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. 2009 Mar;4(3):215–216. doi: 10.4161/psb.4.3.7814

Induced resistance triggered by Piriformospora indica

Alexandra Molitor 1, Karl-Heinz Kogel 1,✉
PMCID: PMC2652532  PMID: 19721753

Abstract

The root endophytic Basidiomycete Piriformospora indica forms a specific type of mycorrhiza symbiosis with a broad spectrum of plant species, including the Brassicaceae. A recent report on the interaction of P. indica with Arabidopsis thaliana suggests that the fungus induces a mode of resistance to microbial pathogens reminiscent of Induced Systemic Resistance (ISR) first discovered with non-pathogenic rhizobacteria. The characteristics of P. indica mediated resistance are the dependency on JA-signalling and the cytosolic function of the master regulator protein Non-expressor-of-PR-genes 1 (NPR1), a low level of altered systemic gene expression in leaves before pathogen challenge, the induction of the JA-inducible marker gene vegetative storage protein 1 (VSP1) after pathogen challenge, and an independency of the resistance phenotype from salicylate biosynthesis and signalling. We discuss here two more factors regarding the P. indica-mediated ISR response: the role of the plant hormone ethylene as well as a possible contribution of the recently discovered close association of P. indica with the α-proteobacterium Rhizobium radiobacter.

Key words: induced systemic resistance, mycorrhiza, Piriformospora indica, powdery mildew, jasmonate, ethylene

Introduction

In addition to innate immunity and R gene-based resistance, induced resistance is one of the main mechanisms utilized by plants to protect themselves against a broad range of microbial pathogens. Certain biological or chemical agents can trigger this kind of resistance. In general, two forms of induced resistance are distinguished. The pathogen induced Systemic Acquired Resistance (SAR) refers to the case, in which non-infected parts of locally infected plants become more resistant to further infection.1 Induced Systemic Resistance (ISR) on the other hand is triggered by strains of non-pathogenic rhizobacteria.2–4 Next to rhizobacteria also certain fungi can systemically protect plants against infections by pathogens.5,6 Whereas SAR is based on salicylic acid (SA) synthesis and signalling, ISR by contrast often relies on an enhancement of jasmonate (JA)- and/or ethylene (ET)-dependent defence.7,8 Both mechanisms require the key regulator Non-expressor-of-PR-genes 1 (NPR1) though the biochemical mechanisms involving this protein are different in SAR and ISR.9

The here described root endophytic fungus Piriformospora indica belongs to the order Sebacinales (Basidiomycota)10 and forms a mutualistic symbiosis with a broad spectrum of host plants, such as barley, maize, Arabidopsis, tomato and tobacco.11–13 In barley the fungus induces resistance to root diseases and leads to systemic protection against powdery mildew caused by Blumeria graminis f. sp. hordei.14,15 Lately, we showed that P. indica similarly induces systemic resistance to Golovinomyces orontii in Arabidopsis.16

P. indica Induced Resistance Resembles ISR

P. indica-mediated resistance in Arabidopsis against the powdery mildew G. orontii shows clear parallels to JA and ET requiring ISR.16 The jasmonate-insensitive mutants jasmonate-resistant 1 (jar1-1)17 and jasmonate-insensitive 1 (jin 1)18 as well as the null mutant npr1-1 [Nonexpressor of pathogenesis-related (PR) genes 1, also known as NIM1]19 are compromised in P. indica-mediated resistance. All these mutants define genes known to be involved in JA signaling. By contrast, NahG plants expressing a bacterial salicylate-hydroxylase20 and the npr1-3 mutant, lacking the nuclear-localisation signal, were not affected in P. indica mediated resistance to G. orontii. Both of them are defective in salicylate-governed SAR. Hence, P. indica induced systemic resistance against powdery mildew requires the transcriptional regulator JIN1/AtMYC2, the JA signalling component JAR1 (a JA-amino synthetase)21 and the cytosolic function of NPR1, but does not require elevated SA levels nor the nuclear function of NPR1 (which is compromised in npr1-1 but not in npr1-3). Thus, the mutational analysis suggests that P. indica exploits mechanism known for ISR.

ISR is accompanied by a rather weak or even not detectable systemic up or downregulation of transcripts in the absence of a challenging pathogen.22,23 Accordingly, leaves of P. indica colonized and non-colonized plants showed comparable, non-induced levels of SA-, JA- and ET-responsive genes.16 Only after powdery mildew challenge a stronger expression of the JA-inducible vegetative storage protein gene VSP1 was observed exclusively in P. indica colonized plants. A similar response of Arabidopsis was described for a vegetative storage protein during rhizobacteria-induced ISR.24 The stronger VSP1 induction in P. indica colonized plants after pathogen challenge not only substantiates the role of JA in P. indica induced resistance. It also indicates a potentiated defence response of these plants, suggesting that “priming” is also associated with the P. indica symbiosis.

P. indica Induced Resistance is not Strongly Dependent on Ethylene Signalling

Ethylene has been shown to play a role during ISR for a variety but not all interactions between resistance-inducing bacteria and plants. While a requirement of the ethylene pathway has been reported for ISR conferred by Pseudomonas fluorescens WCS417r,7,25 ISR mediated by P. fluorescens CHA0r against Peronospora parasitica is independent of the ethylene receptor ETR1 and the downstream signalling component EIN2.26 Mutants defective in ETR1 or EIN2 are impaired in ethylene signalling.27,28 Preliminary results indicate that P. indica-mediated resistance might also be independent of ethylene signalling since the ISR response against G. orontii was not fully compromised in ein2-1 and etr1-3. In these experiments, the mutants showed a slight reduction of G. orontii conidiophores per mycelium in P. indica colonized plants. Moreover, the amount of G. orontii conidia formed 10 days after powdery mildew inoculation per mg of leaf fresh weight was also reduced. The interpretation of these data is complex since the penetration process and subsequent colonization of Arabidopsis roots is strongly influenced by the plant's ethylene biosynthesis and signalling (Schäfer et al., in preparation). An observed lower colonisation level in these mutants might lead to reduced ISR, which is consistent with the finding that the biological effects conferred to host plants is dependent on the concentration of P. indica inoculum (Jakobs S, Molitor A, Waller F unpublished).

Working in Concert: Bacterial Associations

The interpretation of the biological activity conferred by P. indica to host plants is further complicated by the fact that all Sebacinales so far investigated are associated with bacteria.29 For P. indica a close association to the α-proteobacterium Rhizobium radiobacter has been demonstrated. Although all attempts to cure P. indica from these bacteria failed, it was possible to produce R. radiobacter in pure culture. In experiments examining the biological activity of R. radiobacter in barley, Sharma et al.29 proved the potential of the bacteria to induce growth promotion and systemic resistance to barley powdery mildew. In addition, the bacterium induced systemic resistance in Arabidopsis against G. orontii.30 Consistent with the results obtained for P. indica-mediated resistance, a screen of Arabidopsis mutants indicated a requirement of JA and the cytosolic function of NPR1 but no requirement for SA-signalling during R. radiobacter-mediated resistance.30 Comparing fungal and bacterial effects the biological activity exerted by P. indica in association with R. radiobacter as compared with the pure bacterium could hardly be distinguished. Especially the individual impact of the fungus and the bacterium on the observed ISR responses, the interplay between the two microorganisms, and their additive impact on their host remain to be elucidated.

Addendum to: Stein E, Molitor A, Kogel KH, Waller F. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol. 2008;49:1747–1751. doi: 10.1093/pcp/pcn147.

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/7814

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