Skip to main content

A Mixed Bag: The Plant Growth-Promoting Sebacina vermifera Impairs Defense Mechanisms Against Herbivores

  • Chapter
  • First Online:

Part of the book series: Soil Biology ((SOILBIOL,volume 33))

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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

    Article  CAS  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, Van Loon LC (2005) Induction of systemic resistance by Pseudomonas spp. Phytopathology 95:S145

    Google Scholar 

  • Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Barazani O, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J Chem Ecol 25:2397–2406

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Jones J (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  PubMed  CAS  Google Scholar 

  • Glick BR (1995) The enhancement of plant-growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Halitschke R, Baldwin IT (2005) Jasmonates and related compounds in plant-insect interactions. J Plant Growth Regul 23:238–245

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kepczynski J, Kepczynska E (1997) Ethylene in seed dormancy and germination. Physiol Plantarum 101:720–726

    Article  CAS  Google Scholar 

  • Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668

    Article  PubMed  CAS  Google Scholar 

  • Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844

    Article  PubMed  CAS  Google Scholar 

  • Kumari R, Kishan H, Bhoon YK, Varma A (2003) Colonization of cruciferous plants by Piriformospora indica. Curr Sci 85:1672–1674

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sahay NS, Varma A (1999) Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett 181:297–302

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shoji T, Nakajima K, Hashimoto T (2000) Ethylene suppresses jasmonate-induced gene expression in nicotine biosynthesis. Plant Cell Physiol 41:1072–1076

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant-herbivore interactions. J Plant Growth Regul 26:201–209

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ian Thomas Baldwin .

Editor information

Editors and Affiliations

Rights and permissions

Reprints 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

Publish with us

Policies and ethics