Abstract
Belowground interactions of plants with beneficial plant growth-promoting microorganisms (PGPM) enhance plant growth and fitness and can alter a plant’s ability to cope with its environment. By increasing plant nutritional uptake, PGPM may indirectly enhance a plant’s ability to withstand harsh conditions. However, very often the mode of action of PGPM involves interference with a plant’s hormonal balance, which may have either positive or negative effects on a plant’s interactions with biotic and abiotic stressors. Here we discuss the possibility that the outcome of associating with the genetically similar Sebacina vermifera and Piriformospora indica fungi involves increases in a plant’s susceptibility to herbivores. Defense mechanisms against herbivores are mainly regulated by jasmonic acid and its fine-tuned cross talk with other phytohormones. Thus, the ability of the Sebacinales fungi to produce IAA and shut down defenses against microorganisms by interfering with ethylene synthesis can result in promoting growth effects but at a cost to defense-related signaling pathways. That growth promotion comes at the expense of resistance to herbivore attack calls into question the mutualistic nature of the interaction with these fungi.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209
Bakker PAHM, Pieterse CMJ, Van Loon LC (2005) Induction of systemic resistance by Pseudomonas spp. Phytopathology 95:S145
Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243
Baldwin IT, Morse L (1994) Up in smoke. 2. Germination of Nicotiana attenuata in response to smoke-derived cues and nutrients in burned and unburned soils. J Chem Ecol 20:2373–2391
Baldwin IT, Staszakkozinski L, Davidson R (1994) Up in smoke. 1. Smoke-derived germination cues for postfire annual, Nicotiana attenuata Torr Ex Watson. J Chem Ecol 20:2345–2371
Barazani O, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J Chem Ecol 25:2397–2406
Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146:234–243
Barazani O, Von Dahl CC, Baldwin IT (2007) Sebacina vermifera promotes the growth and fitness of Nicotiana attenuata by inhibiting ethylene signaling. Plant Physiol 144:1223–1232
Bari R, Jones J (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Barriuso J, Solano BR, Manero FJG (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp on Arabidopsis thaliana. Phytopathology 98:666–672
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18
Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503
Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, Oelmuller R (2010) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185:1062–1073
Cui JP, Jander G, Racki LR, Kim PD, Pierce NE, Ausubel FM (2002) Signals involved in Arabidopsis resistance to Trichoplusia ni caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae. Plant Physiol 129:551–564
De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937
Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755
Farwell AJ, Vesely S, Nero V, Rodriguez H, McCormack K, Shah S, Dixon DG, Glick BR (2007) Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal-contaminated field site. Environ Pollut 147:540–545
Frey-Klett P, Churin JL, Pierrat JC, Garbaye J (1999) Dose effect in the dual inoculation of an ectomycorrhizal fungus and a mycorrhiza helper bacterium in two forest nurseries. Soil Biol Biochem 31:1555–1562
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Glick BR (1995) The enhancement of plant-growth by free-living bacteria. Can J Microbiol 41:109–117
Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7
Glick BR, Penrose DM, Li JP (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68
Glick BR, Todorovic B, Czarny J, Cheng ZY, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242
Grichko VP, Glick BR (2001) Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35S, rolD or PRB-1b promoter. Plant Physiol Biochem 39:19–25
Grichko VP, Filby B, Glick BR (2000) Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd, Co, Cu, Ni, Pb, and Zn. J Biotechnol 81:45–53
Gurska J, Wang WX, Gerhardt KE, Khalid AM, Isherwood DM, Huang XD, Glick BR, Greenberg BM (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43:4472–4479
Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M (2001) The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plantarum 111:206–211
Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807
Halitschke R, Baldwin IT (2005) Jasmonates and related compounds in plant-insect interactions. J Plant Growth Regul 23:238–245
Halitschke R, Gase K, Hui DQ, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131:1894–1902
Heidel AJ, Barazani O, Baldwin IT (2010) Interaction between herbivore defense and microbial signaling: bacterial quorum-sensing compounds weaken JA-mediated herbivore resistance in Nicotiana attenuata. Chemoecology 20:149–154
Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410
Jia YJ, Kakuta Y, Sugawara M, Igarashi T, Oki N, Kisaki M, Shoji T, Kanetuna Y, Horita T, Matsui H, Honma M (1999) Synthesis and degradation of 1-aminocyclopropane-1-carboxylic acid by Penicillium citrinum. Biosci Biotechnol Biochem 63:542–549
