Indole-3-Acetaldoxime-Derived Compounds Restrict Root Colonization in the Beneficial Interaction Between <i>Arabidopsis</i> Roots and the Endophyte <i>Piriformospora indica</i>

Nongbri, Pyniarlang L.; Johnson, Joy Michal; Sherameti, Irena; Glawischnig, Erich; Halkier, Barbara Ann; Oelmüller, Ralf

doi:10.1094/mpmi-03-12-0071-r

Cited by 49 publications

(52 citation statements)

References 78 publications

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“…Since qRT-PCR changes in transcript abundance were marked 8 DPI for Lutea, and not until 22 DPI for CDC Bethune, this suggests constitutive defenses or mechanisms to delay the pathogen interaction in the later variety, as has been seen in other pathosystems (Lawrence et al, 2000). These two chitinases are presumed orthologs, of a class I basic chitinase (At3g12500) which was initially classified as a pathogen induced and defense-related protein (Passarinho and de Vries, 2002), and has shown upregulation in other systems upon pathogen incursion (Ascencio-Ibáñez et al, 2008; Nongbri et al, 2012). Therefore, the increase in the two orthologous chitinases represents a biomarker for F. oxysporum f. sp.…”

Section: Resultsmentioning

confidence: 99%

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Galindo‐González

Deyholos

2016

Front. Plant Sci.

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Fusarium oxysporum f. sp. lini is a hemibiotrophic fungus that causes wilt in flax. Along with rust, fusarium wilt has become an important factor in flax production worldwide. Resistant flax cultivars have been used to manage the disease, but the resistance varies, depending on the interactions between specific cultivars and isolates of the pathogen. This interaction has a strong molecular basis, but no genomic information is available on how the plant responds to attempted infection, to inform breeding programs on potential candidate genes to evaluate or improve resistance across cultivars. In the current study, disease progression in two flax cultivars [Crop Development Center (CDC) Bethune and Lutea], showed earlier disease symptoms and higher susceptibility in the later cultivar. Chitinase gene expression was also divergent and demonstrated and earlier molecular response in Lutea. The most resistant cultivar (CDC Bethune) was used for a full RNA-seq transcriptome study through a time course at 2, 4, 8, and 18 days post-inoculation (DPI). While over 100 genes were significantly differentially expressed at both 4 and 8 DPI, the broadest deployment of plant defense responses was evident at 18 DPI with transcripts of more than 1,000 genes responding to the treatment. These genes evidenced a reception and transduction of pathogen signals, a large transcriptional reprogramming, induction of hormone signaling, activation of pathogenesis-related genes, and changes in secondary metabolism. Among these, several key genes that consistently appear in studies of plant-pathogen interactions, had increased transcript abundance in our study, and constitute suitable candidates for resistance breeding programs. These included: an induced RPMI-induced protein kinase; transcription factors WRKY3, WRKY70, WRKY75, MYB113, and MYB108; the ethylene response factors ERF1 and ERF14; two genes involved in auxin/glucosinolate precursor synthesis (CYP79B2 and CYP79B3); the flavonoid-related enzymes chalcone synthase, dihydroflavonol reductase and multiple anthocyanidin synthases; and a peroxidase implicated in lignin formation (PRX52). Additionally, regulation of some genes indicated potential pathogen manipulation to facilitate infection; these included four disease resistance proteins that were repressed, indole acetic acid amido/amino hydrolases which were upregulated, activated expansins and glucanases, amino acid transporters and aquaporins, and finally, repression of major latex proteins.

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Section: Resultsmentioning

confidence: 99%

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Galindo‐González

Deyholos

2016

Front. Plant Sci.

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“…Under beneficial co-cultivation conditions, defense and stress genes including PDF1.2 are not upregulated in Arabidopsis roots 3 , 18 , 19 , 21 , 22 , 24 - 26 . However, Arabidopsis mutants, which are impaired in establishing a beneficial interaction or are unable to maintain a long-term harmony between the 2 symbionts, activate a mild defense response against P. indica 18 , 19 , 21 , 22 , 24 - 26 .…”

Section: Discussionmentioning

confidence: 99%

“…However, Arabidopsis mutants, which are impaired in establishing a beneficial interaction or are unable to maintain a long-term harmony between the 2 symbionts, activate a mild defense response against P. indica 18 , 19 , 21 , 22 , 24 - 26 . In particular, PDF1.2 has been reported repeatedly as being upregulated under these conditions 19 .…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, they could show that the ability to suppress host immunity is compromised in the jasmonate mutants jasmonate-insensitive 1 ( jin1 ) and jasmonate-resistant 1 ( jar1 ). We and others have shown that the mutualistic interaction is disturbed in Arabidopsis mutants with lesions in specific defense genes or signaling processes leading to defense gene activation 19 , 21 , 23 - 26 . Mutants with lesions in a specific defense response are often unable to restrict growth of P. indica hyphae in the roots, and consequently, the roots become overcolonized.…”

