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Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes.

Banhara A, Ding Y, Kühner R, Zuccaro A, Parniske M - Front Plant Sci (2015)

Bottom Line: Here we show that intracellular colonization of root cells and intracellular sporulation by P. indica occurred in CSG mutants of the legume Lotus japonicus and in Arabidopsis thaliana, which belongs to the Brassicaceae, a family that has lost the ability to form AM as well as a core set of CSGs.A. thaliana mutants of homologs of CSGs (HCSGs) interacted with P. indica similar to the wild-type.Moreover, increased biomass of A. thaliana evoked by P. indica was unaltered in HCSG mutants.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biology, Institute of Genetics, University of Munich Martinsried, Germany.

ABSTRACT
Arbuscular mycorrhiza (AM) fungi (Glomeromycota) form symbiosis with and deliver nutrients via the roots of most angiosperms. AM fungal hyphae are taken up by living root epidermal cells, a program which relies on a set of plant common symbiosis genes (CSGs). Plant root epidermal cells are also infected by the plant growth-promoting fungus Piriformospora indica (Basidiomycota), raising the question whether this interaction relies on the AM-related CSGs. Here we show that intracellular colonization of root cells and intracellular sporulation by P. indica occurred in CSG mutants of the legume Lotus japonicus and in Arabidopsis thaliana, which belongs to the Brassicaceae, a family that has lost the ability to form AM as well as a core set of CSGs. A. thaliana mutants of homologs of CSGs (HCSGs) interacted with P. indica similar to the wild-type. Moreover, increased biomass of A. thaliana evoked by P. indica was unaltered in HCSG mutants. We conclude that colonization and growth promotion by P. indica are independent of the CSGs and that AM fungi and P. indica exploit different host pathways for infection.

No MeSH data available.


Related in: MedlinePlus

Quantification of P. indica in L. japonicus (A) and A. thaliana (B) wild-type and mutant roots. Real-time qPCR was used to quantify DNA from surface-washed P. indica-colonized roots at 14 dpi grown on modified HO medium using primers for the fungal gene Transcription Elongation Factor (TEF) and for A. thaliana and L. japonicus Ubiquitin (UBI) genes. Differences between the wild-type and mutants were investigated with a two-sided, unpaired t-test. *P < 0.05, **P < 0.01.
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Figure 3: Quantification of P. indica in L. japonicus (A) and A. thaliana (B) wild-type and mutant roots. Real-time qPCR was used to quantify DNA from surface-washed P. indica-colonized roots at 14 dpi grown on modified HO medium using primers for the fungal gene Transcription Elongation Factor (TEF) and for A. thaliana and L. japonicus Ubiquitin (UBI) genes. Differences between the wild-type and mutants were investigated with a two-sided, unpaired t-test. *P < 0.05, **P < 0.01.

Mentions: In order to quantify the relative fungal biomass within host roots, we determined the ratio between fungal DNA and plant DNA. Interestingly, in L. japonicus, we detected a tendency for an increased relative amount of fungal DNA in most of the tested common symbiosis mutants, with a significant difference to the wild-type in nup85-1, ccamk-13, and cyclops-3 (Figure 3). This higher ratio of fungal to plant DNA may be the result of increased fungal proliferation, reduced root growth, and/or plant cell death in the mutants. Curiously, this effect was only observed on L. japonicus but not on A. thaliana mutants (Figure 3). Our results reveal that CSG-mediated pathways affect the relative P. indica colonization level in L. japonicus, and that this regulation is not operational in A. thaliana. Interestingly, CSGs potentially have a cell protecting effect (Esseling et al., 2004; Genre et al., 2009; Evangelisti et al., 2014). Apart from its signaling role in symbiosis (Antolín-Llovera et al., 2014; Ried et al., 2014), SYMRK has been implicated in desensitization of root hair cells against mechanic stress (Esseling et al., 2004), and CCaMK increased tolerance against the cell killing effect of Colletotrichum (Genre et al., 2009). In a ccamk mutant of M. truncatula infected by the hemi-biotrophic fungal pathogen Colletotrichum trifolii, the switch from biotrophy to necrotrophy occurred earlier (Genre et al., 2009).


Colonization of root cells and plant growth promotion by Piriformospora indica occurs independently of plant common symbiosis genes.

