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The interaction of Arabidopsis with Piriformospora indica shifts from initial transient stress induced by fungus-released chemical mediators to a mutualistic interaction after physical contact of the two symbionts.

Vahabi K, Sherameti I, Bakshi M, Mrozinska A, Ludwig A, Reichelt M, Oelmüller R - BMC Plant Biol. (2015)

Bottom Line: Once a physical contact is established, the stomata re-open, ROS and phytohormone levels decline, and the number and expression level of defense/stress-related genes decreases.We propose that exudated compounds from P. indica induce stress and defense responses in the host.Root colonization results in the down-regulation of defense responses and the activation of genes involved in promoting plant growth, metabolism and performance.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Piriformospora indica, an endophytic fungus of Sebacinales, colonizes the roots of many plant species including Arabidopsis thaliana. The symbiotic interaction promotes plant performance, growth and resistance/tolerance against abiotic and biotic stress.

Results: We demonstrate that exudated compounds from the fungus activate stress and defense responses in the Arabidopsis roots and shoots before the two partners are in physical contact. They induce stomata closure, stimulate reactive oxygen species (ROS) production, stress-related phytohormone accumulation and activate defense and stress genes in the roots and/or shoots. Once a physical contact is established, the stomata re-open, ROS and phytohormone levels decline, and the number and expression level of defense/stress-related genes decreases.

Conclusions: We propose that exudated compounds from P. indica induce stress and defense responses in the host. Root colonization results in the down-regulation of defense responses and the activation of genes involved in promoting plant growth, metabolism and performance.

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Epidermis with stomata of Arabidopsis leaves two or six days after exposure of the seedlings to an agar plaque without (control) or withP. indica(+P. indica). Guard cells were visualized under the fluorescent microscope (450-520 nm) after stained with calcoflour white (the upper level). The lower panel shows the % closed stomata. Based on 3 independent biological experiments with 10 leaves from individual seedlings each. Bars represent SEs. Asterisks indicate significant differences, as determined by Student’s t-test (**P < 0.01).
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Fig1: Epidermis with stomata of Arabidopsis leaves two or six days after exposure of the seedlings to an agar plaque without (control) or withP. indica(+P. indica). Guard cells were visualized under the fluorescent microscope (450-520 nm) after stained with calcoflour white (the upper level). The lower panel shows the % closed stomata. Based on 3 independent biological experiments with 10 leaves from individual seedlings each. Bars represent SEs. Asterisks indicate significant differences, as determined by Student’s t-test (**P < 0.01).

Mentions: Although a physical contact between the two partners has not yet been established after two days, the leaves of the seedlings respond to the presence of the fungus by closing the stomata (Figure 1). Prior to expose to P. indica, 14.6 ± 1.1% of the stomata in the leaves were closed. Almost identical results were obtained for seedlings exposed to an agar plaque without the fungus for either two or six days (two days: 13.9 ± 3.3%; six days: 12.9 ± 3.7%). In contrast, two days after exposure of the seedlings to the P. indica-containing plaque, 76.7 ± 2.9% of the stomata were closed. Longer co-cultivation resulted in re-opening of the stomata, and after six days, only 17.5 ± 1.2% of the stomata remained closed (Figure 1). This demonstrates that regulation of stomata opening in the leaves in response to the root-colonizing fungus P. indica is a sensitive marker for the interaction of the two partners. To clarify whether the fungal signal(s) is an exudated compound in the medium or a gas, we co-cultivated Arabidopsis seedlings with P. indica on split Petri dishes. Exudated compounds from the fungus in the medium cannot reach the roots, while communication via gases or volatiles is possible. The number of closed stomata in Arabidopsis seedling was not significantly different two days after co-cultivation of the symbionts on the split Petri dishes compared to the mock-treated control (control: 18.00 ± 1.65%; split Petri dishes: 18.87 ± 2.17%) which excludes gases and volatiles as chemical mediators.Figure 1


The interaction of Arabidopsis with Piriformospora indica shifts from initial transient stress induced by fungus-released chemical mediators to a mutualistic interaction after physical contact of the two symbionts.