Kahl J, Siemens DH, Aerts RJ, Gaebler R, Kuehnemann F, Preston CA, Baldwin IT (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342
Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320
Kepczynski J, Kepczynska E (1997) Ethylene in seed dormancy and germination. Physiol Plantarum 101:720–726
Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668
Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844
Kumari R, Kishan H, Bhoon YK, Varma A (2003) Colonization of cruciferous plants by Piriformospora indica. Curr Sci 85:1672–1674
Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS One 3:e2702
Long HH, Sonntag DG, Schmidt DD, Baldwin IT (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuata is organized by soil composition and host plant ethylene production and perception. New Phytol 185:554–567
Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278
Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530
Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572
Meharg AA, Killham K (1995) Loss of exudates from the roots of perennial ryegrass inoculated with a range of microorganisms. Plant Soil 170:345–349
O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917
Onkokesung N, Galis I, von Dahl CC, Matsuoka K, Saluz HP, Baldwin IT (2010) Jasmonic acid and ethylene modulate local responses to wounding and simulated herbivory in Nicotiana attenuata leaves. Plant Physiol 153:785–798
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 Hort 111:38–43
Pierik R, Visser EJW, De Kroon H, Voesenek LACJ (2003) Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ 26:1229–1234
Pierik R, Voesenek LACJ, de Kroon H, Visser EJW (2004) Density-induced plant size reduction and size inequalities in ethylene-sensing and ethylene-insensitive tobacco. Plant Biol 6:201–205
Pierik R, Djakovic-Petrovic T, Keuskamp DH, de Wit M, Voesenek LACJ (2009) Auxin and ethylene regulate elongation responses to neighbor proximity signals independent of gibberellin and DELLA proteins in Arabidopsis. Plant Physiol 149:1701–1712
Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569
Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, Leon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Van der Sluis I, Bakker PAHM, Van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signalling and expression. Eur J Plant Pathol 107:51–61
Rai M, Varma A (2005) Arbuscular mycorrhiza-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasica Nees. Electronic J Biotechnol 8:107–112
Riedel T, Groten K, Baldwin IT (2008) Symbiosis between Nicotiana attenuata and Glomus intraradices: ethylene plays a role, jasmonic acid does not. Plant Cell Environ 31:1203–1213
Ryu CM, Hu CH, Locy RD, Kloepper JW (2005) Study of mechanisms for plant growth promotion elicited by rhizobacteria in Arabidopsis thaliana. Plant Soil 268:285–292
Sahay NS, Varma A (1999) Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett 181:297–302
Sergeeva E, Shah S, Glick BR (2006) Growth of transgenic canola (Brassica napus cv. Westar) expressing a bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene on high concentrations of salt. World J Microbiol Biotechnol 22:277–282
Shoji T, Nakajima K, Hashimoto T (2000) Ethylene suppresses jasmonate-induced gene expression in nicotine biosynthesis. Plant Cell Physiol 41:1072–1076
Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light: Piriformospora indica - a revolutionary plant growth promoting fungus. Curr Sci 79:1548–1554
Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847
Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268
Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235
Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novak O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant Microbe Interact 21:1371–1383
van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483
Varma A, Verma S, Sudha SN, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant-herbivore interactions. J Plant Growth Regul 26:201–209
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391
Wang YQ, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Interact 18:385–396
Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125:2189–2202
Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida CR12-2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71
Zavala JA, Patankar AG, Gase K, Baldwin IT (2004a) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612
Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT (2004b) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Barazani, O., Baldwin, I.T. (2013). A Mixed Bag: The Plant Growth-Promoting Sebacina vermifera Impairs Defense Mechanisms Against Herbivores. In: Varma, A., Kost, G., Oelmüller, R. (eds) Piriformospora indica. Soil Biology, vol 33. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33802-1_15
Download citation
DOI: https://doi.org/10.1007/978-3-642-33802-1_15
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-33801-4
Online ISBN: 978-3-642-33802-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)