Banhara A, Ding Y, Kühner R, Zuccaro A, Parniske M - Front Plant Sci (2015)

Quantification of P. indica in L. japonicus (A) and A. thaliana (B) wild-type and mutant roots. Real-time qPCR was used to quantify DNA from surface-washed P. indica-colonized roots at 14 dpi grown on modified HO medium using primers for the fungal gene Transcription Elongation Factor (TEF) and for A. thaliana and L. japonicus Ubiquitin (UBI) genes. Differences between the wild-type and mutants were investigated with a two-sided, unpaired t-test. *P < 0.05, **P < 0.01.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585188&req=5

Figure 3: Quantification of P. indica in L. japonicus (A) and A. thaliana (B) wild-type and mutant roots. Real-time qPCR was used to quantify DNA from surface-washed P. indica-colonized roots at 14 dpi grown on modified HO medium using primers for the fungal gene Transcription Elongation Factor (TEF) and for A. thaliana and L. japonicus Ubiquitin (UBI) genes. Differences between the wild-type and mutants were investigated with a two-sided, unpaired t-test. *P < 0.05, **P < 0.01.
Mentions: In order to quantify the relative fungal biomass within host roots, we determined the ratio between fungal DNA and plant DNA. Interestingly, in L. japonicus, we detected a tendency for an increased relative amount of fungal DNA in most of the tested common symbiosis mutants, with a significant difference to the wild-type in nup85-1, ccamk-13, and cyclops-3 (Figure 3). This higher ratio of fungal to plant DNA may be the result of increased fungal proliferation, reduced root growth, and/or plant cell death in the mutants. Curiously, this effect was only observed on L. japonicus but not on A. thaliana mutants (Figure 3). Our results reveal that CSG-mediated pathways affect the relative P. indica colonization level in L. japonicus, and that this regulation is not operational in A. thaliana. Interestingly, CSGs potentially have a cell protecting effect (Esseling et al., 2004; Genre et al., 2009; Evangelisti et al., 2014). Apart from its signaling role in symbiosis (Antolín-Llovera et al., 2014; Ried et al., 2014), SYMRK has been implicated in desensitization of root hair cells against mechanic stress (Esseling et al., 2004), and CCaMK increased tolerance against the cell killing effect of Colletotrichum (Genre et al., 2009). In a ccamk mutant of M. truncatula infected by the hemi-biotrophic fungal pathogen Colletotrichum trifolii, the switch from biotrophy to necrotrophy occurred earlier (Genre et al., 2009).

Bottom Line: Here we show that intracellular colonization of root cells and intracellular sporulation by P. indica occurred in CSG mutants of the legume Lotus japonicus and in Arabidopsis thaliana, which belongs to the Brassicaceae, a family that has lost the ability to form AM as well as a core set of CSGs.A. thaliana mutants of homologs of CSGs (HCSGs) interacted with P. indica similar to the wild-type.Moreover, increased biomass of A. thaliana evoked by P. indica was unaltered in HCSG mutants.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Biology, Institute of Genetics, University of Munich Martinsried, Germany.

ABSTRACT
Arbuscular mycorrhiza (AM) fungi (Glomeromycota) form symbiosis with and deliver nutrients via the roots of most angiosperms. AM fungal hyphae are taken up by living root epidermal cells, a program which relies on a set of plant common symbiosis genes (CSGs). Plant root epidermal cells are also infected by the plant growth-promoting fungus Piriformospora indica (Basidiomycota), raising the question whether this interaction relies on the AM-related CSGs. Here we show that intracellular colonization of root cells and intracellular sporulation by P. indica occurred in CSG mutants of the legume Lotus japonicus and in Arabidopsis thaliana, which belongs to the Brassicaceae, a family that has lost the ability to form AM as well as a core set of CSGs. A. thaliana mutants of homologs of CSGs (HCSGs) interacted with P. indica similar to the wild-type. Moreover, increased biomass of A. thaliana evoked by P. indica was unaltered in HCSG mutants. We conclude that colonization and growth promotion by P. indica are independent of the CSGs and that AM fungi and P. indica exploit different host pathways for infection.

No MeSH data available.


Related in: MedlinePlus