The Sulfated PSY Peptide Negatively Regulates Receptor Kinase Activity to Promote Growth

Complex signaling pathways organize cell expansion and proliferation across cells to pattern tissues and organs in plants. The sulfotyrosine peptide hormone family, P LANT PEPTIDE CONTAINING S ULFATED T Y ROSINE (PSY), contributes to these processes. We identified two plasma membrane-localized receptors, PSYR1 and PSYR2, that are necessary for PSY signaling and regulate growth in Physcomitrium patens. Membrane-associated PSYRs accumulate to high levels in a mutant lacking TYROSYL PROTEIN SULFOTRANSFERASE (TPST). Given that a tpst null mutant ( Δtpst ) is impaired in sulfation, this suggests that in the absence of sulfated peptides, PSYRs accumulate on the membrane. A null mutant of the PSY receptors, Δpsyr1/ 2, showed increased growth and was epistatic to Δtpst, suppressing defects in gametophore formation and early senescence. The transcriptional profiles comparing wild type to Δpsyr1/2 and Δpsyr1/2/Δtpst showed 25 to 30 differentially expressed genes between the receptor null mutants and wild type, with a common signature of cell wall remodeling and stress responses. Similarly, a PSYR1 kinase-inactive mutation rescued Δtpst and relieved the accumulation of membrane-associated PSYRs. In contrast, overexpression of PSYRs inhibited plant growth, with phenotypic severity correlating with the amount of overexpression. These data are consistent with a constitutive activation model in which membrane-associated PSYRs unbound to PSY serve to inhibit growth through an active kinase. In the presence of the PSY peptide, the kinase is inactivated, promoting growth and driving PSY expression. The relationship between growth-repressive PSYR kinase activity and growth-promoting PSYR kinase inactivation in P. patens serves as a model for optimizing plant growth and development.

As sessile organisms, plant growth and development rely on the intricate integration of external and internal signals. Plants produce peptide hormones and those signals are read by leucine rich receptor like kinases (LRR-RLKs), which normally are activated by binding to peptide. Taking advantage of the ability to generate point mutations directly in the genome, we show that PSY peptide binding leads to kinase inactivation, shifting the paradigm for peptide signaling in plants.