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Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata

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Abstract

A Sebacinales species was recovered from a clone library made from a pooled rhizosphere sample of Nicotiana attenuata plants from 14 native populations. Axenic cultures of the related species, Piriformospora indica and Sebacina vermifera, were used to examine their effects on plant performance. Inoculation of N. attenuata seeds with either fungus species stimulated seed germination and increased growth and stalk elongation. S. vermifera inoculated plants flowered earlier, produced more flowers and matured more seed capsules than did non-inoculated plants. Jasmonate treatment during rosette-stage growth, which slows growth and elicits herbivore resistance traits, erased differences in vegetative, but not reproductive performance resulting from S. vermifera inoculation. Total nitrogen and phosphorous contents did not differ between inoculated and control plants, suggesting that the performance benefits of fungal inoculation did not result from improvements in nutritional status. Since the expression of trypsin proteinase inhibitors (TPI), defensive proteins which confer resistance to attack from Manduca sexta larvae, incur significant growth and fitness costs for the plant, we examined the effect of S. vermifera inoculation on herbivore resistance and TPI activity. After 10 days of feeding on S. vermifera-inoculated plants, larval mass was 46% higher and TPI activity was 48% lower than that on non-inoculated plants. These results suggest that Sebacina spp. may interfere with defense signaling and allow plants to increase growth rates at the expense of herbivore resistance mediated by TPIs.

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References

  • Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272

    Article  CAS  Google Scholar 

  • Baldwin IT (2001) An ecologically motivated analysis of plant–herbivore interactions in native tobacco. Plant Physiol 127:1449–1458

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145

    Article  CAS  Google Scholar 

  • Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 82:3057–3068

    Google Scholar 

  • Bubner B, Gase K, Baldwin IT (2004) Two-fold differences are the detection limit for determining transgene copy numbers in plants by real-time PCR. BMC Biotechnol 4:1–11

    Article  CAS  Google Scholar 

  • van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27:547–568

    Article  PubMed  Google Scholar 

  • Gange AC (2001) Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol 150:611–618

    Article  Google Scholar 

  • Gange AC, Nice HE (1997) Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization. New Phytol 137:335–343

    Article  Google Scholar 

  • Gange AC, Stagg PG, Ward LK (2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol Lett 5:11–15

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  PubMed  CAS  Google Scholar 

  • Gehring CA, Whitham TG (1991) Herbivore-driven mycorrhizal mutualism in insect-susceptible pinyon pine. Nature 353:556–557

    Article  Google Scholar 

  • Gehring CA, Whitham TG (1995) Duration of herbivore removal and environmental-stress affect the ectomycorrhizae of pinyon pines. Ecology 76:2118–2123

    Article  Google Scholar 

  • Glawe GA, Zavala JA, Kessler A, Van Dam NM, Baldwin IT (2003) Ecological costs and benefits correlated with trypsin protease inhibitor production in Nicotiana attenuata. Ecology 84:79–90

    Article  Google Scholar 

  • Glen M, Tommerup IC, Bougher NL, O’Brien PA (2002) Are Sebacinaceae common and widespread ectomycorrhizal associates of Eucalyptus species in Australian forests? Mycorrhiza 12:243–247

    Article  PubMed  CAS  Google Scholar 

  • Goverde M, van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (2000) Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125:362–369

    Article  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422

    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, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid–amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125:711–717

    CAS  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  PubMed  CAS  Google Scholar 

  • Hogeweg P, Hesper B (1984) The alignment of sets of sequences and the construction of phylogenetic trees: an integrated method. J Mol Evol 20:175–186

    Article  PubMed  CAS  Google Scholar 

  • Käfer E (1977) Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv Genet 19:33–131

    Article  PubMed  Google Scholar 

  • Kaldorf M, Kuhn AJ, Schroder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728

    CAS  Google Scholar 

  • Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101:6285–6290

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago

    Google Scholar 

  • Keinanen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J Agric Food Chem 49:3553–3558

    Article  PubMed  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  PubMed  CAS  Google Scholar 

  • Kottke I, Beiter A, Weiss M, Haug I, Oberwinkler F, Nebel M (2003) Heterobasidiomycetes form symbiotic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycol Res 107:957–968

    Article  PubMed  Google Scholar 

  • Krügel T, Lim M, Gase K, Halitschke R, Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12:177–183

    Article  Google Scholar 

  • Kula AAR, Hartnett DC, Wilson GWT (2005) Effect of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions. Ecol Lett 8:61–69

