Root-knot nematodes produce functional mimics of tyrosine-sulfated plant peptides

Authors: YIMER, HENOK - University Of California; LUU, DEE - University Of California; COOMER, ALISON - University Of California; ERCOLI, MARIA - University Of California; Vieira, Paulo; WILLIAMSON, VALERIE - University Of California; RONALD, PAMELA - University Of California; SIDDIQUE, SHAHID - University Of California

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/8/2023
Publication Date: 7/10/2023
Citation: Yimer, H.Z., Luu, D.D., Coomer, A., Ercoli, M.F., Reis Vieira, P.C., Williamson, V.M., Ronald, P.C., Siddique, S. 2023. Root-knot nematodes produce functional mimics of tyrosine-sulfated plant peptides. Proceedings of the National Academy of Sciences (PNAS). https://doi,org/10.1073/pnas.2304612120.
DOI: https://doi.org/10.1073/pnas.2304612120

Interpretive Summary: Plant-parasitic nematodes are among the most destructive plant pathogens, causing an annual economic loss of $8 billion to U.S. growers and over $100 billion worldwide. Root-infecting sedentary endoparasitic nematodes including root-knot nematodes (RKNs; Meloidogyne spp.) cause the greatest economic damage. The RKN species M. incognita, M. javanica, and M. arenaria boast extremely broad host ranges and can infect thousands of plant species, including annual and perennial crops and both dicots and monocots. The establishment of a long-term feeding site allows PPNs to acquire nutrients from their plant host and facilitates their development and reproduction. Here, we identify RKN genes encoding several peptides with high sequence similarity to both bacterial and plant. We further characterize their expression and investigate their potential roles in parasitism. This information will be used by plant pathologists to understand and manage the interactions between nematodes and their plant hosts.

Technical Abstract: Root-knot nematodes (Meloidogyne spp.) are highly evolved obligate parasites that threaten global food security. These parasites have a remarkable ability to establish elaborate feeding sites in roots, which are their only source of nutrients throughout their life cycle. A wide range of nematode effectors have been implicated in modulation of host pathways for feeding site development. Plants produce a diverse array of peptide hormones including plant peptides containing sulfated tyrosine (PSYs), which promote root growth via cell expansion and proliferation. A sulfated PSY-like peptide RaxX (required for activation of XA21 mediated immunity X) produced by the biotrophic bacterial pathogen (Xanthomonas oryzae pv. oryzae), has been previously shown to contribute to bacterial virulence. Here, we report the identification of genes from root-knot nematodes predicted to encode PSY-like peptides with high sequence similarity to both bacterial RaxX and plant PSYs. Synthetic peptides encoding predicted nematode PSY domains (MigPSYs) stimulate root growth in Arabidopsis. Transcript levels are highest early in the infection cycle. Down-regulation of MigPSY gene expression reduces root galling and egg production, suggesting that the MigPSYs serve as nematode virulence factors. Together these results indicate that nematodes and bacteria utilize similar sulfated peptides to hijack plant developmental signaling pathways to facilitate parasitism.