Extracellular matrix sensing by FERONIA and Leucine‐Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana

• Published in: The EMBO journal 2019-04, Vol.38 (7), p.n/a
• Main Authors: Dünser, Kai, Gupta, Shibu, Herger, Aline, Feraru, Mugurel I, Ringli, Christoph, Kleine‐Vehn, Jürgen
• Format: Article
• Language: English
• Subjects: Acidification; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; cell expansion; cell wall; Cell Wall - metabolism; Cell walls; Cytosol; Detection; Elongation; EMBO20; EMBO30; Enlargement; Extensin; Extracellular matrix; Extracellular Matrix - metabolism; Gene Expression Regulation, Plant; Glycoproteins - metabolism; growth; Intracellular; Kinases; Leucine; Loosening; Morphology; Occupancy; Organelles; Phosphotransferases - metabolism; plant; Plant Development; Plant Proteins - metabolism; Proteins; Proteins - metabolism; vacuole; Vacuoles; Vacuoles - metabolism
• ISSN: 0261-4189; 1460-2075
• DOI: 10.15252/embj.2018100353

Cellular elongation requires the defined coordination of intra‐ and extracellular processes, but the underlying mechanisms are largely unknown. The vacuole is the biggest plant organelle, and its dimensions play a role in defining plant cell expansion rates. Here, we show that the increase in vacuolar occupancy enables cellular elongation with relatively little enlargement of the cytosol in Arabidopsis thaliana . We demonstrate that cell wall properties are sensed and impact on the intracellular expansion of the vacuole. Using vacuolar morphology as a quantitative read‐out for intracellular growth processes, we reveal that the underlying cell wall sensing mechanism requires interaction of extracellular leucine‐rich repeat extensins (LRXs) with the receptor‐like kinase FERONIA (FER). Our data suggest that LRXs link plasma membrane‐localised FER with the cell wall, allowing this module to jointly sense and convey extracellular signals to the cell. This mechanism coordinates the onset of cell wall acidification and loosening with the increase in vacuolar size. Synopsis Vacuoles are the biggest plant organelles and contribute to cellular expansion. Extracellular Leucine‐Rich Repeat Extensin (LRX) proteins link plasma membrane receptor‐like kinase FERONIA (FER) with the cell wall for sensing mechanical constraints affecting vacuolar size and cellular elongation. The space‐filling function of the vacuole allows for rapid cell elongation with little de novo production of cytosolic content. LRXs and FER interact and sense cell wall status. LRXs and FER align cell wall status with the intracellular expansion of the vacuole. Graphical Abstract Extracellular Leucine‐Rich Repeat Extensin proteins link the plasma membrane receptor‐like kinase FERONIA with the cell wall for sensing mechanical constraints affecting vacuolar size and plant cell elongation.