco, J.M., Shen, Q., Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci. Rep., 5, 2015, 13438, 10.1038/srep13438.
Zhang, N., Wang, D., Liu, Y., Li, S., Shen, Q., Zhang, R., Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374 (2014), 689–700, 10.1007/S11104-013-1915-6.
Allard-Massicotte, R., Tessier, L., Lécuyer, F., Lakshmanan, V., Lucier, J.-F., Garneau, D., Caudwell, L., Vlamakis, H., Bais, H.P., Beauregard, P.B., Bacillus subtilis Early Colonization of Arabidopsis thaliana Roots Involves Multiple Chemotaxis Receptors. mBio, 7, 2016, e01664, 10.1128/mBio.01664-16.
Nihorimbere, V., Cawoy, H., Seyer, A., Brunelle, A., Thonart, P., Ongena, M., Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol. Ecol. 79 (2012), 176–191, 10.1111/j.1574-6941.2011.01208.x.
Hoff, G., Arguelles Arias, A., Boubsi, F., Pršić, J., Meyer, T., Ibrahim, H.M.M., Steels, S., Luzuriaga, P., Legras, A., Franzil, L., et al. Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus-Plant Mutualistic Interaction. mBio, 12, 2021, e0177421, 10.1128/mBio.01774-21.
Fan, B., Carvalhais, L.C., Becker, A., Fedoseyenko, D., von Wirén, N., Borriss, R., Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol., 12, 2012, 116, 10.1186/1471-2180-12-116.
Zhang, N., Yang, D., Wang, D., Miao, Y., Shao, J., Zhou, X., Xu, Z., Li, Q., Feng, H., Li, S., et al. Whole transcriptomic analysis of the plant-beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 during enhanced biofilm formation regulated by maize root exudates. BMC Genom., 16, 2015, 685, 10.1186/s12864-015-1825-5.
Debois, D., Fernandez, O., Franzil, L., Jourdan, E., de Brogniez, A., Willems, L., Clément, C., Dorey, S., De Pauw, E., Ongena, M., Plant polysaccharides initiate underground crosstalk with bacilli by inducing synthesis of the immunogenic lipopeptide surfactin. Environ. Microbiol. Rep. 7 (2015), 570–582, 10.1111/1758-2229.12286.
Wu, K., Fang, Z., Guo, R., Pan, B., Shi, W., Yuan, S., Guan, H., Gong, M., Shen, B., Shen, Q., 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, 2015, e0127418, 10.1371/journal.pone.0127418.
Beauregard, P.B., Chai, Y., Vlamakis, H., Losick, R., Kolter, R., Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci. USA 110 (2013), E1621–E1630, 10.1073/pnas.1218984110.
Li, M., Shu, C., Ke, W., Li, X., Yu, Y., Guan, X., Huang, T., Plant Polysaccharides Modulate Biofilm Formation and Insecticidal Activities of Bacillus thuringiensis Strains. Front. Microbiol., 12, 2021, 676146, 10.3389/fmicb.2021.676146.
Habib, C., Yu, Y., Gozzi, K., Ching, C., Shemesh, M., Chai, Y., Characterization of the regulation of a plant polysaccharide utilization operon and its role in biofilm formation in Bacillus subtilis. PLoS One, 12, 2017, e0179761, 10.1371/journal.pone.0179761.
Du, J., Anderson, C.T., Xiao, C., Dynamics of pectic homogalacturonan in cellular morphogenesis and adhesion, wall integrity sensing and plant development. Nat. Plants 8 (2022), 332–340, 10.1038/s41477-022-01120-2.
Andrić, S., Meyer, T., Rigolet, A., Prigent-Combaret, C., Höfte, M., Balleux, G., Steels, S., Hoff, G., De Mot, R., McCann, A., et al. Lipopeptide Interplay Mediates Molecular Interactions between Soil Bacilli and Pseudomonads. Microbiol. Spectr., 9, 2021, e0203821, 10.1128/spectrum.02038-21.
Bonnin, E., Pelloux, J., Pectin Degrading Enzymes. Kontogiorgos, V., (eds.) Pectin: Technological and Physiological Properties, 2020, Springer International Publishing), 37–60.
Fuxreiter, M., Tompa, P., Simon, I., Local structural disorder imparts plasticity on linear motifs. Bioinformatics 23 (2007), 950–956, 10.1093/bioinformatics/btm035.
