Tyrosylprotein sulfotransferase-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 169 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.

Peptide ligand-mediated trade-off between plant growth and stress response

“…We first cultured the tpst-1 seedlings in culture medium supplemented with synthetic mature PSY peptides. Because tpst-1 is deficient in biosynthesis of all tyrosine sulfated peptides, this mutant serves as a substitute for a polymutant of the sulfated peptide hormones (18)(19)(20). The addition of 1 mM PSY2, PSY3, PSY5, PSY6, or PSY8 to the culture medium rescued the root growth defect otherwise seen in tpst-1 with PSY5 being most potent; this peptide was selected as a representative of the PSY family (fig.…”

Integrative Transcriptomics Data Mining to Explore the Functions of TDP1α and TDP1β Genes in the Arabidopsis thaliana Model Plant

“…Looking at the heatmap, it is possible to observe that in the root epidermidis, TDP1β is more expressed than TDP1α in the wer mutant. The Weekly Epidemiological Record ( WER ) gene encodes a nuclear-localized MyB-related protein involved in root and hypocotyl epidermal cell fate determination and its loss of function produces a phenotype with extra root hairs [ 58 ]. These results may support the hypothesis of the possible involvement of TDP1β in root and hypocotyl development, in agreement with what was observed above ( Figure 1 a).…”

MYB Transcription Factors Becoming Mainstream in Plant Roots

“…Moreover, TRY in HC can upregulate the expression of the SCM gene, contributing to the HC fate [ 49 ]. Recently, phytosulfokine receptors (PSKRs) which belong to the LRR-RLK family and an O-fucosyltransferase protein, SPINDLY (SPY), were reported to participate in position-dependent root epidermal cell fate determination as well [ 50 , 51 ]. Together, both the position signals and various feedback pathways determine the dominance of different MBW complexes in HCs and NHCs which consequently specify the root epidermal cell fate.…”