Abstract
Plant-derived root exudates modulate plant-microbe interactions and may play an important role in pathogen suppression. Root exudates may, for instance, directly inhibit pathogens or alter microbiome composition. Here, we tested if plants modulate their root exudation in the presence of a pathogen and if these shifts alter the rhizosphere microbiome composition. We added exudates from healthy and Ralstonia solanacearum-infected tomato plants to an unplanted soil and followed changes in bacterial community composition. The presence of pathogen changed the exudation of phenolic compounds and increased the release of caffeic acid. The amendment of soils with exudates from the infected plants led to a development of distinct and less diverse soil microbiome communities. Crucially, we could reproduce similar shift in microbiome composition by adding pure caffeic acid into the soil. Caffeic acid further suppressed R. solanacearum growth in vitro. We conclude that pathogen-induced changes in root exudation profile may serve to control pathogen both by direct inhibition and by indirectly shifting the composition of rhizosphere microbiome.
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References
Badri DV, Chaparro JM, Zhang R, Shen Q, 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 288:4502–4512. doi:10.1074/jbc.M112.433300
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
Bais HP, Park S-W, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32. doi:10.1016/j.tplants.2003.11.008
Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM (2005) Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434:217–221. doi:10.1038/nature09809
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
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. doi:10.1016/j.tplants.2012.04.001
Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068. doi:10.1890/0012-9658(2001)082[3057:DAMFAP]2.0.CO;2
Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M, Kitanidis PK, Jardine PM, Zhou J, Criddle CS, Marsh TL, Tiedje JM (2010) Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach. Appl Environ Microbiol 76:6778–6786. doi:10.1128/AEM.01097-10
Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant-Microbe Interact 28:1049–1058. doi:10.1094/MPMI-01-15-0016-R
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
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499. doi:10.1007/s00374-012-0691-4
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
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. doi:10.1038/nmeth.2604
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi:10.1093/bioinformatics/btr381
Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903. doi:10.1016/j.soilbio.2010.02.003
Etten EV (2005) Multivariate analysis of ecological data using CANOCO. Austral Ecol 30:486–487. doi:10.1111/j.1442-9993.2005.01433.x
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. doi:10.1890/05-1839
Garau G, Mele E, Castaldi P, Lauro GP, Deiana S (2015) Role of polygalacturonic acid and the cooperative effect of caffeic and malic acids on the toxicity of Cu(II) towards triticale plants (× Triticosecale Wittm). Biol Fertil Soils 51:535–544. doi:10.1007/s00374-015-0999-y
Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, Wallenstein MD, Brodie EL (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2:94. doi:10.3389/fmicb.2011.00094
Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. doi:10.1038/ismej.2008.80
Hood MI, Skaar EP (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10:525–537. doi:10.1038/nrmicro2836
Jacobs JM, Babujee L, Meng F, Milling A, Allen C (2012) The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. MBio 3:e00114–00112. doi:10.1128/mBio.00114-12
Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S (2011) Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol Plant-Microbe Interact 24:352–358. doi:10.1094/MPMI-09-10-0208
Lagos LM, Navarrete OU, Maruyama F, Crowley DE, Cid FP, Mora ML, Jorquera MA (2014) Bacterial community structures in rhizosphere microsites of ryegrass (Lolium perenne var. Nui) as revealed by pyrosequencing. Biol Fertil Soils 50:1253–1266. doi:10.1007/s00374-014-0939-2
Lanoue A, Burlat V, Henkes GJ, Koch I, Schurr U, Röse US (2009) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytol 185:577–588. doi:10.1111/j.1469-8137.2009.03066.x
Li X, Yn Z, Ding C, Jia Z, He Z, Zhang T, Wang X (2015) Declined soil suppressiveness to Fusarium oxysporum by rhizosphere microflora of cotton in soil sickness. Biol Fertil Soils 51:935–946. doi:10.1007/s00374-015-1038-8
Ling N, Huang Q, Guo S, Shen Q (2010) Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f. sp. niveum. Plant Soil 341:485–493. doi:10.1007/s11104-010-0660-3
Ling N, Zhang W, Wang D, Mao J, Huang Q, Guo S, Shen Q (2013) Root exudates from grafted-root watermelon showed a certain contribution in inhibiting Fusarium oxysporum f. sp. niveum. PLoS One 8:e63383. doi:10.1371/journal.pone.0063383