Berlow, R.B., Dyson, H.J., Wright, P.E., Functional advantages of dynamic protein disorder. FEBS Lett. 589 (2015), 2433–2440, 10.1016/j.febslet.2015.06.003.
Kalamara, M., Spacapan, M., Mandic-Mulec, I., Stanley-Wall, N.R., Social behaviours by Bacillus subtilis: quorum sensing, kin discrimination and beyond. Mol. Microbiol. 110 (2018), 863–878, 10.1111/mmi.14127.
Xiong, Q., Liu, D., Zhang, H., Dong, X., Zhang, G., Liu, Y., Zhang, R., Quorum sensing signal autoinducer-2 promotes root colonization of Bacillus velezensis SQR9 by affecting biofilm formation and motility. Appl. Microbiol. Biotechnol. 104 (2020), 7177–7185, 10.1007/s00253-020-10713-w.
Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y., Morishima, K., KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45 (2017), D353–D361, 10.1093/nar/gkw1092.
Massalha, H., Korenblum, E., Malitsky, S., Shapiro, O.H., Aharoni, A., Live imaging of root–bacteria interactions in a microfluidics setup. Proc. Natl. Acad. Sci. USA 114 (2017), 4549–4554, 10.1073/pnas.1618584114.
Dong, L., Guo, Q., Wang, P., Zhang, X., Su, Z., Zhao, W., Lu, X., Li, S., Ma, P., Qualitative and Quantitative Analyses of the Colonization Characteristics of Bacillus subtilis Strain NCD-2 on Cotton Root. Curr. Microbiol. 77 (2020), 1600–1609, 10.1007/s00284-020-01971-y.
Nordgaard, M., Mortensen, R.M.R., Kirk, N.K., Gallegos-Monterrosa, R., Kovács, Á.T., Deletion of Rap-Phr systems in Bacillus subtilis influences in vitro biofilm formation and plant root colonization. Microbiologyopen, 10, 2021, e1212, 10.1002/mbo3.1212.
Al-Ali, A., Deravel, J., Krier, F., Béchet, M., Ongena, M., Jacques, P., Biofilm formation is determinant in tomato rhizosphere colonization by Bacillus velezensis FZB42. Environ. Sci. Pollut. Res. Int. 25 (2018), 29910–29920, 10.1007/s11356-017-0469-1.
Guttenplan, S.B., Blair, K.M., Kearns, D.B., The EpsE Flagellar Clutch Is Bifunctional and Synergizes with EPS Biosynthesis to Promote Bacillus subtilis Biofilm Formation. PLoS Genet., 6, 2010, e1001243, 10.1371/journal.pgen.1001243.
Blair, K.M., Turner, L., Winkelman, J.T., Berg, H.C., Kearns, D.B., A Molecular Clutch Disables Flagella in the Bacillus subtilis Biofilm. Science 320 (2008), 1636–1638, 10.1126/science.1157877.
Zeriouh, H., de Vicente, A., Pérez-García, A., Romero, D., Surfactin triggers biofilm formation of Bacillus subtilis in melon phylloplane and contributes to the biocontrol activity. Environ. Microbiol. 16 (2014), 2196–2211, 10.1111/1462-2920.12271.
Zhang, Y., Qi, J., Wang, Y., Wen, J., Zhao, X., Qi, G., Comparative study of the role of surfactin-triggered signalling in biofilm formation among different Bacillus species. Microbiol. Res., 254, 2022, 126920, 10.1016/j.micres.2021.126920.
Peng, N., Cai, P., Mortimer, M., Wu, Y., Gao, C., Huang, Q., The exopolysaccharide–eDNA interaction modulates 3D architecture of Bacillus subtilis biofilm. BMC Microbiol., 20, 2020, 115, 10.1186/s12866-020-01789-5.
Zafra, O., Lamprecht-Grandío, M., de Figueras, C.G., González-Pastor, J.E., Extracellular DNA Release by Undomesticated Bacillus subtilis Is Regulated by Early Competence. PLoS One, 7, 2012, e48716, 10.1371/journal.pone.0048716.
Chan, S.Y., Choo, W.S., Young, D.J., Loh, X.J., Pectin as a rheology modifier: Origin, structure, commercial production and rheology. Carbohydr. Polym. 161 (2017), 118–139, 10.1016/j.carbpol.2016.12.033.
Serra, D.O., Richter, A.M., Hengge, R., Cellulose as an Architectural Element in Spatially Structured Escherichia coli Biofilms. J. Bacteriol. 195 (2013), 5540–5554, 10.1128/JB.00946-13.
