Evidence for early evolution of sulfated peptide signaling in plant development

In plants, the cell wall fixes the position of each cell; therefore, during development, plants rely on cellular proliferation and expansion for tissue patterning and organ formation. How plant cells communicate with neighboring cells to coordinate expansion for properly patterned tissues and organs is not well understood. In seed plants, organ growth is known to be modulated by sulfotyrosyl peptide signaling. Here, we report that the activity of TYROSYL PROTEIN SULFOTRANSFERASE (TPST), which is responsible for the posttranslational modification of sulfotyrosyl peptides, is essential for expansion during development in the nonvascular plant, Physcomitrium patens. Plants that harbor a null mutation in the gene encoding TPST (Δtpst) were smaller, formed fewer caulonemal filaments, and were unable to form expanded gametophores. In Δtpst multiple aspects of gametophore development were affected, including the first division of the gametophore initial, as well as reduced rates of cell division and expansion. Mutational analysis of P. patens TPST identified the residue Histidine 124, a candidate catalytic residue, as essential for TPST function. Notably, the addition of the sulfated signaling peptide PSY1, from either P. patens or Arabidopsis thaliana, rescued all Δtpst developmental deficits. Taken together, these data suggest that TPST functions to sulfate PSY, and this activity is necessary for plant growth and development. Furthermore, since the addition of AtPSY fully rescues Δtpst and PpPSY promotes root elongation in Arabidopsis and rice, these findings suggest that PSY signaling is evolutionarily conserved.