Abstract
Plants are confronted with an ever-changing spectrum of pathogenic and mutualistic microbes among which a considerable number possess the ability to colonize plant roots. Root pathogens cause the most devastating diseases whose control is mostly unsuccessful in agricultural ecosystems due to the limited access of roots for chemical protection strategies and the unavailability of resistant germplasms. Roots are also colonized by mutualistic microbes such as mycorrhizal fungi or nitrogen-fixing bacteria. It is currently almost unknown how plants discriminate between harmful and beneficial root colonizers. Recent studies demonstrated the existence of a root innate immune system, whose organization shows high similarities to leaf innate immunity and which is also activated after recognition of microbe-associated molecular patterns. Within this review, we will introduce the current knowledge of root innate immunity in pathogenic and mutualistic plant–microbe interactions. We will put emphasis on the colonization strategy of the mutualistic fungus Piriformospora indica and describe its immune-suppressing activity in roots, which is essentially required to colonize roots.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 6:91–94
Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 8:2117–29
Adie BAT, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano J, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681
Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983
Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, Boller T, Molinaro A, Jackson RW, Cooper RM (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol 10:375–87
Asselbergh B, De Vleesschauwer D, Höfte M (2008) Global switches and fine-tuning-ABA modulates plant pathogen defense. Mol Plant Microbe Interact 21:709–19
Attard A, Gourgues M, Callemeyn-Torre N, Keller H (2010) The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection. New Phytol 187:449–60
Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, Hammes UZ, Börnke F (2009) The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Mol Plant Microbe Interact 22:655–64
Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2:101–6
Berrocal-Lobo M, Molina A (2004) Ethylene response factor 1 mediates Arabidopsis resistance to the soilborne fungus Fusarium oxysporum. Mol Plant Microbe Interact 17:763–70
Blechert O, Kost G, Hassel A, Rexer RH, Varma A (1999) First remarks on the symbiotic interactions between Piriformospora indica and terrestrial orchid. In: Varme A, Hock B (eds) Mycorrhizae, 2nd edn. Springer, Germany
Blee KA, Anderson AJ (1996) Defense related transcript accumulation in Phaseolus vulgar L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices. Plant Physiol 10:675–688
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–22
Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2010) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502–7
Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol 6:629–639
Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 5:e1002051
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host–microbe interactions: shaping the evolution of the plant immune response. Cell 24:803–14
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 2:95–101
Deguchi Y, Banba M, Shimoda Y, Chechetka SA, Suzuri R, Okusako Y, Ooki Y, Toyokura K, Suzuki A, Uchiumi T, Higashi S, Abe M, Kouchi H, Izui K, Hata S (2007) Transcriptome profiling of Lotus japonicus roots during arbuscular mycorrhiza development and comparison with that of nodulation. DNA Res 14:117–33
Deshmukh S, Kogel KH (2007) Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J Plant Dis Protect 114:263–268
Deshmukh S, Hückelhoven R, Schäfer P, Imani J, Sharma M, Weiß M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA 103:18450–18457
Ding Y, Oldroyd GE (2009) Positioning the nodule, the hormone dictum. Plant Signal Behav 4:89–93
El Gueddari NE, Rauchhaus U, Moerschbacher BM, Deising HB (2002) Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 156:103–112
Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–76
Felle HH, Waller F, Molitor A, Kogel KH (2009) The mycorrhiza fungus Piriformospora indica induces fast root-surface pH signaling and primes systemic alkalinization of the leaf apoplast upon powdery mildew infection. Mol Plant Microbe Interact 9:1179–85
Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 5:373–9
Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44
García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–86
Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–27
Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 19:8955–9
Golotte A, Gianinazzi-Pearson V, Giovanetti M, Sbrana C, Avio L, Gianinazzi S (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a ‘locus a’ myc − mutant of Pisum sativum L. Planta 191:112–122
Golotte A, Gianinazzi-Pearson V, Gianinazzi S (1995) Immunodetection of infection thread glycoprotein and arabinogalactan protein in wild type Pisum sativum (L.) or an isogenic mycorrhiza-resistant mutant interacting with Glomus mosseae. Symbiosis 18:69–85
Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–11
Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 3:277–84
Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–72
Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–99
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–10
He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nürnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575
Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–64
Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol 196:520–534
Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–301
Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V, Kogel KH, Schaefer P (2011) Broad spectrum suppression of innate immunity is required for colonization of Arabidopsis thaliana roots by the fungus Piriformospora indica. Plant Physiol. doi:10.1104/pp.111.176446
Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222–226
Johansson A, Staal J, Dixelius C (2006) Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR1 and RFO1. Mol Plant Microbe Interact 9:958–69
Jones JD, Dangl JL (2006) The plant immune system. Nature 16:323–9
Khatabi B, Molitor A, Lindermayr C, Pfiffi S, Durner J, von Wettstein D, Kogel KH, Schäfer P (2012) Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLoS One 7:e35502
Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209
Lambais MR, Mehdy MC (1995) Differential expression of defense-related genes in arbuscular mycorrhiza. Can J Bot 3:533–540
