A microbially derived tyrosine sulfated peptide mimics a plant peptide hormone

Abstract

SummaryThe biotrophic pathogen Xanthomonas oryzae pv. oryzae (Xoo) produces a sulfated peptide named RaxX, which shares similarity to peptides in the PSY (plant peptide containing sulfated tyrosine) family. We hypothesize that RaxX functionally mimics the growth stimulating activity of PSY peptides.Root length was measured in Arabidopsis and rice treated with synthetic RaxX peptides. We also used comparative genomic analysis and Reactive Oxygen Species (ROS) burst assay to evaluate the activity of RaxX and PSY peptides.Here we found that a synthetic sulfated RaxX derivative comprising 13 residues (RaxX13-sY), highly conserved between RaxX and PSY, induces root growth in Arabidopsis and rice in a manner similar to that triggered by PSY. We identified residues that are required for activation of immunity mediated by the rice XA21 receptor but that are not essential for root growth induced by PSY. Finally, we showed that a Xanthomonas strain lacking raxX is impaired in virulence.These findings suggest that RaxX serves as a molecular mimic of PSY peptides to facilitate Xoo infection and that XA21 has evolved the ability to recognize and respond specifically to the microbial form of the peptide.

Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor

“…In rice, the transmembrane immune receptor XA21, which shares similarities to animal Toll-like receptors and the Arabidopsis flagellin-sensitive 2 and EF-Tu receptors (6), responds to sulfated derivatives of the microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced by the Gram-negative pathogenic bacterium Xanthomonas oryzae pv. oryzae (Xoo) (7)(8)(9)(10). The XA21/RaxX interaction conforms to the "gene-for-gene relationship" initially described by Flor (11) in the 1940s.…”

Phytoparasitic Nematode Control of Plant Hormone Pathways

“…It was recently discovered that the fungal pathogen Fusarium oxysporum and the bacterial pathogen Xanthomonas oryzae pv. oryzae secrete functional peptide mimics of plant rapid alkalinization factor and plant peptide containing sulfated tyrosine peptides, respectively (Masachis et al, 2016;Pruitt et al, 2017). Thus, as we continue to uncover the complex interplay between peptide and hormone signaling in plantnematode interactions, the findings are likely to have much broader applicability in molecular plant-microbe interactions than previously thought.…”

Sulfated RaxX, which represents an unclassified group of ribosomally synthesized post-translationally modified peptides, binds a host immune receptor

“…Although RaxX shares similarities with PSY1 in both sequence and root growth-123 promoting activities, synthetic sulfated PSY1 peptides derived from Arabidopsis and rice 124 fail to activate XA21-dependent immune responses (Pruitt et al, 2017). Consistent with 125 these reports, sulfated PSY1 failed to specifically bind XA21 ECD (Figure 2).…”

“…This K D is 20-fold higher than the sulfated form (RaxX21-sY), which had a K D of 20 120 nM (Figure 2), indicating that sulfated RaxX binds XA21 with higher affinity than non-121 sulfated RaxX. 122Although RaxX shares similarities with PSY1 in both sequence and root growth-123 promoting activities, synthetic sulfated PSY1 peptides derived from Arabidopsis and rice 124 fail to activate XA21-dependent immune responses (Pruitt et al, 2017). Consistent with 125 these reports, sulfated PSY1 failed to specifically bind XA21 ECD (Figure 2).…”

“…59In rice, the transmembrane immune receptor XA21, which shares similarities to 60 animal TOLL like receptors (TLRs) and the Arabidopsis flagellin-sensitive 2 (FLS2) and 61 EF-Tu receptors (EFR) (Dardick et al, 2012), responds to sulfated derivatives of the 62 microbial peptide RaxX (required for activation of XA21-mediated immunity X) produced 63 by the Gram-negative pathogenic bacterium Xanthomonas oryzae pv. oryzae (Xoo) 64 (Pruitt et al, 2015(Pruitt et al, , 2017 Schwessinger et al, 2016; Wei et al, 2016). Tyrosine sulfated 65RaxX16, a 16-residue synthetic peptide derived from residues 40-55 of the 60-residue 66 RaxX precursor, is the shortest characterized immunogenic derivative of RaxX (Pruitt et 67 al., 2017).…”