Analysis of plant growth-promoting properties of Bacillus amyloliquefaciens UCMB5113 using Arabidopsis thaliana as host plant
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
PubMed
27541497
PubMed Central
PMC5226999
DOI
10.1007/s00425-016-2580-9
PII: 10.1007/s00425-016-2580-9
Knihovny.cz E-zdroje
- Klíčová slova
- Beneficial bacteria *, Biocontrol *, Growth promotion *, Phytohormones *, Rhizosphere *, Root structure *,
- MeSH
- Arabidopsis účinky léků růst a vývoj mikrobiologie MeSH
- Bacillus amyloliquefaciens účinky léků fyziologie MeSH
- brassinosteroidy farmakologie MeSH
- cytokininy farmakologie MeSH
- gibereliny farmakologie MeSH
- interakce hostitele a patogenu * účinky léků MeSH
- kořeny rostlin anatomie a histologie účinky léků MeSH
- kyseliny indoloctové farmakologie MeSH
- lipopeptidy farmakologie MeSH
- regulátory růstu rostlin farmakologie MeSH
- semenáček účinky léků růst a vývoj MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- brassinosteroidy MeSH
- cytokininy MeSH
- gibereliny MeSH
- kyseliny indoloctové MeSH
- lipopeptidy MeSH
- regulátory růstu rostlin MeSH
This study showed that Bacillus amyloliquefaciens UCMB5113 colonizing Arabidopsis roots changed root structure and promoted growth implying the usability of this strain as a novel tool to support sustainable crop production. Root architecture plays a crucial role for plants to ensure uptake of water, minerals and nutrients and to provide anchorage in the soil. The root is a dynamic structure with plastic growth and branching depending on the continuous integration of internal and environmental factors. The rhizosphere contains a complex microbiota, where some microbes can colonize plant roots and support growth and stress tolerance. Here, we report that the rhizobacterium Bacillus amyloliquefaciens subsp. plantarum UCMB5113 stimulated the growth of Arabidopsis thaliana Col-0 by increased lateral root outgrowth and elongation and root-hair formation, although primary root elongation was inhibited. In addition, the growth of the above ground tissues was stimulated by UCMB5113. Specific hormone reporter gene lines were tested which suggested a role for at least auxin and cytokinin signaling during rhizobacterial modulation of Arabidopsis root architecture. UCMB5113 produced cytokinins and indole-3-acetic acid, and the formation of the latter was stimulated by root exudates and tryptophan. The plant growth promotion effect by UCMB5113 did not appear to depend on jasmonic acid in contrast to the disease suppression effect in plants. UCMB5113 exudates inhibited primary root growth, while a semi-purified lipopeptide fraction did not and resulted in the overall growth promotion indicating an interplay of many different bacterial compounds that affect the root growth of the host plant. This study illustrates that beneficial microbes interact with plants in root development via classic and novel signals.
Zobrazit více v PubMed
Abd El-Daim IA, Bejai S, Meijer J. Improved heat stress tolerance of wheat seedlings by bacterial seed treatment. Plant Soil. 2014;379:337–350. doi: 10.1007/s11104-014-2063-3. DOI
Abreu ME, Munné-Bosch S. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot. 2009;60:1261–1271. doi: 10.1093/jxb/ern363. PubMed DOI PMC
Alexandre G. Coupling metabolism and chemotaxis-dependent behaviours by energy taxis receptors. Microbiology. 2010;156:2283–2293. doi: 10.1099/mic.0.039214-0. PubMed DOI
Antoniadi I, Plačková L, Simonovik B, Doležal K, Turnbull C, Ljung K, Novák O. Cell-type specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell. 2015;27:1955–1967. doi: 10.1105/tpc.15.00176. PubMed DOI PMC
Armengaud P, Zambaux K, Hills A, Sulpice R, Pattison RJ, Blatt MR, Amtmann A. EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J. 2009;57:945–956. doi: 10.1111/j.1365-313X.2008.03739.x. PubMed DOI
Asghar HN, Zahir ZA, Arshad M, Khalid A. Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils. 2002;35:231–237. doi: 10.1007/s00374-002-0462-8. DOI
Azevedo LB, van Zelm R, Leuven RSEW, Hendriks AJ, Huijbregts MAJ. Combined ecological risks of nitrogen and phosphorus in European freshwaters. Environ Pollut. 2015;200:85–92. doi: 10.1016/j.envpol.2015.02.011. PubMed DOI
Badri DV, Vivanco JM. Regulation and function of root exudates. Plant Cell Environ. 2009;32:666–681. doi: 10.1111/j.1365-3040.2009.01926.x. PubMed DOI
