Abstract
Background and aims
Plant growth-promoting rhizobacteria (PGPR) have garnered interest in agriculture due to their ability to influence the growth and production of host plants. ATP-binding cassette (ABC) transporters play important roles in plant-microbe interactions by modulating plant root exudation. The present study aimed to provide a more precise understanding of the mechanism and specificity of the interaction between PGPR and host plants.
Methods
In the present study, the effects of interactions between a PGPR strain, Bacillus cereus AR156, and Arabidopsis thaliana wild type (Col-0) or its ABC transporter mutants on plant growth have been studied.
Results
B. cereus AR156 promoted the shoot growth of Col-0 and Atabcg30 but repressed the growth of Atabcc5. Bacterial volatiles and secretion promoted the shoot growth of Col-0 and Atabcg30 but had no effect on Atabcc5. We also found that root exudates of Col-0 induced the expression of B. cereus AR156 genes related to siderophore and chitinase production; while root exudates of Atabcc5 inhibited the expression level of those genes. Further analysis of root exudates revealed that amino acids, organic acids, and sugars were significantly less abundant in Atabcc5 when compared to Col-0.
Conclusions
Our findings highlight that both host plant and PGPR play active roles in the outcome of the plant-microbe interaction.
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References
Acea MJ, Moore CR, Alexander M (1988) Survival and growth of bacteria introduced into soil. Soil Biol Biochem 20:509–515. doi:10.1016/0038-0717(88)90066-1
Ahmed E, Holmström SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208. doi:10.1111/1751-7915.12117
Aliasgharzad N, Neyshabouri M, Salimi G (2006) Effects of arbuscular mycorrhizal fungi and Bradyrhizobium japonicum on drought stress of soybean. Biologia 61:S324–S328. doi:10.2478/s11756-006-0182-x
Almaghrabi OA, Massoud SI, Abdelmoneim TS (2013) Influence of inoculation with plant growth promoting rhizobacteria (PGPR) on tomato plant growth and nematode reproduction under greenhouse conditions. Saudi J Biol Sci 20:57–61. doi:10.1016/j.sjbs.2012.10.004
Azcón R, Medina A, Aroca R, Ruiz-Lozano JM (2013) Abiotic stress remediation by the arbuscular mycorrhizal symbiosis and rhizosphere bacteria/yeast Interactions. Mol Microb Ecol Rhizosphere. doi:10.1002/9781118297674.ch93, John Wiley & Sons, Inc
Badri DV, Loyola-Vargas VM, Broeckling CD, De-la-Peña C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz F, Vivanco JM (2008) Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-Binding cassette transporter mutants. Plant Physiol 146:762–771. doi:10.1104/pp. 107.109587
Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–2017. doi:10.1104/pp. 109.147462
Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:10. doi:10.1074/jbc.M112.433300
Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134:307–319. doi:10.1104/pp. 103.028712
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi:10.1146/annurev.arplant.57.032905.105159
Bertani G (1951) Studies on Lysogenesis I.: the mode of phage liberation by Lysogenic Escherichia coli. J. Bacteriol. 62:293–300
Brimecombe M, Leij F, Lynch J (2001) Nematode community structure as a sensitive indicator of microbial perturbations induced by a genetically modified Pseudomonas fluorescens strain. Biol Fertil Soils 34:270–275. doi:10.1007/s003740100412
Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW (2005) Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot 56:323–336. doi:10.1093/jxb/eri058
Campbell RG, Greaves MP (1990) Anatomy and community structure of the rhizosphere. In: Lynch JM (ed) The rhizosphere. Wiley, Chichester
Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM (2013) Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS ONE 8, e55731. doi:10.1371/journal.pone.0055731
Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo JH, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430. doi:10.1111/j.1365-2958.2012.08109.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. doi:10.1111/j.1462-2920.2012.02860.x
Chet I (1990) Biological control of soil-borne plant pathogens with fungal antagonists in combination with soil treatments. In: Hornby D (ed) Biological control of soil-borne plant pathogens
Chet I, Inbar J (1994) Biological control of fungal pathogens. Appl Biochem Biotechnol 48:37–43. doi:10.1007/BF02825358
Crowley D (2006) Microbial siderophores in the plant rhizosphere. In: Barton L, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands
Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867. doi:10.1128/MMBR.64.4.847-867.2000
Dawwam GE, Elbeltagy A, Emara HM, Abbas IH, Hassan MM (2013) Beneficial effect of plant growth promoting bacteria isolated from the roots of potato plant. Ann Agric Sci 58:195–201. doi:10.1016/j.aoas.2013.07.007