Lioussanne L, Perreault F, Jolicoeur M, St-Arnaud M (2010) The bacterial community of tomato rhizosphere is modified by inoculation with arbuscular mycorrhizal fungi but unaffected by soil enrichment with mycorrhizal root exudates or inoculation with Phytophthora nicotianae. Soil Biol Biochem 42:473–483. doi:10.1016/j.soilbio.2009.11.034
Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585. doi:10.1128/aem.01996-06
Milling A, Babujee L, Allen C (2011) Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS One 6:e15853. doi:10.1371/journal.pone.0015853
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
Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K, Turgeon BG (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836–2853. doi:10.1105/tpc.106.045633
Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610. doi:10.1111/j.1469-8137.2006.01931.x
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110:6548–6553. doi:10.1073/pnas.1302837110
Qiu M, Li S, Zhou X, Cui X, Vivanco JM, Zhang N, Shen Q, Zhang R (2013) De-coupling of root–microbiome associations followed by antagonist inoculation improves rhizosphere soil suppressiveness. Biol Fertil Soils 50:217–224. doi:10.1007/s00374-013-0835-1
Qu XH, Wang JG (2008) Effect of amendments with different phenolic acids on soil microbial biomass, activity, and community diversity. Appl Soil Ecol 39:172–179. doi:10.1016/j.apsoil.2007.12.007
Rodriguez A, Sanders IR (2015) The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J 9:1053–1061. doi:10.1038/ismej.2014.207
Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556. doi:10.1104/pp.108.127613
Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M, Billault A, Brottier P, Camus J, Cattolico L (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497–502. doi:10.1038/415497a
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09
Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K, Li J, Da Rocha UN, He Z, Pett-Ridge J, Brodie EL, Zhou J, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. MBio 6:e00746. doi:10.1128/mBio.00746-15
Trivedi P, He Z, Van Nostrand JD, Albrigo G, Zhou J, Wang N (2011) Huanglongbing alters the structure and functional diversity of microbial communities associated with citrus rhizosphere. ISME J 6:363–383. doi:10.1038/ismej.2011.100
Van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72. doi:10.1038/23932
Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562. doi:10.1111/j.1469-8137.2006.01854.x
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi:10.1128/AEM.00062-07
Wei Z, Yang X, Yin S, Shen Q, Ran W, Xu Y (2011) Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol 48:152–159. doi:10.1016/j.apsoil.2011.03.013
Xue C, Penton CR, Shen Z, Zhang R, Huang Q, Li R, Ruan Y, Shen Q (2015) Manipulating the banana rhizosphere microbiome for biological control of Panama disease. Sci Rep 5:11124. doi:10.1038/srep11124
Yu Z, Zhang Y, Luo W, Wang Y (2014) Root colonization and effect of biocontrol fungus Paecilomyces lilacinus on composition of ammonia-oxidizing bacteria, ammonia-oxidizing archaea and fungal populations of tomato rhizosphere. Biol Fertil Soils 51:343–351. doi:10.1007/s00374-014-0983-y
Zhou X, Wu F (2012) P-coumaric acid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f. Sp Cucumerinum owen. PLoS One 7:e48288. doi:10.1371/journal.pone.0048288
Acknowledgments
We thank Wu Xiong from Nanjing Agricultural University for help with bioinformatic analysis. Joana Falcao Salles from University of Groningen is acknowledged for providing helpful advices. This research was financially supported by the National Key Basic Research Program of China (2015CB150503), the National Natural Science Foundation of China (31501837, 41301262, 41471213), the Natural Science Foundation of Jiangsu Province (BK20130677), the 111 project (B12009), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions (Qirong Shen), the China Post-doctoral Science Foundation (2013M541687) and the Qing Lan Project (Yangchun Xu and Zhong Wei).
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Fig. S1
High-performance liquid chromatography (HPLC) profile of exudates originating from pathogen-only (RS; blue line), plant-only (Tomato; red line) and plant-and-pathogen together (Tomato + RS; green line) treatments. (GIF 31 kb)
Fig. S2
The relative abundance of the major bacterial phyla in the control, caffeic acid, plant-only (Tomato) and plant-and-pathogen (Tomato + RS) treatments. (GIF 58 kb)
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Gu, Y., Wei, Z., Wang, X. et al. Pathogen invasion indirectly changes the composition of soil microbiome via shifts in root exudation profile. Biol Fertil Soils 52, 997–1005 (2016). https://doi.org/10.1007/s00374-016-1136-2
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DOI: https://doi.org/10.1007/s00374-016-1136-2