Bastian F, Cohen A, Piccoli P, Luna V, Baraldi R, Botini R. Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically defined media. Plant Growth Regul. 1998;24:7–11. doi: 10.1023/A:1005964031159. DOI
Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L. Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol. 2011;13:3047–3058. doi: 10.1111/j.1462-2920.2011.02582.x. PubMed DOI
Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009;60:379–406. doi: 10.1146/annurev.arplant.57.032905.105346. PubMed DOI
Brown ME, Funk CC. Climate—food security under climate change. Science. 2008;319:580–581. doi: 10.1126/science.1154102. PubMed DOI
Campanoni P, Nick P. Auxin-dependent cell division and cell elongation: 1-naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol. 2005;137:939–948. doi: 10.1104/pp.104.053843. PubMed DOI PMC
Choudhary DK, Johri BN. Interactions of Bacillus spp. and plants-with special reference to induced systemic resistance (ISR) Microbiol Res. 2009;164:493–513. doi: 10.1016/j.micres.2008.08.007. PubMed DOI
Claeys H, De Bodt S, Inzé D. Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci. 2014;19:231–239. doi: 10.1016/j.tplants.2013.10.001. PubMed DOI
Conrath U. Molecular aspects of defence priming. Trends Plant Sci. 2011;16:524–531. doi: 10.1016/j.tplants.2011.06.004. PubMed DOI
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol. 2011;11:163. doi: 10.1186/1471-2229-11-163. PubMed DOI PMC
D’Agostino IB, Deruère J, Kieber JJ. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 2000;124:1706–1717. doi: 10.1104/pp.124.4.1706. PubMed DOI PMC
Danielsson J, Reva O, Meijer J. Protection of oilseed rape (Brassica napus) toward fungal pathogens by strains of plant-associated Bacillus amyloliquefaciens. Microb Ecol. 2007;54:134–140. doi: 10.1007/s00248-006-9181-2. PubMed DOI
Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B. PGPR-Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plant Signal Behav. 2009;4(4):319–321. doi: 10.4161/psb.4.4.8106. PubMed DOI PMC
Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol. 1999;215:407–419. doi: 10.1006/dbio.1999.9443. PubMed DOI
Gaillochet C, Daum G, Lohmann JU. O cell, where art thou? The mechanisms of shoot meristem patterning. Curr Opin Plant Biol. 2015;23:91–97. doi: 10.1016/j.pbi.2014.11.002. PubMed DOI
Glickmann E, Dessaux Y. A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol. 1995;61:793–796. PubMed PMC
Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M. The plant-growth-promoting rhizobacteria Bacillus pumilis and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant. 2001;111:206–211. doi: 10.1034/j.1399-3054.2001.1110211.x. DOI
Hou X, Ding L, Yu H. Crosstalk between GA and JA signaling mediates plant growth and defense. Plant Cell Rep. 2013;32:1067–1074. doi: 10.1007/s00299-013-1423-4. PubMed DOI
Howell SH, Lall S, Che P. Cytokinins and shoot development. Trends Plant Sci. 2003;8:453–459. doi: 10.1016/S1360-1385(03)00191-2. PubMed DOI
Idris EE, Iglesias DJ, Talon M, Borriss R. Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant Microbe Interact. 2007;20:619–626. doi: 10.1094/MPMI-20-6-0619. PubMed DOI
Johansson AH, Bejai S, Niazi A, Manzoor S, Bongcam-Rudloff E, Meijer J. Studies of plant colonisation by closely related Bacillus amyloliquefaciens biocontrol agents using strain specific quantitative PCR assays. Antonie Van Leeuwenhoek. 2014;106:1247–1257. doi: 10.1007/s10482-014-0295-0. PubMed DOI
Joo GJ, Kim YM, Lee IJ, Song KS, Rhee IK. Growth promotion of red pepper plug seedlings and the production of gibberellins by Bacillus cereus, Bacillus macroides and Bacillus pumilus. Biotechnol Lett. 2004;26:487–491. doi: 10.1023/B:BILE.0000019555.87121.34. PubMed DOI
Khalid A, Arshad M, Zahir ZA. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol. 2004;96:473–480. doi: 10.1046/j.1365-2672.2003.02161.x. PubMed DOI
Kim PI, Bai H, Bai D, Chae H, Chung S, Kim Y, Park R, Chi YT. Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol. 2004;97:942–949. doi: 10.1111/j.1365-2672.2004.02356.x. PubMed DOI
Loper JE, Schroth MN. Influence of bacterial sources of indole-3-acetic acid in root elongation of sugar beet. Phytopathology. 1986;76:386–389. doi: 10.1094/Phyto-76-386. DOI
Lucy M, Reed E, Glick BR. Applications of free living plant growth-promoting rhizobacteria. Antonie Leeuwenhoek Int J G. 2004;86:1–25. doi: 10.1023/B:ANTO.0000024903.10757.6e. PubMed DOI