de Werra P, Huser A, Tabacchi R, Keel C, Maurhofer M (2011) Plant- and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Appl Environ Microbiol 77:2807–2812. doi:10.1128/aem.01760-10
Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36:232–244. doi:10.3109/10408411003766806
Dutta S, Rani TS, Podile AR (2013) Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PLoS ONE 8, e78369. doi:10.1371/journal.pone.0078369
Fan TWM, Lane AN, Pedler J, Crowley D, Higashi RM (1997) Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatography–mass spectrometry. Anal Biochem 251:57–68. doi:10.1006/abio.1997.2235
Figueiredo M, Seldin L, Araujo F, Mariano R (2011) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin Heidelberg
Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadia J, Álvarez-Fernández A, Briat J-F (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–167. doi:10.1111/nph.12471
Frans AAMDL, James ML, Melissa JB (2007) Rhizodeposition and microbial populations. The Rhizosphere. CRC Press
Frapolli M, Défago G, Moënne-Loccoz Y (2010) Denaturing gradient gel electrophoretic analysis of dominant 2,4-diacetylphloroglucinol biosynthetic phlD alleles in fluorescent Pseudomonas from soils suppressive or conducive to black root rot of tobacco. Soil Biol Biochem 42:649–656. doi:10.1016/j.soilbio.2010.01.005
Frelet-Barrand A, Kolukisaoglu HU, Plaza S, Ruffer M, Azevedo L, Hortensteiner S, Marinova K, Weder B, Schulz B, Klein M (2008) Comparative mutant analysis of Arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxification, vacuolar organic anion transport and chlorophyll degradation. Plant Cell Physiol 49:557–569. doi:10.1093/pcp/pcn034
Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Muller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20:1875–1887. doi:10.1093/emboj/20.8.1875
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15. doi:10.6064/2012/963401
Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412. doi:10.1016/j.soilbio.2004.08.030
Gupta A, Gopal M, Tilak KV (2000) Mechanism of plant growth promotion by rhizobacteria. Indian J Exp Biol 38:856–862
Halket JM, Przyborowska A, Stein SE, Mallard WG, Down S, Chalmers RA (1999) Deconvolution gas chromatography/mass spectrometry of urinary organic acids – potential for pattern recognition and automated identification of metabolic disorders. Rapid Commun Mass Spectrom 13:279–284. doi:10.1002/(SICI)1097-0231(19990228)13:4<279::AID-RCM478>3.0.CO;2-I
Herrera-Estrella A, Chet I (1999) Chitinases in biological control. EXS 87:171–184
Hrynkiewicz K, Baum C, Leinweber P (2010) Density, metabolic activity, and identity of cultivable rhizosphere bacteria on Salix viminalis in disturbed arable and landfill soils. J Plant Nutr Soil Sci 173:747–756. doi:10.1002/jpln.200900286
Huang CJ, Tsay JF, Chang SY, Yang HP, Wu WS, Chen CY (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310. doi:10.1002/ps.3301
Huang XF, Zhou DM, Guo JH, Manter DK, Reardon KF, Vivanco JM (2015) Bacillus spp. from rainforest soil promote plant growth under limited nitrogen conditions. J Appl Microbiol 118:672–684. doi:10.1111/jam.12720
Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbes Interact 20:619–626. doi:10.1094/mpmi-20-6-0619
Jasinski M, Ducos E, Martinoia E, Boutry M (2003) The ATP-Binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177. doi:10.1104/pp. 102.014720
Joo HS, Chang CS (2005) Production of protease from a new alkalophilic Bacillus sp. I-312 grown on soybean meal: optimization and some properties. Process Biochem 40:1263–1270. doi:10.1016/j.procbio.2004.05.010
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci 107:2355–2360. doi:10.1073/pnas.0909222107
Karlidag H, Esitken A, Turan M, Sahin F (2007) Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci Hortic 114:16–20. doi:10.1016/j.scienta.2007.04.013
Keshav Prasad Shukla SS, Singh NK, Singh V, Tiwari K, Singh S (2011) Nature and role of root exudates: efficacy in bioremediation. Afr J Biotechnol 10:9717–9724
Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480. doi:10.1046/j.1365-2672.2003.02161.x
Kim HJ, Chen F, Wang X, Rajapakse NC (2005) Effect of chitosan on the biological properties of sweet basil (Ocimum basilicum L.). J Agric Food Chem 53:3696–3701. doi:10.1021/jf0480804
Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. Station de pathologic Vegetal et Phytobacteriologic, Agners, France
Kloepper J, Leong J, Teintze M, Schroth M (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320. doi:10.1007/BF02602840
Knauth S, Hurek T, Brar D, Reinhold-Hurek B (2005) Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ Microbiol 7:1725–1733. doi:10.1111/j.1462-2920.2005.00841.x
Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344. doi:10.1038/nature10873
