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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over a decade of experimentation with the obscure DSE symbiosis and synthesize across large bodies of published and unpublished data from Arabidopsis thaliana and Allium porrum model systems as well as from experiments that use native plants to better resolve the host responses to DSE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.


Related in: MedlinePlus

Frequency distribution of Arabidopsis responses to inoculation in 157 experiments that paired Arabidopsis thaliana either inoculated with Periconia macrospinosa or with sterile fungal medium (mock-control). The experimental procedures are described in full detail 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). t-test on the mean of 157 experiments indicates that average response to inoculation is negative (P < 0.0001) suggesting thus an overall parasitic association. The box identifies median, quartiles and 95% confidence intervals. Dashed line identifies the mean response across all 157 experiments.
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Figure 1: Frequency distribution of Arabidopsis responses to inoculation in 157 experiments that paired Arabidopsis thaliana either inoculated with Periconia macrospinosa or with sterile fungal medium (mock-control). The experimental procedures are described in full detail 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). t-test on the mean of 157 experiments indicates that average response to inoculation is negative (P < 0.0001) suggesting thus an overall parasitic association. The box identifies median, quartiles and 95% confidence intervals. Dashed line identifies the mean response across all 157 experiments.

Mentions: The model plant Arabidopsis thaliana is subject to colonization by a variety of bacterial (Bulgarelli et al., 2012) and fungal endophytes (Garcia et al., 2013), including fungi that occupy root and rhizosphere (Mandyam et al., 2013; Mandyam and Jumpponen, 2014). As such, A. thaliana and its endophytes may provide a model for exploring endophyte associations in a well-defined system (Garcia et al., 2013). Mandyam et al. (2013) utilized a closed petri plate system that permitted 6–8 weeks incubation of A. thaliana with a minimal contamination risk. These experiments standardly used pairs of experimental treatments that were either mock-inoculated with a disk from fungal medium (fungus-free control) or inoculated with P. macrospinosa. While such experiments are tedious to set up and demand substantial growth room capacity, they benefit greatly from simple statistical inference on the host responses to the presence of the endophyte fungus. Furthermore, these experiments easily lend themselves for advanced classroom settings. We were fortunate to conduct a total of 157 such experiments (a total of 3,140 experimental units) with the assistance of more than thirty senior undergraduate students at Kansas State University. These experiments lend further support to conclusions in Mandyam et al. (2013): while the model plant responses to a population of endophytes may be variable and include several examples of symbioses that enhance host growth, on average the host responses are negative and the host growth is inhibited relative to the fungus-free controls (Figure 1).


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

Mandyam KG, Jumpponen A - Front Microbiol (2015)

Frequency distribution of Arabidopsis responses to inoculation in 157 experiments that paired Arabidopsis thaliana either inoculated with Periconia macrospinosa or with sterile fungal medium (mock-control). The experimental procedures are described in full detail 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). t-test on the mean of 157 experiments indicates that average response to inoculation is negative (P < 0.0001) suggesting thus an overall parasitic association. The box identifies median, quartiles and 95% confidence intervals. Dashed line identifies the mean response across all 157 experiments.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Frequency distribution of Arabidopsis responses to inoculation in 157 experiments that paired Arabidopsis thaliana either inoculated with Periconia macrospinosa or with sterile fungal medium (mock-control). The experimental procedures are described in full detail 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). t-test on the mean of 157 experiments indicates that average response to inoculation is negative (P < 0.0001) suggesting thus an overall parasitic association. The box identifies median, quartiles and 95% confidence intervals. Dashed line identifies the mean response across all 157 experiments.
Mentions: The model plant Arabidopsis thaliana is subject to colonization by a variety of bacterial (Bulgarelli et al., 2012) and fungal endophytes (Garcia et al., 2013), including fungi that occupy root and rhizosphere (Mandyam et al., 2013; Mandyam and Jumpponen, 2014). As such, A. thaliana and its endophytes may provide a model for exploring endophyte associations in a well-defined system (Garcia et al., 2013). Mandyam et al. (2013) utilized a closed petri plate system that permitted 6–8 weeks incubation of A. thaliana with a minimal contamination risk. These experiments standardly used pairs of experimental treatments that were either mock-inoculated with a disk from fungal medium (fungus-free control) or inoculated with P. macrospinosa. While such experiments are tedious to set up and demand substantial growth room capacity, they benefit greatly from simple statistical inference on the host responses to the presence of the endophyte fungus. Furthermore, these experiments easily lend themselves for advanced classroom settings. We were fortunate to conduct a total of 157 such experiments (a total of 3,140 experimental units) with the assistance of more than thirty senior undergraduate students at Kansas State University. These experiments lend further support to conclusions in Mandyam et al. (2013): while the model plant responses to a population of endophytes may be variable and include several examples of symbioses that enhance host growth, on average the host responses are negative and the host growth is inhibited relative to the fungus-free controls (Figure 1).

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.


Related in: MedlinePlus