Qin, Y., Angelini, L.L., Chai, Y., Bacillus subtilis Cell Differentiation, Biofilm Formation and Environmental Prevalence. Microorganisms, 10, 2022, 1108, 10.3390/microorganisms10061108.
Fujita, M., Losick, R., Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19 (2005), 2236–2244, 10.1101/gad.1335705.
Molle, V., Fujita, M., Jensen, S.T., Eichenberger, P., González-Pastor, J.E., Liu, J.S., Losick, R., The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 50 (2003), 1683–1701, 10.1046/j.1365-2958.2003.03818.x.
Banse, A.V., Chastanet, A., Rahn-Lee, L., Hobbs, E.C., Losick, R., Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 105 (2008), 15547–15552, 10.1073/pnas.0805203105.
Aguilar, C., Vlamakis, H., Guzman, A., Losick, R., Kolter, R., KinD Is a Checkpoint Protein Linking Spore Formation to Extracellular-Matrix Production in Bacillus subtilis Biofilms. mBio, 1, 2010, 10.1128/mBio.00035-10 e00035-10.
Borriss, R., Wu, H., Gao, X., Secondary Metabolites of the Plant Growth Promoting Model Rhizobacterium Bacillus velezensis FZB42 Are Involved in Direct Suppression of Plant Pathogens and in Stimulation of Plant-Induced Systemic Resistance. Singh, H., Keswani, C., Reddy, M., Sansinenea, E., García-Estrada, C., (eds.) Secondary Metabolites of Plant Growth Promoting Rhizomicroorganisms, 2019, Springer Singapore, 147–168.
Pluskal, T., Castillo, S., Villar-Briones, A., Orešič, M., MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinf., 11, 2010, 395, 10.1186/1471-2105-11-395.
Ongena, M., Jacques, P., Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16 (2008), 115–125, 10.1016/j.tim.2007.12.009.
Sun, H., Jiang, S., Jiang, C., Wu, C., Gao, M., Wang, Q., A review of root exudates and rhizosphere microbiome for crop production. Environ. Sci. Pollut. Res. Int. 28 (2021), 54497–54510, 10.1007/s11356-021-15838-7.
Sasse, J., Martinoia, E., Northen, T., Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?. Trends Plant Sci. 23 (2018), 25–41, 10.1016/j.tplants.2017.09.003.
Zhang, L., van Kan, J.A.L., Pectin as a Barrier and Nutrient Source for Fungal Plant Pathogens. Kempken, F., ed, (eds.) In A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research, 2013, Springer Berlin, 361–365.
Schmitz, K., Protzko, R., Zhang, L., Benz, J.P., Spotlight on fungal pectin utilization—from phytopathogenicity to molecular recognition and industrial applications. Appl. Microbiol. Biotechnol. 103 (2019), 2507–2524, 10.1007/s00253-019-09622-4.
Kubicek, C.P., Starr, T.L., Glass, N.L., Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi. Annu. Rev. Phytopathol. 52 (2014), 427–451, 10.1146/annurev-phyto-102313-045831.
Lyu, X., Shen, C., Fu, Y., Xie, J., Jiang, D., Li, G., Cheng, J., Comparative genomic and transcriptional analyses of the carbohydrate-active enzymes and secretomes of phytopathogenic fungi reveal their significant roles during infection and development. Sci. Rep., 5, 2015, 15565, 10.1038/srep15565.
Synek, L., Rawat, A., L'Haridon, F., Weisskopf, L., Saad, M.M., Hirt, H., Multiple strategies of plant colonization by beneficial endophytic Enterobacter sp. SA187. Environ. Microbiol. 23 (2021), 6223–6240, 10.1111/1462-2920.15747.
Wheatley, R.M., Poole, P.S., Mechanisms of bacterial attachment to roots. FEMS Microbiol. Rev. 42 (2018), 448–461, 10.1093/femsre/fuy014.
Tian, T., Sun, B., Shi, H., Gao, T., He, Y., Li, Y., Liu, Y., Li, X., Zhang, L., Li, S., et al. Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization. ISME J. 15 (2021), 2723–2737, 10.1038/s41396-021-00966-2.
Guttenplan, S.B., Kearns, D.B., Regulation of flagellar motility during biofilm formation. FEMS Microbiol. Rev. 37 (2013), 849–871, 10.1111/1574-6976.12018.
Vlamakis, H., Chai, Y., Beauregard, P., Losick, R., Kolter, R., Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol. 11 (2013), 157–168, 10.1038/nrmicro2960.
