Systemic Resistance in Arabidopsis Conferred by the Mycorrhizal Fungus Piriformospora indica Requires Jasmonic Acid Signaling and the Cytoplasmic Function of NPR1

Stein, Elke; Molitor, Alexandra; Kogel, Karl‐Heinz; Waller, Frank

doi:10.1093/pcp/pcn147

Cited by 259 publications

(193 citation statements)

References 24 publications

Supporting

Mentioning

180

Contrasting

Unclassified

Order By: Relevance

“…6). In contrast to our prior results (Stein et al, 2008), npr1-1 did not exhibit an altered colonization in five independent experiments. Since previously our Figure 8.…”

Section: Discussioncontrasting

confidence: 99%

Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the FungusPiriformospora indica

Jacobs

Zechmann

Molitor³

et al. 2011

Plant Physiology

Self Cite

287

313

View full text Add to dashboard Cite

Piriformospora indica is a root-colonizing basidiomycete that confers a wide range of beneficial traits to its host. The fungus shows a biotrophic growth phase in Arabidopsis (Arabidopsis thaliana) roots followed by a cell death-associated colonization phase, a colonization strategy that, to our knowledge, has not yet been reported for this plant. P. indica has evolved an extraordinary capacity for plant root colonization. Its broad host spectrum encompasses gymnosperms and monocotyledonous as well as dicotyledonous angiosperms, which suggests that it has an effective mechanism(s) for bypassing or suppressing host immunity. The results of our work argue that P. indica is confronted with a functional root immune system. Moreover, the fungus does not evade detection but rather suppresses immunity triggered by various microbe-associated molecular patterns. This ability to suppress host immunity is compromised in the jasmonate mutants jasmonate insensitive1-1 and jasmonate resistant1-1. A quintuple-DELLA mutant displaying constitutive gibberellin (GA) responses and the GA biosynthesis mutant ga1-6 (for GA requiring 1) showed higher and lower degrees of colonization, respectively, in the cell death-associated stage, suggesting that P. indica recruits GA signaling to help establish proapoptotic root cell colonization. Our study demonstrates that mutualists, like pathogens, are confronted with an effective innate immune system in roots and that colonization success essentially depends on the evolution of strategies for immunosuppression.

show abstract

“…6). In contrast to our prior results (Stein et al, 2008), npr1-1 did not exhibit an altered colonization in five independent experiments. Since previously our Figure 8.…”

Section: Discussioncontrasting

confidence: 99%

Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the FungusPiriformospora indica

Jacobs

Zechmann

Molitor³

et al. 2011

Plant Physiology

Self Cite

287

313

View full text Add to dashboard Cite

show abstract

“…RrF4 mediates ISR to Pseudomonas syringae P. indica-induced resistance in Arabidopsis against the powdery mildew fungus Golovinomyces orontii involved the activation of the ISR pathway (Stein et al, 2008). To assess whether RrF4 induces ISR, Arabidopsis mutants indicative of SA signaling (SAdegrading SA hydroxylase (NahG), non-expressor of PR 1-3 (npr1-3)), JA signaling (jasmonate-responsive 1-1 (jar1-1), jasmonate-insensitive 1 (jin1), npr1-1), and ethylene signaling (ethylene insensitive 2-1 (ein2-1)) were assessed for RrF4-mediated resistance to Pseudomonas syringae pv.…”

Section: Plant Defense Gene Expression In Response To Rrf4mentioning

confidence: 99%

“…Since its discovery in the Indian Thar dessert in 1996 (Varma et al, 1999), P. indica and related Sebacina vermifera strains were shown to promote biomass, yield and health of a broad spectrum of plants (Varma et al, 2012;Ye et al, 2014). Genetic and biochemical assessments of the resistance mechanism that is induced by P. indica in Arabidopsis thaliana (Arabidopsis) against a wide spectrum of leaf and root pathogens showed a requirement of jasmonate synthesis and signaling and thus an operable induced systemic resistance (ISR) pathway (Stein et al, 2008;Jacobs et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

et al. 2015

Self Cite

View full text Add to dashboard Cite

The Alphaproteobacterium Rhizobium radiobacter F4 (RrF4) was originally characterized as an endofungal bacterium in the beneficial endophytic Sebacinalean fungus Piriformospora indica. Although attempts to cure P. indica from RrF4 repeatedly failed, the bacterium can easily be grown in pure culture. Here, we report on RrF4's genome and the beneficial impact the free-living bacterium has on plants. In contrast to other endofungal bacteria, the genome size of RrF4 is not reduced. Instead, it shows a high degree of similarity to the plant pathogenic R. radiobacter (formerly: Agrobacterium tumefaciens) C58, except vibrant differences in both the tumor-inducing (pTi) and the accessor (pAt) plasmids, which can explain the loss of RrF4's pathogenicity. Similar to its fungal host, RrF4 colonizes plant roots without host preference and forms aggregates of attached cells and dense biofilms at the root surface of maturation zones. RrF4-colonized plants show increased biomass and enhanced resistance against bacterial leaf pathogens. Mutational analysis showed that, similar to P. indica, resistance mediated by RrF4 was dependent on the plant's jasmonate-based induced systemic resistance (ISR) pathway. Consistent with this, RrF4-and P. indica-induced pattern of defense gene expression were similar. In clear contrast to P. indica, but similar to plant growth-promoting rhizobacteria, RrF4 colonized not only the root outer cortex but also spread beyond the endodermis into the stele. On the basis of our findings, RrF4 is an efficient plant growth-promoting bacterium.

show abstract

“…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.…”

Section: P Indica Induced Resistance Resembles Isrmentioning

confidence: 97%

“…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.…”

mentioning

confidence: 99%

Induced resistance triggered byPiriformospora indica

Molitor

Kogel²

2009

Plant Signaling & Behavior

Self Cite

View full text Add to dashboard Cite

ling, 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][12][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 ISRP. 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-hydroxylase 20 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 [Plant Signaling & Behavior 4:3, 215-216; March 2009] ; ©2009 Landes BioscienceThe 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 Ar...

show abstract

Systemic Resistance in Arabidopsis Conferred by the Mycorrhizal Fungus Piriformospora indica Requires Jasmonic Acid Signaling and the Cytoplasmic Function of NPR1

Cited by 259 publications

References 24 publications

Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the FungusPiriformospora indica

Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the FungusPiriformospora indica

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

Induced resistance triggered byPiriformospora indica

Contact Info

Product

Resources

About