Vahabi K, Sherameti I, Bakshi M, Mrozinska A, Ludwig A, Reichelt M, Oelmüller R - BMC Plant Biol. (2015)

Epidermis with stomata of Arabidopsis leaves two or six days after exposure of the seedlings to an agar plaque without (control) or withP. indica(+P. indica). Guard cells were visualized under the fluorescent microscope (450-520 nm) after stained with calcoflour white (the upper level). The lower panel shows the % closed stomata. Based on 3 independent biological experiments with 10 leaves from individual seedlings each. Bars represent SEs. Asterisks indicate significant differences, as determined by Student’s t-test (**P < 0.01).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4384353&req=5

Fig1: Epidermis with stomata of Arabidopsis leaves two or six days after exposure of the seedlings to an agar plaque without (control) or withP. indica(+P. indica). Guard cells were visualized under the fluorescent microscope (450-520 nm) after stained with calcoflour white (the upper level). The lower panel shows the % closed stomata. Based on 3 independent biological experiments with 10 leaves from individual seedlings each. Bars represent SEs. Asterisks indicate significant differences, as determined by Student’s t-test (**P < 0.01).
Mentions: Although a physical contact between the two partners has not yet been established after two days, the leaves of the seedlings respond to the presence of the fungus by closing the stomata (Figure 1). Prior to expose to P. indica, 14.6 ± 1.1% of the stomata in the leaves were closed. Almost identical results were obtained for seedlings exposed to an agar plaque without the fungus for either two or six days (two days: 13.9 ± 3.3%; six days: 12.9 ± 3.7%). In contrast, two days after exposure of the seedlings to the P. indica-containing plaque, 76.7 ± 2.9% of the stomata were closed. Longer co-cultivation resulted in re-opening of the stomata, and after six days, only 17.5 ± 1.2% of the stomata remained closed (Figure 1). This demonstrates that regulation of stomata opening in the leaves in response to the root-colonizing fungus P. indica is a sensitive marker for the interaction of the two partners. To clarify whether the fungal signal(s) is an exudated compound in the medium or a gas, we co-cultivated Arabidopsis seedlings with P. indica on split Petri dishes. Exudated compounds from the fungus in the medium cannot reach the roots, while communication via gases or volatiles is possible. The number of closed stomata in Arabidopsis seedling was not significantly different two days after co-cultivation of the symbionts on the split Petri dishes compared to the mock-treated control (control: 18.00 ± 1.65%; split Petri dishes: 18.87 ± 2.17%) which excludes gases and volatiles as chemical mediators.Figure 1

Bottom Line: Once a physical contact is established, the stomata re-open, ROS and phytohormone levels decline, and the number and expression level of defense/stress-related genes decreases.We propose that exudated compounds from P. indica induce stress and defense responses in the host.Root colonization results in the down-regulation of defense responses and the activation of genes involved in promoting plant growth, metabolism and performance.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Piriformospora indica, an endophytic fungus of Sebacinales, colonizes the roots of many plant species including Arabidopsis thaliana. The symbiotic interaction promotes plant performance, growth and resistance/tolerance against abiotic and biotic stress.

Results: We demonstrate that exudated compounds from the fungus activate stress and defense responses in the Arabidopsis roots and shoots before the two partners are in physical contact. They induce stomata closure, stimulate reactive oxygen species (ROS) production, stress-related phytohormone accumulation and activate defense and stress genes in the roots and/or shoots. Once a physical contact is established, the stomata re-open, ROS and phytohormone levels decline, and the number and expression level of defense/stress-related genes decreases.

Conclusions: We propose that exudated compounds from P. indica induce stress and defense responses in the host. Root colonization results in the down-regulation of defense responses and the activation of genes involved in promoting plant growth, metabolism and performance.

Show MeSH
Related in: MedlinePlus