Arnaouteli, S., MacPhee, C.E., Stanley-Wall, N.R., Just in case it rains: building a hydrophobic biofilm the Bacillus subtilis way. Curr. Opin. Microbiol. 34 (2016), 7–12, 10.1016/j.mib.2016.07.012.
Molina-Santiago, C., Pearson, J.R., Navarro, Y., Berlanga-Clavero, M.V., Caraballo-Rodriguez, A.M., Petras, D., García-Martín, M.L., Lamon, G., Haberstein, B., Cazorla, F.M., et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat. Commun., 10, 2019, 1919, 10.1038/s41467-019-09944-x.
Nicholson, W.L., Fajardo-Cavazos, P., Rebeil, R., Slieman, T.A., Riesenman, P.J., Law, J.F., Xue, Y., Bacterial endospores and their significance in stress resistance. Antonie Leeuwenhoek 81 (2002), 27–32, 10.1023/a:1020561122764.
Dittmann, C., Han, H.-M., Grabenbauer, M., Laue, M., Dormant Bacillus spores protect their DNA in crystalline nucleoids against environmental stress. J. Struct. Biol. 191 (2015), 156–164, 10.1016/j.jsb.2015.06.019.
Setlow, P., I will survive: DNA protection in bacterial spores. Trends Microbiol. 15 (2007), 172–180, 10.1016/j.tim.2007.02.004.
Lopez, D., Vlamakis, H., Kolter, R., Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol. Rev. 33 (2009), 152–163, 10.1111/j.1574-6976.2008.00148.x.
Veening, J.-W., Kuipers, O.P., Brul, S., Hellingwerf, K.J., Kort, R., Effects of Phosphorelay Perturbations on Architecture, Sporulation, and Spore Resistance in Biofilms of Bacillus subtilis. J. Bacteriol. 188 (2006), 3099–3109, 10.1128/JB.188.8.3099-3109.2006.
Hamon, M.A., Lazazzera, B.A., The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42 (2001), 1199–1209, 10.1046/j.1365-2958.2001.02709.x.
Ellermeier, C.D., Hobbs, E.C., Gonzalez-Pastor, J.E., Losick, R., A Three-Protein Signaling Pathway Governing Immunity to a Bacterial Cannibalism Toxin. Cell 124 (2006), 549–559, 10.1016/j.cell.2005.11.041.
González-Pastor, J.E., Hobbs, E.C., Losick, R., Cannibalism by Sporulating Bacteria. Science 301 (2003), 510–513, 10.1126/science.1086462.
Höfler, C., Heckmann, J., Fritsch, A., Popp, P., Gebhard, S., Fritz, G., Mascher, T., Cannibalism stress response in Bacillus subtilis. Microbiology 162 (2016), 164–176, 10.1099/mic.0.000176.
González-Pastor, J.E., Cannibalism: a social behavior in sporulating Bacillus subtilis. FEMS Microbiol. Rev. 35 (2011), 415–424, 10.1111/j.1574-6976.2010.00253.x.
Pršić, J., Ongena, M., Elicitors of Plant Immunity Triggered by Beneficial Bacteria. Front. Plant Sci., 11, 2020, 594530, 10.3389/fpls.2020.594530.
Wu, G., Liu, Y., Xu, Y., Zhang, G., Shen, Q., Zhang, R., Exploring Elicitors of the Beneficial Rhizobacterium Bacillus amyloliquefaciens SQR9 to Induce Plant Systemic Resistance and Their Interactions With Plant Signaling Pathways. Mol. Plant Microbe Interact. 31 (2018), 560–567, 10.1094/MPMI-11-17-0273-R.
Han, Q., Wu, F., Wang, X., Qi, H., Shi, L., Ren, A., Liu, Q., Zhao, M., Tang, C., The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity. Environ. Microbiol. 17 (2015), 1166–1188, 10.1111/1462-2920.12538.
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J.L., Thonart, P., Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9 (2007), 1084–1090, 10.1111/J.1462-2920.2006.01202.X.
Li, Y., Héloir, M.C., Zhang, X., Geissler, M., Trouvelot, S., Jacquens, L., Henkel, M., Su, X., Fang, X., Wang, Q., Adrian, M., Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defence stimulation. Mol. Plant Pathol. 20 (2019), 1037–1050, 10.1111/mpp.12809.
Chen, X.H., Scholz, R., Borriss, M., Junge, H., Mögel, G., Kunz, S., Borriss, R., Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J. Biotechnol. 140 (2009), 38–44, 10.1016/j.jbiotec.2008.10.015.
