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Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains

View Article: PubMed Central - PubMed

ABSTRACT

Cell surface receptors govern a multitude of signalling pathways in multicellular organisms. In plants, prominent examples are the receptor kinases FLS2 and BRI1, which activate immunity and steroid-mediated growth, respectively. Intriguingly, despite inducing distinct signalling outputs, both receptors employ common downstream signalling components, which exist in plasma membrane (PM)-localised protein complexes. An important question is thus how these receptor complexes maintain signalling specificity. Live-cell imaging revealed that FLS2 and BRI1 form PM nanoclusters. Using single-particle tracking we could discriminate both cluster populations and we observed spatiotemporal separation between immune and growth signalling platforms. This finding was confirmed by visualising FLS2 and BRI1 within distinct PM nanodomains marked by specific remorin proteins and differential co-localisation with the cytoskeleton. Our results thus suggest that signalling specificity between these pathways may be explained by the spatial separation of FLS2 and BRI1 with their associated signalling components within dedicated PM nanodomains.

Doi:: http://dx.doi.org/10.7554/eLife.25114.001

No MeSH data available.


Related in: MedlinePlus

Activation of FLS2 results in reduced lateral receptor cluster displacement.(A) Time-dependent quantification of short-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (B) Time-dependent quantification of short FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (C) Time-dependent quantification of medium-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (D) Time-dependent quantification of medium FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (E) Time-dependent quantification of long-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (F) Time-dependent quantification of long FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. The presented data points were obtained from VAEM time series with a temporal resolution of 0.5 s over 250 frames. The coloured data points represent the technical replicates of 3 independent experiments. The indicated p-values were obtained using a one-tailed heteroscedastic t-test and a Bonferroni multiple hypothesis correction.DOI:http://dx.doi.org/10.7554/eLife.25114.011
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fig4: Activation of FLS2 results in reduced lateral receptor cluster displacement.(A) Time-dependent quantification of short-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (B) Time-dependent quantification of short FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (C) Time-dependent quantification of medium-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (D) Time-dependent quantification of medium FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (E) Time-dependent quantification of long-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (F) Time-dependent quantification of long FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. The presented data points were obtained from VAEM time series with a temporal resolution of 0.5 s over 250 frames. The coloured data points represent the technical replicates of 3 independent experiments. The indicated p-values were obtained using a one-tailed heteroscedastic t-test and a Bonferroni multiple hypothesis correction.DOI:http://dx.doi.org/10.7554/eLife.25114.011

Mentions: Accordingly, we observed a reduction in lateral cluster displacement for FLS2 receptors after seedlings were exposed to 100 nM flg22, whereas BRI1 was unaffected (Figure 4). Again, there was no quantitative effect on the receptor cluster lifetimes of both receptors (Figure 4).10.7554/eLife.25114.011Figure 4.Activation of FLS2 results in reduced lateral receptor cluster displacement.


Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains
Activation of FLS2 results in reduced lateral receptor cluster displacement.(A) Time-dependent quantification of short-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (B) Time-dependent quantification of short FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (C) Time-dependent quantification of medium-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (D) Time-dependent quantification of medium FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (E) Time-dependent quantification of long-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (F) Time-dependent quantification of long FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. The presented data points were obtained from VAEM time series with a temporal resolution of 0.5 s over 250 frames. The coloured data points represent the technical replicates of 3 independent experiments. The indicated p-values were obtained using a one-tailed heteroscedastic t-test and a Bonferroni multiple hypothesis correction.DOI:http://dx.doi.org/10.7554/eLife.25114.011
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Related In: Results  -  Collection

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fig4: Activation of FLS2 results in reduced lateral receptor cluster displacement.(A) Time-dependent quantification of short-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (B) Time-dependent quantification of short FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (C) Time-dependent quantification of medium-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (D) Time-dependent quantification of medium FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (E) Time-dependent quantification of long-range FLS2-GFP and BRI1-GFP receptor cluster displacements in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. (F) Time-dependent quantification of long FLS2-GFP and BRI1-GFP receptor cluster lifetimes in epidermal cells of Arabidopsis seedling cotyledons after application of 100 nM flg22. The presented data points were obtained from VAEM time series with a temporal resolution of 0.5 s over 250 frames. The coloured data points represent the technical replicates of 3 independent experiments. The indicated p-values were obtained using a one-tailed heteroscedastic t-test and a Bonferroni multiple hypothesis correction.DOI:http://dx.doi.org/10.7554/eLife.25114.011
Mentions: Accordingly, we observed a reduction in lateral cluster displacement for FLS2 receptors after seedlings were exposed to 100 nM flg22, whereas BRI1 was unaffected (Figure 4). Again, there was no quantitative effect on the receptor cluster lifetimes of both receptors (Figure 4).10.7554/eLife.25114.011Figure 4.Activation of FLS2 results in reduced lateral receptor cluster displacement.

View Article: PubMed Central - PubMed

ABSTRACT

Cell surface receptors govern a multitude of signalling pathways in multicellular organisms. In plants, prominent examples are the receptor kinases FLS2 and BRI1, which activate immunity and steroid-mediated growth, respectively. Intriguingly, despite inducing distinct signalling outputs, both receptors employ common downstream signalling components, which exist in plasma membrane (PM)-localised protein complexes. An important question is thus how these receptor complexes maintain signalling specificity. Live-cell imaging revealed that FLS2 and BRI1 form PM nanoclusters. Using single-particle tracking we could discriminate both cluster populations and we observed spatiotemporal separation between immune and growth signalling platforms. This finding was confirmed by visualising FLS2 and BRI1 within distinct PM nanodomains marked by specific remorin proteins and differential co-localisation with the cytoskeleton. Our results thus suggest that signalling specificity between these pathways may be explained by the spatial separation of FLS2 and BRI1 with their associated signalling components within dedicated PM nanodomains.

Doi:: http://dx.doi.org/10.7554/eLife.25114.001

No MeSH data available.


Related in: MedlinePlus