    Article  Google Scholar 

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

    Google Scholar 

  • Little LR, Maun MA (1996) The “Ammophila problem” revisited: a role for mycorrhizal fungi. J Ecol 84:1–7

    Article  Google Scholar 

  • Lynds GY, Baldwin IT (1998) Fire, nitrogen, and defensive plasticity in Nicotiana attenuata. Oecologia 115:531–540

    Google Scholar 

  • Marulanda A, Azcon R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plantarum 119:526–533

    Article  CAS  Google Scholar 

  • McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435

    Article  CAS  Google Scholar 

  • Norman JR, Atkinson D, Hooker JE (1996) Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant Soil 185:191–198

    Article  CAS  Google Scholar 

  • van der Peer Y, De Watcher R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Peškan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelmüller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant–microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plantarum 122:465–477

    Article  CAS  Google Scholar 

  • Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128

    Article  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  PubMed  CAS  Google Scholar 

  • Read DJ (1998) Biodiversity: plants on the web. Nature 396:22–23

    Article  CAS  Google Scholar 

  • Regvar M, Gogala N, Zalar P (1996) Effects of jasmonic acid on mycorrhizal Allium sativum. New Phytol 134:703–707

    Article  CAS  Google Scholar 

  • Regvar M, Gogala N, Znidarsic N (1997) Jasmonic acid effects mycorrhization of spruce seedlings with Laccaria laccata. Trees Struct Funct 11:511–514

    Google Scholar 

  • Roda A, Halitschke R, Steppuhn A, Baldwin IT (2004) Individual variability in herbivore-specific elicitors from the plant’s perspective. Mol Ecol 13:2421–2433

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plantarum 95:472–478

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Palma JM (1996) Superoxide dismutase activity in arbuscular mycorrhizal Lactuca sativa plants subjected to drought stress. New Phytol 134:327–333

    Article  CAS  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcón R (2001) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. J Exp Bot 52:2241–2242

    PubMed  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 

  • Schittko U, Hermsmeier D, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs in response to insect-derived cues. Plant Physiol 125:701–710

    Article  PubMed  CAS  Google Scholar 

  • Selosse MA, Bauer R, Moyersoen B (2002a) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytol 155:183–195

    Article  CAS  Google Scholar 

  • Selosse MA, Weiss M, Jany JL, Tillier A (2002b) Communities and populations of sebacinoid basidiomycetes associated with the achlorophyllous orchid Neottia nidus-avis (L.) LCM Rich. and neighbouring tree ectomycorrhizae. Mol Ecol 11:1831–1844

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego, CA, USA

    Google Scholar 

  • Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide-sequences. Mol Biol Evol 1:269–285

    PubMed  CAS  Google Scholar 

  • Taylor DL, Bruns TD, Szaro TM, Hodges SA (2003) Divergence in mycorrhizal specialization within Hexalectris spicata (Orchidaceae), a nonphotosynthetic desert orchid. Am J Bot 90:1168–1179

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Trotta A, Varese GC, Gnavi E, Fusconi A, Sampo S, Berta G (1996) Interactions between the soilborne root pathogen Phytophthora nicotianae var parasitica and the arbuscular mycorrhizal fungus Glomus mosseae in tomato plants. Plant Soil 185:199–209

    Article  CAS  Google Scholar 

  • Urban A, Weiss M, Bauer R (2003) Ectomycorrhizas involving sebacinoid mycobionts. Mycol Res 107:3–14

    Article  PubMed  Google Scholar 

  • Varma A, Verma S, Sudha, Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    PubMed  CAS  Google Scholar 

  • Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Bütehorn B, Franken P (1998) Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90:896–903

    Article  CAS  Google Scholar 

  • Vicari M, Hatcher PE, Ayres PG (2002) Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 83:2452–2464

    Article  Google Scholar 

  • Warcup JH (1988) Mycorrhizal associations of isolates of Sebacina vermifera. New Phytol 110:227–231

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    Article  PubMed  Google Scholar 

  • Zavala JA, Baldwin IT (2004) Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecol 4:11 (DOI 10.1186/1472-6785-4-11)

    Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Hui DQ, Baldwin IT (2004a) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190

    Article  CAS  Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Baldwin IT (2004b) Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata. Proc Natl Acad Sci USA 101:1607–1612

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the Max-Planck-Gesellschaft for financial support of this study and Prof. A. Varma and Dr. P. Franken for providing us with the two fungal clones.

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Correspondence to Ian T. Baldwin.

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Communicated by Christian Koerner

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Barazani, O., Benderoth, M., Groten, K. et al. Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146, 234–243 (2005). https://doi.org/10.1007/s00442-005-0193-2

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