Lambais MR, Mehdy MC (1998) Spatial distribution of chitinases and 1,3-glucanase transcripts in bean arbuscular mycorrhizal roots under low and high soil phosphate conditions. New Phytol 140:33–42
Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310:1180–3
Liu Y, Schiff M, Dinesh-Kumar SP (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 38:800–9
Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902–17
Mabood F, Souleimanov A, Khan W, Smith DL (2006) Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol Biochem 44:759–765
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 8:969–80
Mersmann S, Bourdais G, Rietz S, Robatzek S (2010) Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400
Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990
Miya A, Albert P, Shiny T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618
Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–28
Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JDG (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655
Nomura K, Melotto M, He SY (2005) Suppression of host defense in compatible plant-Pseudomonas syringae interactions. Curr Opin Plant Biol 4:361–8
Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY (2006) A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–223
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–46
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–75
Peskan-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 Plant 122:465–477
Petutschnig EK, Jones AM, Serazetdinova L, Lipka U, Lipka V (2010) The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J Biol Chem 37:28902–11
Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–16
Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, de Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 3:683–701
Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P (2012) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24:794–809
Rosas S, Soria R, Correa N, Abdala G (1998) Jasmonic acid stimulates the expression of nod genes in rhizobium. Plant Mol Biol 38:1161–1168
Salzer P, Boller T (2000) Elicitor-induced reactions in mycorrhizae and their suppression. In: Podila GK, Douds DD Jr (eds) Current advances in mycorrhizae research. APS Press, St. Paul, Minnesota
Salzer P, Corbiere H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319–325
Scervino JM, Ponce MA, Erra-Bassells R, Bompadre J, Vierheilig H, Ocampo JA, Godeas A (2007) The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Can J Microbiol 53:702–9
Schäfer P, Kogel KH (2009) The sebacinoid fungus Piriformospora indica: an orchid mycorrhiza which may increase host plant reproduction and fitness. In: Deising HB, Esser K (eds) The mycota, vol 5, Plant relationships. Springer, Heidelberg, pp 99–112
Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler PM, Waller F, Scholz U, Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–74
Schlink K (2010) Down-regulation of defense genes and resource allocation into infected roots as factors for compatibility between Fagus sylvatica and Phytophthora citricola. Funct Integr Genomics 2:253–64
Schulze-Lefert P, Panstruga R (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16:117–25
Sesma A, Osbourn AE (2004) The rice leaf blast pathogen undergoes developmental processes typical of root-infecting fungi. Nature 431:582–586
Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 17:17–27
Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant Microbe Interact 6:799–807
Silipo A, Sturiale L, Garozzo D, Erbs G, Jensen TT, Lanzetta R, Dow JM, Parrilli M, Newman MA, Molinaro A (2008) The acylation and phosphorylation pattern of lipid A from Xanthomonas campestris strongly influence its ability to trigger the innate immune response in Arabidopsis. Chembiochem 14:896–904
Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–51
Sun J, Cardoza V, Mitchell DM, Bright L, Oldroyd GED, Harris JM (2006) Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J 46:961–970
Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939
Trujillo M, Ichimura K, Casais C, Shirasu K (2008) Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol 18:1396–401
Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 12:e1000772
Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, Scheel D, Lee J, Oelmüller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 2:193–206
Varma A, Verma S, Sudha SN, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Verma S, Varma A, Rexer K-H, 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 90:898–905
Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J (1998) A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA 95:7209–7214
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neuman 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 L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J (2009) Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5:e1000301
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
Weiß M, Sýkorová Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F, Bauer R, Redecker D (2011) Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS One 6:e16793
Wigchert SC, Kuiper E, Boelhouwer GJ, Nefkens GH, Verkleij JA, Zwanenburg B (1999) Dose–response of seeds of the parasitic weeds Striga and Orobanche toward the synthetic germination stimulants GR 24 and Nijmegen 1. J Agric Food Chem 47:1705–10
Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou JM (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 8:74–80
Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 20:26532–44
Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007a) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185
Zhang J, Subramanian S, Zhang Y, Yu O (2007b) Flavone synthases from Medicago truncatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol 144:741–751
Zhao SZ, Qi XQ (2008) Signaling in plant disease resistance and symbiosis. J Integr Plant Biol 50:799–807
Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 19:749–60
Zuccaro A, Basiewicz M, Zurawska M, Biedenkopf D, Kogel KH (2009) Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica. Fungal Genet Biol 46:543–550
Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:e1002290
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
Jacobs, S., Kogel, KH., Schäfer, P. (2013). Root-Based Innate Immunity and Its Suppression by the Mutualistic Fungus Piriformospora indica . 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_13
Download citation
DOI: https://doi.org/10.1007/978-3-642-33802-1_13
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)