Section: Introductionmentioning

confidence: 99%

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Growth ofArabidopsisseedlings on high fungal doses ofPiriformospora indicahas little effect on plant performance, stress, and defense gene expression in spite of elevated jasmonic acid and jasmonic acid-isoleucine levels in the roots

Vahabi

Camehl

Sherameti³

et al. 2013

Plant Signaling & Behavior

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The endophytic fungus Piriformospora indica colonizes the roots of many plant species including Arabidopsis and promotes their performance, biomass, and seed production as well as resistance against biotic and abiotic stress. Imbalances in the symbiotic interaction such as uncontrolled fungal growth result in the loss of benefits for the plants and activation of defense responses against the microbe. We exposed Arabidopsis seedlings to a dense hyphal lawn of P. indica. The seedlings continue to grow, accumulate normal amounts of chlorophyll, and the photosynthetic parameters demonstrate that they perform well. In spite of high fungal doses around the roots, the fungal material inside the roots was not significantly higher when compared with roots that live in a beneficial symbiosis with P. indica. Fifteen defense- and stress-related genes including PR2, PR3, PAL2, and ERF1 are only moderately upregulated in the roots on the fungal lawn, and the seedlings did not accumulate H2O2/radical oxygen species. However, accumulation of anthocyanin in P. indica-exposed seedlings indicates stress symptoms. Furthermore, the jasmonic acid (JA) and jasmonic acid-isoleucine (JA-Ile) levels were increased in the roots, and consequently PDF1.2 and a newly characterized gene for a 2-oxoglurate and Fe2+-dependent oxygenase were upregulated more than 7-fold on the dense fungal lawn, in a JAR1- and EIN3-dependent manner. We conclude that growth of A. thaliana seedlings on high fungal doses of P. indica has little effect on the overall performance of the plants although elevated JA and JA-Ile levels in the roots induce a mild stress or defense response.

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“…Piriformospora indica , an endophytic fungus of Sebacinaceae, colonizes the roots of many plant species and promotes their growth and performance (Peškan-Berghöfer et al, 2004; Waller et al, 2005, 2008; Shahollari et al, 2007; Oelmüller et al, 2009; Camehl et al, 2010; Nongbri et al, 2012; Varma et al, 2012; Jogawat et al, 2013; Ye et al, 2014). The fungus improves nutrition uptake from the soil to the host roots (Sherameti et al, 2005; Shahollari et al, 2005; Kumar et al, 2011) suggesting a strong fungal influence on the plant transport processes and metabolism.…”

Section: Introductionmentioning

confidence: 99%

Piriformospora indica Reprograms Gene Expression in Arabidopsis Phosphate Metabolism Mutants But Does Not Compensate for Phosphate Limitation

et al. 2017

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Piriformospora indica is an endophytic fungus of Sebacinaceae which colonizes the roots of many plant species and confers benefits to the hosts. We demonstrate that approximately 75% of the genes, which respond to P. indica in Arabidopsis roots, differ among seedlings grown on normal phosphate (Pi) or Pi limitation conditions, and among wild-type and the wrky6 mutant impaired in the regulation of the Pi metabolism. Mapman analyses suggest that the fungus activates different signaling, transport, metabolic and developmental programs in the roots of wild-type and wrky6 seedlings under normal and low Pi conditions. Under low Pi, P. indica promotes growth and Pi uptake of wild-type seedlings, and the stimulatory effects are identical for mutants impaired in the PHOSPHATE TRANSPORTERS1;1, -1;2 and -1;4. The data suggest that the fungus does not stimulate Pi uptake, but adapts the expression profiles to Pi limitation in Pi metabolism mutants.

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Indole-3-Acetaldoxime-Derived Compounds Restrict Root Colonization in the Beneficial Interaction Between Arabidopsis Roots and the Endophyte Piriformospora indica

Cited by 49 publications

References 78 publications

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Growth ofArabidopsisseedlings on high fungal doses ofPiriformospora indicahas little effect on plant performance, stress, and defense gene expression in spite of elevated jasmonic acid and jasmonic acid-isoleucine levels in the roots

Piriformospora indica Reprograms Gene Expression in Arabidopsis Phosphate Metabolism Mutants But Does Not Compensate for Phosphate Limitation

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