Wu, L., Wu, H., Chen, L., Yu, X., Borriss, R., Gao, X., Difficidin and bacilysin from Bacillus amyloliquefaciens FZB42 have antibacterial activity against Xanthomonas oryzae rice pathogens. Sci. Rep., 5, 2015, 12975, 10.1038/srep12975.
Müller, S., Strack, S.N., Hoefler, B.C., Straight, P.D., Kearns, D.B., Kirby, J.R., Bacillaene and Sporulation Protect Bacillus subtilis from Predation by Myxococcus xanthus. Appl. Environ. Microbiol. 80 (2014), 5603–5610, 10.1128/AEM.01621-14.
Im, S.M., Yu, N.H., Joen, H.W., Kim, S.O., Park, H.W., Park, A.R., Kim, J.-C., Biological control of tomato bacterial wilt by oxydifficidin and difficidin-producing Bacillus methylotrophicus DR-08. Pestic. Biochem. Physiol. 163 (2020), 130–137, 10.1016/j.pestbp.2019.11.007.
Barger, S.R., Hoefler, B.C., Cubillos-Ruiz, A., Russell, W.K., Russell, D.H., Straight, P.D., Imaging secondary metabolism of Streptomyces sp. Mg1 during cellular lysis and colony degradation of competing Bacillus subtilis. Antonie Leeuwenhoek 102 (2012), 435–445, 10.1007/s10482-012-9769-0.
Konishi, H., Hio, M., Kobayashi, M., Takase, R., Hashimoto, W., Bacterial chemotaxis towards polysaccharide pectin by pectin-binding protein. Sci. Rep., 10, 2020, 3977, 10.1038/s41598-020-60274-1.
Taylor, B.L., Zhulin, I.B., PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light. Microbiol. Mol. Biol. Rev. 63 (1999), 479–506, 10.1128/MMBR.63.2.479-506.1999.
Higgins, D., Dworkin, J., Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36 (2012), 131–148, 10.1111/j.1574-6976.2011.00310.x.
Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., Henrissat, B., The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 37 (2009), D233–D238, 10.1093/nar/gkn663.
Bryksin, A.V., Matsumura, I., Overlap extension PCR cloning: a simple and reliable way to create recombinant plasmids. Biotechniques 48 (2010), 463–465, 10.2144/000113418.
Jarmer, H., Berka, R., Knudsen, S., Saxild, H.H., Transcriptome analysis documents induced competence of Bacillus subtilis during nitrogen limiting conditions. FEMS Microbiol. Lett. 206 (2002), 197–200, 10.1016/S0378-1097(01)00525-0.
Tamura, K., Stecher, G., Kumar, S., MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 38 (2021), 3022–3027, 10.1093/molbev/msab120.
Collmer, A., Ried, J.L., Mount, M.S., Assay methods for pectic enzymes. Methods Enzymol. 161 (1988), 329–335, 10.1016/0076-6879(88)61037-8.
Carpita, N.C., Cell Wall Development in Maize Coleoptiles. Plant Physiol. 76 (1984), 205–212, 10.1104/pp.76.1.205.
Silva, G.B., Ionashiro, M., Carrara, T.B., Crivellari, A.C., Tiné, M.A.S., Prado, J., Carpita, N.C., Buckeridge, M.S., Cell wall polysaccharides from fern leaves: Evidence for a mannan-rich Type III cell wall in Adiantum raddianum. Phytochemistry 72 (2011), 2352–2360, 10.1016/j.phytochem.2011.08.020.
Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, 2001, 45e, 10.1093/nar/29.9.e45.
Voxeur, A., Habrylo, O., Guénin, S., Miart, F., Soulié, M.C., Rihouey, C., Pau-Roblot, C., Domon, J.-M., Gutierrez, L., Pelloux, J., et al. Oligogalacturonide production upon Arabidopsis thaliana – Botrytis cinerea interaction. Proc. Natl. Acad. Sci. USA 116 (2019), 19743–19752, 10.1073/pnas.1900317116.
Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120, 10.1093/bioinformatics/btu170.
Li, H., Durbin, R., Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25 (2009), 1754–1760, 10.1093/bioinformatics/btp324.
Anders, S., Pyl, P.T., Huber, W., HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31 (2015), 166–169, 10.1093/bioinformatics/btu638.
Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 (2010), 511–515, 10.1038/nbt.1621.
Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550, 10.1186/s13059-014-0550-8.