Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana

Abstract

Phytosulfokine (PSK) is a peptide growth factor that requires tyrosine sulfation carried out by tyrosylprotein sulfotransferase (TPST) for its activity. PSK is processed from precursor proteins encoded by five genes in Arabidopsis thaliana and perceived by receptor kinases encoded by two genes in Arabidopsis. pskr1-3 pskr2-1 and tpst-1 knockout mutants displayed reduced seed production, indicative of a requirement for PSK peptide signaling in sexual plant reproduction. Expression analysis revealed PSK precursor and PSK receptor gene activity in reproductive organs with strong expression of PSK2 in pollen. In support of a role for PSK signaling in pollen, in vitro pollen tube (PT) growth was enhanced by exogenously added PSK while PTs of pskr1-3 pskr2-1 and of tpst-1 were shorter. In planta, growth of wild-type pollen in pskr1-3 pskr2-1 and tpst-1 flowers appeared slower than growth in wild-type flowers. But PTs did eventually reach the base of the style, suggesting that PT elongation rate may not be responsible for the reduced fertility. Detailed analysis of anthers, style and ovules did not reveal obvious developmental defects. By contrast, a high percentage of unfertilized ovules in pskr1-3 pskr2-1 and in tpst-1 siliques displayed loss of funicular PT guidance, suggesting that PSK signaling is required to guide the PT from the transmitting tract to the embryo sac. Cross-pollination experiments with wild-type, pskr1-3 pskr2-1 and tpst-1 male and female parents revealed that both the PT and the female sporophytic tissue and/or female gametophyte contribute to successful PT guidance via PSK signaling and to fertilization success.

New Insights on Leucine-Rich Repeats Receptor-Like Kinase Orthologous Relationships in Angiosperms

“…These receptors have overlapping functions in promoting cellular proliferation, longevity and expansion (Matsubayashi et al, 2006; Amano et al, 2007; Hartmann et al, 2013). The PSKR subfamily is also required for PSK peptide signaling in sexual reproduction in plants (Stuhrwohldt et al, 2015). Moreover, these receptors play a role in modifying responses to biotic pathogens and wounding (Loivamaki et al, 2010; Mosher et al, 2013).…”

Arabinogalactan Proteins as Interactors along the Crosstalk between the Pollen Tube and the Female Tissues

“…PSK is perceived by receptor kinases and requires sulfation by a tyrosylprotein sulfotransferase (TPST) to be active. pskr1-3 pskr2-1 and tpst siliques present a high level of unfertilized ovules and loss of funicular guidance, suggesting the importance of PSK for funicular guidance (Stührwohldt et al, 2015). Curiously, PSKR1 was recently shown to be involved in plant defense to pathogens as well as PSK (Mosher and Kemmerling, 2013).…”

Gametophytic Pollen Tube Guidance: Attractant Peptides, Gametic Controls, and Receptors

“…The relationships between CNGC18 and MDIS1-MIK/PRK6 are of interest. Other pollen tube molecules for ovular guidance include glycosylphosphatidylinositol anchor and its biosynthesis proteins Dai et al, 2014), mitogen-activated protein kinases (Guan et al, 2014), AGC kinases for eukaryotic polarized cell growth (Zhang et al, 2009), endoplasmic reticulum-localized K + channel (Lu et al, 2011) and luminal proteins (Li et al, 2011), small secreted peptide phytosulfokine (Stührwohldt et al, 2015), and inositol polyphosphate kinases (Zhan et al, 2015). It remains to be elucidated whether these molecules are involved in sensing and competency control for LURE or other gametophytic attractant pathways .…”