Martínez-Morales LJ, Soto-Urzúa L, Baca BE, Sánchez-Ahédo JA. Indole-3-butyric acid (IBA) production in culture medium by wild strain Azospririllum brasilense. FEMS Microbiol Lett. 2003;228:167–173. doi: 10.1016/S0378-1097(03)00694-3. PubMed DOI
Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J. The role of microbial signals in plant growth and development. Plant Signal Behav. 2009;4:701–712. doi: 10.4161/psb.4.8.9047. PubMed DOI PMC
Pacifici E, Polverari L, Sabatini S. Plant hormone cross-talk: the pivot of root growth. J Exp Bot. 2015;66:1113–1121. doi: 10.1093/jxb/eru534. PubMed DOI
Pěnčík A, Rolčík J, Novák O, Magnus V, Barták P, Buchtík R, Salopek-Sondi B, Strnad M. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta. 2009;80:651–655. doi: 10.1016/j.talanta.2009.07.043. PubMed DOI
Persello-Cartieaux F, Naussaume L, Robaglia C. Tales from the underground: molecular plant-rhizobacteria interactions. Plant Cell Environ. 2003;26:189–199. doi: 10.1046/j.1365-3040.2003.00956.x. DOI
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012;28:489–521. doi: 10.1146/annurev-cellbio-092910-154055. PubMed DOI
Reva ON, Dixelius C, Meijer J, Priest FG. Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol. 2004;48:249–259. doi: 10.1016/j.femsec.2004.02.003. PubMed DOI
Rittenberg D, Foster GL. A new procedure for quantitative analysis by isotope dilution with application to the determination of amino acids and fatty acids. J Biol Chem. 1940;133:737–744.
Rogers ED, Benfey PN. Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol. 2014;32:93–98. doi: 10.1016/j.copbio.2014.11.015. PubMed DOI
Ryu C-M, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA. 2003;100:4927–4932. doi: 10.1073/pnas.0730845100. PubMed DOI PMC
Sarosh BR, Danielsson J, Meijer J. Transcript profiling of oilseed rape (Brassica napus) primed for biocontrol differentiate genes involved in microbial interactions with beneficial Bacillus amyloliquefasciens from pathogenic Botrytis cinerea. Plant Mol Biol. 2009;70:31–45. doi: 10.1007/s11103-009-9455-4. PubMed DOI
Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Meth. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC
Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic in microbial and microorganism plant signaling. FEMS Microbiol Rev. 2007;31:425–448. doi: 10.1111/j.1574-6976.2007.00072.x. PubMed DOI
Spíchal L. Cytokinins—recent news and views of evolutionally old molecules. Funct Plant Biol. 2012;39:267–284. doi: 10.1071/FP11276. PubMed DOI
Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 2007;19:2169–2185. doi: 10.1105/tpc.107.052068. PubMed DOI PMC
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014;203:32–43. doi: 10.1111/nph.12797. PubMed DOI
Svačinová J, Novák O, Plačková L, Lenobel R, Holík J, Strnad M, Doležal K. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods. 2012;8:17. doi: 10.1186/1746-4811-8-17. PubMed DOI PMC
Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19:2186–2196. doi: 10.1105/tpc.107.052100. PubMed DOI PMC
Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF. Separate jasmonate-dependent and salicylate-dependent defence response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA. 1998;95:15107–15111. doi: 10.1073/pnas.95.25.15107. PubMed DOI PMC
Tian H, De Smet I, Ding Z. Shaping a root system: regulating lateral versus primary root growth. Trends Plant Sci. 2014;19:426–431. doi: 10.1016/j.tplants.2014.01.007. PubMed DOI
Urbanova T, Tarkowska D, Novák O, Hedden P, Strnad M. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta. 2013;112:85–94. doi: 10.1016/j.talanta.2013.03.068. PubMed DOI
Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C. Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci. 2013;4:356. doi: 10.3389/fpls.2013.00356. PubMed DOI PMC
Van der Ent S, Van Wess SCM, Pieterse CMJ. Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry. 2009;70:1581–1588. doi: 10.1016/j.phytochem.2009.06.009. PubMed DOI
Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol. 2013;11:157–168. doi: 10.1038/nrmicro2960. PubMed DOI PMC
Zamioudis C, Pieterse CMJ. Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact. 2012;25:139–150. doi: 10.1094/MPMI-06-11-0179. PubMed DOI
Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CM. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 2013;162:304–318. doi: 10.1104/pp.112.212597. PubMed DOI PMC
Zhu JY, Sae-Seaw J, Wang ZY. Brassinosteroid signaling. Development. 2013;140:1615–1620. doi: 10.1242/dev.060590. PubMed DOI PMC