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Mutualism-parasitism paradigm synthesized from results of root-endophyte models.

Mandyam KG, Jumpponen A - Front Microbiol (2015)

Bottom Line: Despite the high frequency and suspected ecological importance, the effects of DSE colonization on plant growth and performance have remained unclear.These data highlight the context dependency of the DSE symbioses: not only plant species but also ecotypes vary in their responses to populations of conspecific DSE fungi - environmental conditions further shift the host responses similar to those predicted based on the mutualism-parasitism-continuum paradigm.The model systems provide several established avenues of inquiry that permit more detailed molecular and functional dissection of fungal endophyte symbioses, identifying thus likely mechanisms that may underlie the observed host responses to endophyte colonization.

View Article: PubMed Central - PubMed

Affiliation: Department of Agriculture, Alcorn State University Lorman, MS, USA.

ABSTRACT
Plant tissues host a variety of fungi. One important group is the dark septate endophytes (DSEs) that colonize plant roots and form characteristic intracellular structures - melanized hyphae and microsclerotia. The DSE associations are common and frequently observed in various biomes and plant taxa. Reviews suggest that the proportion of plant species colonized by DSE equal that colonized by AM and microscopic studies show that the proportion of the root system colonized by fungi DSE can equal, or even exceed, the colonization by AM fungi. Despite the high frequency and suspected ecological importance, the effects of DSE colonization on plant growth and performance have remained unclear. Here, we draw from over a decade of experimentation with the obscure DSE symbiosis and synthesize across large bodies of published and unpublished data from Arabidopsis thaliana and Allium porrum model systems as well as from experiments that use native plants to better resolve the host responses to DSE colonization. The data indicate similar distribution of host responses in model and native plant studies, validating the use of model plants for tractable dissection of DSE symbioses. The available data also permit empirical testing of the environmental modulation of host responses to DSE colonization and refining the "mutualism-parasitism-continuum" paradigm for DSE symbioses. These data highlight the context dependency of the DSE symbioses: not only plant species but also ecotypes vary in their responses to populations of conspecific DSE fungi - environmental conditions further shift the host responses similar to those predicted based on the mutualism-parasitism-continuum paradigm. The model systems provide several established avenues of inquiry that permit more detailed molecular and functional dissection of fungal endophyte symbioses, identifying thus likely mechanisms that may underlie the observed host responses to endophyte colonization.

No MeSH data available.


Responses of three Arabidopsis thaliana accessions (Col-0, Cvi-1, Kin-1) to inoculation with 25 strains of Periconia macrospinosa. The analyses follow those described in Mandyam et al. (2013). Response (R) to inoculation indicates the difference between the control and inoculated plants relative to control (inoculated < control) or inoculated plants (control < inoculated; Klironomos, 2003). Values above x-axis indicate a positive response, values below negative. Gray arrows indicate responses consistent across the three accessions, black arrows responses that range from negative to positive depending on the host accession. Asterisks indicate significant difference between the control and inoculated plants (ANOVA, P < 0.05). Figure is redrawn from Figure 2 in Mandyam et al. (2013).
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Figure 3: Responses of three Arabidopsis thaliana accessions (Col-0, Cvi-1, Kin-1) to inoculation with 25 strains of Periconia macrospinosa. The analyses follow those described in Mandyam et al. (2013). Response (R) to inoculation indicates the difference between the control and inoculated plants relative to control (inoculated < control) or inoculated plants (control < inoculated; Klironomos, 2003). Values above x-axis indicate a positive response, values below negative. Gray arrows indicate responses consistent across the three accessions, black arrows responses that range from negative to positive depending on the host accession. Asterisks indicate significant difference between the control and inoculated plants (ANOVA, P < 0.05). Figure is redrawn from Figure 2 in Mandyam et al. (2013).

Mentions: Experiments with model plants indicate that not only do the host species differ in their responses, but also that Arabidopsis ecotypes that have very limited genotypic variability differ in their responses to DSE fungi (Figure 3). More importantly, it is rare that one fungal strain leads to similar host responses across different Arabidopsis accessions. Taken together, these findings suggest that host responses to DSE fungi vary among fungal strains and perhaps also among host genetic backgrounds. These findings clearly demonstrate that growth promoting fungal strains are present in environmental samples (Gentili and Jumpponen, 2006), but that the host responses may depend on the host genotype and are therefore often unpredictable.


