Pectin Methylesterase Activity is Crucial for RALF1 Peptide Signaling in Plant Roots

Conceitos essenciais

Pectin demethylation status is a key determinant for the perception and signaling output of the plant peptide hormone RALF1 via the receptor FERONIA.

Resumo

This study investigates the role of the cell wall component pectin in the signaling of the plant peptide hormone RAPID ALKALINIZATION FACTOR 1 (RALF1) in Arabidopsis roots. The key findings are:

Pharmacological and genetic interference with PECTIN METHYL ESTERASE (PME) activity, which catalyzes the demethylation of pectin, abolishes RALF1-induced root growth repression, cell wall alterations, and apoplastic pH changes.

RALF1 peptides bind with high avidity to demethylated pectin fragments, and this association is required for the FERONIA (FER) receptor-mediated perception and signaling of RALF1.

The positive charges in the RALF1 peptide are essential for its binding to demethylated pectin and subsequent bioactivity, suggesting a charge-dependent interaction.

The root-expressed LEUCINE-RICH REPEAT EXTENSIN (LRX) proteins, which physically link the FER receptor to the cell wall, are not required for the PME-dependent RALF1 signaling.

The authors propose that the methylation status of pectin acts as a conceptualizing signaling scaffold for RALF peptides, linking extracellular matrix dynamics to peptide hormone-mediated responses in plant roots.

Estatísticas

The application of RALF1 peptides induces strong repression of main root growth in Arabidopsis thaliana.
Pharmacological and genetic interference with PME activity leads to the repression of RALF1 effects on root growth.
RALF1 application induces swollen cell walls and plasma membrane invaginations in root epidermal cells, which are abolished by PME inhibition.
RALF1 induces apoplastic pH alkalization in wild-type roots, but this effect is abolished by PME inhibition or overexpression of PMEI3.
RALF1-induced internalization of the FER receptor is disrupted by PME inhibition or overexpression of PMEI3.
Biotinylated RALF1 binds to demethylated oligogalacturonides (OGs) with an equilibrium dissociation constant (Kd) of 105 nM.
Substitution of the positively charged amino acids in RALF1 (RALF1-KR) abolishes its bioactivity in roots.

Citações

"Our data suggests that negatively charged, demethylated pectin binds to positively charged RALF1 peptides with high avidity."
"We accordingly propose that the RALF interaction with demethylated pectin is crucial for its FER-dependent perception in roots."
"We hence conclude that the methylation status of pectin provides a conceptualising input to RALF peptide hormone signalling."

Principais Insights Extraídos De

Pectin methylesterase activity is required for RALF1 peptide signalling output

by Roessling,A.... às www.biorxiv.org 08-19-2023

https://www.biorxiv.org/content/10.1101/2023.08.18.553913v2

Perguntas Mais Profundas

How might the PME-dependent pectin demethylation status be dynamically regulated in response to developmental or environmental cues to modulate RALF1 signaling in roots?

Pectin methylesterase (PME) activity and the demethylation status of pectin play a crucial role in modulating RALF1 signaling in roots. The dynamic regulation of PME activity and pectin demethylation status in response to developmental or environmental cues can be influenced by various factors.

Developmental Signals: During different stages of plant development, the expression and activity of PMEs can be regulated to alter the demethylation status of pectin. For example, in growing root tips where cell expansion is high, there may be an upregulation of PME activity to maintain a certain level of demethylated pectin for optimal RALF1 signaling.

Environmental Stimuli: Environmental cues such as changes in pH, temperature, or nutrient availability can also impact PME activity. For instance, under conditions of stress or nutrient deficiency, plants may regulate PME expression to adjust the demethylation status of pectin and fine-tune RALF1 signaling to adapt to the changing environment.

Signaling Pathways: Signaling pathways involved in plant growth and stress responses can cross-talk with the PME-pectin axis. Hormones like auxins or ethylene, which regulate growth and development, may influence PME activity to modulate pectin demethylation and RALF1 signaling.

Epigenetic Regulation: Epigenetic modifications, such as DNA methylation or histone modifications, can also impact the expression of genes involved in PME activity. Changes in epigenetic marks in response to developmental or environmental cues can indirectly affect pectin demethylation and RALF1 signaling.

Overall, the dynamic regulation of PME-dependent pectin demethylation status in roots is likely a finely tuned process that integrates various signals to modulate RALF1 signaling and coordinate plant growth and responses to the environment.

What other cell wall components or modifications could potentially contribute to the integration of RALF peptide signals beyond the pectin-FER interaction described here?

In addition to pectin and the pectin methylesterase (PME) activity described in the context, several other cell wall components and modifications could potentially contribute to the integration of RALF peptide signals in plants:

Cellulose: Cellulose, a major component of the plant cell wall, provides structural support and rigidity. Changes in cellulose deposition or organization could impact cell wall properties and affect the perception or transmission of RALF peptide signals.

Hemicelluloses: Hemicelluloses like xyloglucan and arabinoxylans are important components of the cell wall matrix. Modifications in hemicellulose composition or cross-linking could influence cell wall dynamics and potentially interact with RALF peptides.

Lignin: Lignin, a complex polymer, contributes to cell wall strength and impermeability. Alterations in lignin content or composition may affect cell wall properties and the transmission of RALF signaling cues.

Glycoproteins: Cell wall glycoproteins, such as extensins or arabinogalactan proteins, are involved in cell wall structure and signaling. Interactions between RALF peptides and specific glycoproteins could modulate signal transduction pathways.

Enzymatic Modifications: Enzymes involved in cell wall modifications, such as expansins, peroxidases, or glycosyltransferases, can impact cell wall properties. Changes in the activity or expression of these enzymes could influence the response to RALF peptide signals.

By considering the complex interplay of various cell wall components and modifications, we can gain a more comprehensive understanding of how RALF peptide signals are integrated and transduced in plant cells beyond the pectin-FER interaction.

Given the proposed role of pectin as an extracellular signaling scaffold, how might this concept extend to the regulation of other plant peptide hormone pathways or cell-cell communication processes?

The concept of pectin acting as an extracellular signaling scaffold in the regulation of plant peptide hormone pathways can be extended to other signaling processes and cell-cell communication mechanisms in plants. Here are some ways in which this concept might apply:

Other Peptide Hormone Pathways: Similar to RALF peptides, other plant peptide hormones like systemin, CLAVATA3, or CLE peptides may also interact with specific cell wall components to modulate their signaling outputs. Pectin or other cell wall components could serve as platforms for the perception and transmission of signals in these pathways.

Receptor-Ligand Interactions: Cell wall components can influence receptor-ligand interactions beyond peptide hormones. For example, receptor kinases or receptor-like proteins involved in pathogen recognition or stress responses may interact with specific cell wall molecules to initiate downstream signaling cascades.

Cell-Cell Communication: In addition to hormone signaling, cell-cell communication processes such as plasmodesmata-mediated signaling or intercellular signaling in root nodules could also involve the extracellular matrix. Pectin or other cell wall components may play a role in regulating the passage of signaling molecules between cells.

Environmental Sensing: The extracellular matrix, including pectin, could function as a sensor for environmental cues and relay this information to the intracellular signaling network. Changes in the cell wall composition or structure in response to environmental stimuli could impact various signaling pathways.

By viewing the cell wall as a dynamic and interactive platform for signaling molecules, including peptide hormones, plants can integrate external cues, coordinate developmental processes, and mount appropriate responses to biotic and abiotic stresses. The role of pectin as an extracellular signaling scaffold highlights the complexity and versatility of plant cell wall-mediated signaling mechanisms.