Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis

doi:10.1073/pnas.0706403104

Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis

Graduate School of Bio-Agricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan

Edited by Clarence A. Ryan, Jr., Washington State University, Pullman, WA, and approved October 1, 2007 (received for review July 9, 2007)

Abstract

Posttranslational modification can confer special functions to peptides. Based on exhaustive liquid chromatography mass spectrometry analysis targeting tyrosine-sulfated peptides, we identified an 18-aa tyrosine-sulfated glycopeptide in Arabidopsis cell suspension culture medium. This peptide, which we named PSY1, significantly promotes cellular proliferation and expansion at nanomolar concentrations. PSY1 is widely expressed in various Arabidopsis tissues, including shoot apical meristem, and is highly up-regulated by wounding. Perception of PSY1 depends on At1g72300, which is a leucine-rich repeat receptor kinase (LRR-RK) whose two paralogs are involved in the perception of phytosulfokine (PSK), which is a 5-aa tyrosine-sulfated peptide that primarily promotes cellular proliferation. Multiple loss-of-function mutations in these three paralogous LRR-RKs significantly enhanced phenotypes, compared with single disruptants, suggesting that these LRR-RKs have overlapping functions. Triple mutations in these LRR-RKs resulted in dwarfism because of decreases in cell number and cell size and caused insufficiency in tissue repair after wounding. The present results suggest that this paralogous LRR-RK family integrates growth-promoting signals mediated by two structurally distinct sulfated peptides: PSY1 and PSK.

Footnotes

*To whom correspondence should be addressed. E-mail: matsu{at}agr.nagoya-u.ac.jp
Author contributions: Y.M. designed research; Y.A., H.T., H.S., M.O., and Y.M. performed research; Y.A., H.T., H.S., M.O., and Y.M. analyzed data; and Y.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. AB304257).
This article contains supporting information online at www.pnas.org/cgi/content/full/0706403104/DC1.
Abbreviations:

GUS,

β-glucuronidase;

LC/MS,

liquid chromatography/mass spectrometry;

LC-MS/MS,

LC-tandem MS;

LRR-RK,

leucine-rich repeat receptor kinase;

PSK,

phytosulfokine;

TPST,

tyrosylprotein sulfotransferase.