Mutualism-parasitism paradigm synthesized from results of root-endophyte models.

Mandyam KG, Jumpponen A - Front Microbiol (2015)

Responses of three Arabidopsis thaliana accessions (Col-0, Cvi-1, Kin-1) to inoculation with 25 strains of Periconia macrospinosa. The analyses follow those described in Mandyam et al. (2013). Response (R) to inoculation indicates the difference between the control and inoculated plants relative to control (inoculated < control) or inoculated plants (control < inoculated; Klironomos, 2003). Values above x-axis indicate a positive response, values below negative. Gray arrows indicate responses consistent across the three accessions, black arrows responses that range from negative to positive depending on the host accession. Asterisks indicate significant difference between the control and inoculated plants (ANOVA, P < 0.05). Figure is redrawn from Figure 2 in Mandyam et al. (2013).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4290590&req=5

Figure 3: Responses of three Arabidopsis thaliana accessions (Col-0, Cvi-1, Kin-1) to inoculation with 25 strains of Periconia macrospinosa. The analyses follow those described in Mandyam et al. (2013). Response (R) to inoculation indicates the difference between the control and inoculated plants relative to control (inoculated < control) or inoculated plants (control < inoculated; Klironomos, 2003). Values above x-axis indicate a positive response, values below negative. Gray arrows indicate responses consistent across the three accessions, black arrows responses that range from negative to positive depending on the host accession. Asterisks indicate significant difference between the control and inoculated plants (ANOVA, P < 0.05). Figure is redrawn from Figure 2 in Mandyam et al. (2013).
Mentions: Experiments with model plants indicate that not only do the host species differ in their responses, but also that Arabidopsis ecotypes that have very limited genotypic variability differ in their responses to DSE fungi (Figure 3). More importantly, it is rare that one fungal strain leads to similar host responses across different Arabidopsis accessions. Taken together, these findings suggest that host responses to DSE fungi vary among fungal strains and perhaps also among host genetic backgrounds. These findings clearly demonstrate that growth promoting fungal strains are present in environmental samples (Gentili and Jumpponen, 2006), but that the host responses may depend on the host genotype and are therefore often unpredictable.

Bottom Line: Despite the high frequency and suspected ecological importance, the effects of DSE colonization on plant growth and performance have remained unclear.These data highlight the context dependency of the DSE symbioses: not only plant species but also ecotypes vary in their responses to populations of conspecific DSE fungi - environmental conditions further shift the host responses similar to those predicted based on the mutualism-parasitism-continuum paradigm.The model systems provide several established avenues of inquiry that permit more detailed molecular and functional dissection of fungal endophyte symbioses, identifying thus likely mechanisms that may underlie the observed host responses to endophyte colonization.

View Article: PubMed Central - PubMed

Affiliation: Department of Agriculture, Alcorn State University Lorman, MS, USA.

ABSTRACT
Plant tissues host a variety of fungi. One important group is the dark septate endophytes (DSEs) that colonize plant roots and form characteristic intracellular structures - melanized hyphae and microsclerotia. The DSE associations are common and frequently observed in various biomes and plant taxa. Reviews suggest that the proportion of plant species colonized by DSE equal that colonized by AM and microscopic studies show that the proportion of the root system colonized by fungi DSE can equal, or even exceed, the colonization by AM fungi. Despite the high frequency and suspected ecological importance, the effects of DSE colonization on plant growth and performance have remained unclear. Here, we draw from over a decade of experimentation with the obscure DSE symbiosis and synthesize across large bodies of published and unpublished data from Arabidopsis thaliana and Allium porrum model systems as well as from experiments that use native plants to better resolve the host responses to DSE colonization. The data indicate similar distribution of host responses in model and native plant studies, validating the use of model plants for tractable dissection of DSE symbioses. The available data also permit empirical testing of the environmental modulation of host responses to DSE colonization and refining the "mutualism-parasitism-continuum" paradigm for DSE symbioses. These data highlight the context dependency of the DSE symbioses: not only plant species but also ecotypes vary in their responses to populations of conspecific DSE fungi - environmental conditions further shift the host responses similar to those predicted based on the mutualism-parasitism-continuum paradigm. The model systems provide several established avenues of inquiry that permit more detailed molecular and functional dissection of fungal endophyte symbioses, identifying thus likely mechanisms that may underlie the observed host responses to endophyte colonization.

No MeSH data available.