Labuschagne N, Pretorius T, Idris AH (2011) Plant growth promoting rhizobacteria as biocontrol agents against soil-borne plant diseases. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin Heidelberg
Lambert B, Joos H (1989) Fundamental aspects of rhizobacterial plant growth promotion research. Trends Biotechnol 7:215–219. doi:10.1016/0167-7799(89)90107-8
Lee YS, Kim YH, Kim SB (2005) Changes in the respiration, growth, and vitamin C content of soybean sprouts in response to chitosan of different molecular weights. HortSci 40:1333–1335
Li J, Glick BR (2001) Transcriptional regulation of the Enterobacter cloacae UW4 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene (acdS). Can J Microbiol 47:359–367. doi:10.1139/w01-009
Loon LC, Bakker PAHM (2006) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: Siddiqui Z (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands
Loyola-Vargas VM, Broeckling CD, Badri D, Vivanco JM (2007) Effect of transporters on the secretion of phytochemicals by the roots of Arabidopsis thaliana. Planta 225:301–310. doi:10.1007/s00425-006-0349-2
Lucy M, Reed E, Glick B (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25. doi:10.1023/B:ANTO.0000024903.10757.6e
Malhotra M, Srivastava S (2006) Targeted engineering of Azospirillum brasilense SM with indole acetamide pathway for indoleacetic acid over-expression. Can J Microbiol 52:1078–1084. doi:10.1139/w06-071
Malhotra M, Srivastava S (2009) Stress-responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and its ability to modulate plant growth. Eur J Soil Biol 45:73–80. doi:10.1016/j.ejsobi.2008.05.006
Martínez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319. doi:10.4067/S0718-95162010000100006
Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530. doi:10.1016/j.plantsci.2003.10.025
Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451. doi:10.1128/mmbr.00012-07
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Nicholas CU (2007) Types, amounts, and possible functions of compounds released into the Rhizosphere by soil-grown plants. The Rhizosphere. CRC Press.
Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth–promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant-Microbe Interact 24:533–542. doi:10.1094/MPMI-09-10-0213
Notz R, Maurhofer M, Schnider-Keel U, Duffy B, Haas D, Defago G (2001) Biotic factors affecting expression of the 2,4-Diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91:873–881. doi:10.1094/phyto.2001.91.9.873
Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111:38–43. doi:10.1016/j.scienta.2006.09.002
Orr CH, James A, Leifert C, Cooper JM, Cummings SP (2011) Diversity and activity of free-living nitrogen-fixing bacteria and total bacteria in organic and conventionally managed soils. Appl Environ Microbiol 77:911–919. doi:10.1128/aem.01250-10
Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752. doi:10.1007/s13593-014-0233-6
Peterson SB, Dunn AK, Klimowicz AK, Handelsman J (2006) Peptidoglycan from Bacillus cereus mediates commensalism with rhizosphere bacteria from the cytophaga-flavobacterium group. Appl Environ Microbiol 72:5421–5427. doi:10.1128/aem.02928-05
Pilet PE, Saugy M (1987) Effect on root growth of endogenous and applied IAA and ABA: a critical reexamination. Plant Physiol 83:33–38. doi:10.1104/pp. 83.1.33
Prigent-Combaret C, Blaha D, Pothier JF, Vial L, Poirier MA, Wisniewski-Dye F, Moenne-Loccoz Y (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol 65:202–219. doi:10.1111/j.1574-6941.2008.00474.x
Přikryl Z, Vančura V (1980) Root exudates of plants. Plant Soil 57:69–83. doi:10.1007/bf02139643
Ramaekers L, Remans R, Rao IM, Blair MW, Vanderleyden J (2010) Strategies for improving phosphorus acquisition efficiency of crop plants. Field Crop Res 117:169–176. doi:10.1016/j.fcr.2010.03.001
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375. doi:10.1146/annurev.arplant.57.032905.105406
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. doi:10.1104/pp. 111.175448
Rothballer M, Schmid M, Fekete A, Hartmann A (2005) Comparative in situ analysis of ipdC-gfpmut3 promoter fusions of Azospirillum brasilense strains Sp7 and Sp245. Environ Microbiol 7:1839–1846. doi:10.1111/j.1462-2920.2005.00848.x
Rovira A (1969) Plant root exudates. Bot Rev 35:35–57. doi:10.1007/BF02859887
Růžička K, Strader LC, Bailly A, Yang H, Blakeslee J, Łangowski Ł, Nejedlá E, Fujita H, Itoh H, Syōno K, Hejátko J, Gray WM, Martinoia E, Geisler M, Bartel B, Murphy AS, Friml J (2010) Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci U S A 107:10749–10753. doi:10.1073/pnas.1005878107
Ryan AD, Kinkel LL, Schottel JL (2004) Effect of pathogen isolate, potato cultivar, and antagonist strain on potato scab severity and biological control. Biocontrol Sci Tech 14:301–311. doi:10.1080/09583150410001665187
Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932. doi:10.1073/pnas.0730845100
Sayyed RZ, Gangurde NS, Patel PR, Josh SA, Chincholkar SB (2010) Siderophore production by Alcaligenes faecalis and its application for growth promotion in Arachis hypogaea. Indian J Biotechnol 9:302–307
Sgroy V, Cassán F, Masciarelli O, Papa M, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381. doi:10.1007/s00253-009-2116-3
Sharp R (2013) A review of the applications of chitin and its derivatives in agriculture to modify plant-microbial interactions and improve crop yields. Agronomy 3:36. doi:10.3390/agronomy3040757
Siddiqui IA, Shaukat SS (2003) Plant species, host age and host genotype effects on Meloidogyne incognita biocontrol by Pseudomonas fluorescens strain CHA0 and its genetically-modified derivatives. J Phytopathol 151:231–238. doi:10.1046/j.1439-0434.2003.00716.x
Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl Environ Microbiol 71:1803–1810. doi:10.1128/aem.71.4.1803-1810.2005
Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell Online 18:731–746. doi:10.1105/tpc.105.038372
Stenfors Arnesen LP, Fagerlund A, Granum PE (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32:579–606. doi:10.1111/j.1574-6976.2008.00112.x
Strader LC, Bartel B (2009) The Arabidopsis pleiotropic drug resistance8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007. doi:10.1105/tpc.109.065821
Sugiyama A, Shitan N, Yazaki K (2007) Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in Legume-Rhizobium symbiosis. Plant Physiol 144:2000–2008. doi:10.1104/pp. 107.096727
Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7, e52565. doi:10.1371/journal.pone.0052565
Wei LH, Xue QY, Wei BQ, Wang YM, Li SM, Chen LF, Guo JH (2010) Screening of antagonistic bacterial strains against Meloidogyne incognita using protease activity. Biocontrol Sci Tech 20:739–750. doi:10.1080/09583151003714109
Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407. doi:10.1146/annurev.py.26.090188.002115
Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307. doi:10.1016/j.pbi.2005.03.011
Yazaki K, Sasaki K, Tsurumaru Y (2009) Prenylation of aromatic compounds, a key diversification of plant secondary metabolites. Phytochemistry 70:1739–1745. doi:10.1016/j.phytochem.2009.08.023
Zakharova EA, Iosipenko AD, Ignatov VV (2000) Effect of water-soluble vitamins on the production of indole-3-acetic acid by Azospirillum brasilense. Microbiol Res 155:209–214. doi:10.1016/s0944-5013(00)80034-8
Zhou DM, Wang KP, Liu HX, Gu C, Guo JH (2014) Field evaluation of different application methods of the mixture of Bacillus cereus strain AR156 and Bacillus subtilis strain SM21 on pepper growth and disease resistance. Biocontrol Sci Tech 24:1451–1468. doi:10.1080/09583157.2014.945899
Acknowledgments
We thank members of Professors Vivanco’s and Guo’s groups for technical assistance and helpful discussions. We especially thank Prof. Congfeng Song (Nanjing Agricultural University, China) and Dr. Azeddine Driouich (Universite’ de Rouen, France) for helpful suggestions. This work was supported by National Natural Science Foundation of China (No.31471812 and No.31171809) to JG, China Scholarship Council (No. 201206850028) to DZ, and by Colorado State University Agricultural Experiment Station.
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Table S1
Primers used for amplification of Bacillus cereus AR156 bioactivity genes. (PDF 442 kb)
Table S2
Root exudate data of Col-0 and Atabbc5 analyzed via GC-MS. Data is normalized by the internal standard Ribitol within sample. Field name is as follows [molecular weight (retention time followed by compound identification)]. (XLSX 82 kb)
Fig. S1
Effect of B. cereus AR156 on the shoot growth of 35 d-old Arabidopsis Col-0 and different ABC transporter mutants. (A) Shoot fresh weight was determined at 21 days after inoculation of B. cereus AR156. Asterisks indicate statistically significant differences between the treatments of a given mutants with or without AR156 (t-test; p<0.05). (B)The image represents plants at 21 days after inoculation. (GIF 74 kb)
Fig. S2
AR156 is not pathogenic to Atabcc5 and Col-0. The seedlings at 18 d-old were injected with Bacillus AR156 at a concentration of 2×108 CFU/mL on the leaf and incubated for 24 h. The control was inoculated with water. Each treatment contained 6 plants. (GIF 200 kb)
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Zhou, D., Huang, XF., Chaparro, J.M. et al. Root and bacterial secretions regulate the interaction between plants and PGPR leading to distinct plant growth promotion effects. Plant Soil 401, 259–272 (2016). https://doi.org/10.1007/s11104-015-2743-7
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DOI: https://doi.org/10.1007/s11104-015-2743-7