Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis

PLoS Genet. 2020 Jun 19;16(6):e1008847. doi: 10.1371/journal.pgen.1008847. eCollection 2020 Jun.

Abstract

Plant cell growth requires the coordinated expansion of the protoplast and the cell wall, which is controlled by an elaborate system of cell wall integrity (CWI) sensors linking the different cellular compartments. LRR-eXtensins (LRXs) are cell wall-attached extracellular regulators of cell wall formation and high-affinity binding sites for RALF (Rapid ALkalinization Factor) peptide hormones that trigger diverse physiological processes related to cell growth. LRXs function in CWI sensing and in the case of LRX4 of Arabidopsis thaliana, this activity was shown to involve interaction with the transmembrane Catharanthus roseus Receptor-Like Kinase1-Like (CrRLK1L) protein FERONIA (FER). Here, we demonstrate that binding of RALF1 and FER is common to most tested LRXs of vegetative tissue, including LRX1, the main LRX protein of root hairs. Consequently, an lrx1-lrx5 quintuple mutant line develops shoot and root phenotypes reminiscent of the fer-4 knock-out mutant. The previously observed membrane-association of LRXs, however, is FER-independent, suggesting that LRXs bind not only FER but also other membrane-localized proteins to establish a physical link between intra- and extracellular compartments. Despite evolutionary diversification of various LRX proteins, overexpression of several chimeric LRX constructs causes cross-complementation of lrx mutants, indicative of comparable functions among members of this protein family. Suppressors of the pollen-growth defects induced by mutations in the CrRLK1Ls ANXUR1/2 also alleviate lrx1 lrx2-induced mutant root hair phenotypes. This suggests functional similarity of LRX-CrRLK1L signaling processes in very different cell types and indicates that LRX proteins are components of conserved processes regulating cell growth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Cell Wall / metabolism*
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Plant
  • Gene Knockout Techniques
  • Genes, Plant
  • Mutation
  • Peptide Hormones / metabolism*
  • Phosphotransferases / genetics
  • Phosphotransferases / metabolism*
  • Plant Roots / cytology
  • Plant Roots / growth & development
  • Plants, Genetically Modified
  • Pollen / cytology
  • Pollen / growth & development
  • Protein Domains / genetics
  • Protein Interaction Maps
  • Seedlings / cytology
  • Seedlings / growth & development
  • Signal Transduction / genetics

Substances

  • Arabidopsis Proteins
  • LRX1 protein, Arabidopsis
  • Peptide Hormones
  • RALF1 protein, Arabidopsis
  • FERONIA receptor like kinase, Arabidopsis
  • Phosphotransferases

Grants and funding

This work was supported by the Swiss National Science Foundation (grant Nr. 31003A_166577) to CR and in part by a grant from the University of Cologne Centre of Excellence in Plant Sciences to ABD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.