TPST-dependent and -independent regulation of root development and signaling by PSK LRR receptor kinases in Arabidopsis

Abstract Tyrosine-sulfated peptides are key regulators of plant growth and development. The disulfated pentapeptide phytosulfokine (PSK) mediates growth via leucine-rich repeat receptor-like kinases, PSKR1 and PSKR2. PSKRs are part of a response module at the plasma membrane that mediates short-term growth responses, but downstream signaling of transcriptional regulation remains unexplored. In Arabidopsis, tyrosine sulfation is catalyzed by a single-copy gene (TPST). We performed a microarray-based transcriptome analysis in the tpst-1 mutant background that lacks sulfated peptides to identify PSK-regulated genes and genes that are regulated by other sulfated peptides. Of the 160 PSK-regulated genes, several had functions in root growth and development in agreement with shorter roots and a higher lateral root density in tpst-1. Further, tpst-1 roots developed higher numbers of root hairs and PSK induced expression of WEREWOLF (WER), its paralog MYB DOMAIN PROTEIN 23 (MYB23) and At1g66800 that maintain non-hair cell fate. The tpst-1 pskr1-3 pskr2-1 mutant showed even shorter roots, and higher lateral root and root hair density than tpst-1 revealing unexpected synergistic effects of ligand and PSK receptor deficiencies. While residual activities may exist, overexpression of PSKR1 in the tpst-1 background induced root growth suggesting that PSKR1 may be active in the absence of sulfated ligands. HighlightPhytosulfokine (PSK) receptor signaling promotes root elongation, determines lateral root density and maintains non-hair cell fate partially independent of TPST responsible for the activating sulfation of PSK.