title: The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development.
abstract: Plant-parasitic cyst nematodes penetrate plant roots and transform cells near the vasculature into specialized feeding sites called syncytia. Syncytia form by incorporating neighboring cells into a single fused cell by cell wall dissolution. This process is initiated via injection of esophageal gland cell effector proteins from the nematode stylet into the host cell. Once inside the cell, these proteins may interact with host proteins that regulate the phytohormone auxin, as cellular concentrations of auxin increase in developing syncytia. Soybean cyst nematode (Heterodera glycines) Hg19C07 is a novel effector protein expressed specifically in the dorsal gland cell during nematode parasitism. Here, we describe its ortholog in the beet cyst nematode (Heterodera schachtii), Hs19C07. We demonstrate that Hs19C07 interacts with the Arabidopsis (Arabidopsis thaliana) auxin influx transporter LAX3. LAX3 is expressed in cells overlying lateral root primordia, providing auxin signaling that triggers the expression of cell wall-modifying enzymes, allowing lateral roots to emerge. We found that LAX3 and polygalacturonase, a LAX3-induced cell wall-modifying enzyme, are expressed in the developing syncytium and in cells to be incorporated into the syncytium. We observed no decrease in H. schachtii infectivity in aux1 and lax3 single mutants. However, a decrease was observed in both the aux1lax3 double mutant and the aux1lax1lax2lax3 quadruple mutant. In addition, ectopic expression of 19C07 was found to speed up lateral root emergence. We propose that Hs19C07 most likely increases LAX3-mediated auxin influx and may provide a mechanism for cyst nematodes to modulate auxin flow into root cells, stimulating cell wall hydrolysis for syncytium development.
authors.affiliation: Division of Plant Sciences, Interdisciplinary Plant Group and Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211, USA.
authors.forename: Chris
authors.initials: C
authors.lastname: Lee
authors.forename: Demosthenis
authors.initials: D
authors.lastname: Chronis
authors.forename: Charlotte
authors.initials: C
authors.lastname: Kenning
authors.forename: Benjamin
authors.initials: B
authors.lastname: Peret
authors.forename: Tarek
authors.initials: T
authors.lastname: Hewezi
authors.forename: Eric L
authors.initials: EL
authors.lastname: Davis
authors.forename: Thomas J
authors.initials: TJ
authors.lastname: Baum
authors.forename: Richard
authors.initials: R
authors.lastname: Hussey
authors.forename: Malcolm
authors.initials: M
authors.lastname: Bennett
authors.forename: Melissa G
authors.initials: MG
authors.lastname: Mitchum
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D017360:Arabidopsis / Q000235:genetics / Q000469:parasitology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002473:Cell Wall / Q000469:parasitology; D018506:Gene Expression Regulation, Plant; D015726:Giant Cells / Q000469:parasitology; D015801:Helminth Proteins / Q000502:physiology*; D006790:Host-Parasite Interactions; D007210:Indoleacetic Acids / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism*; D008969:Molecular Sequence Data; D009154:Mutation; D009348:Nematoda / Q000502:physiology*; D010937:Plant Growth Regulators / Q000378:metabolism; D018517:Plant Roots / Q000235:genetics / Q000254:growth & development / Q000469:parasitology; D011096:Polygalacturonase / Q000235:genetics / Q000378:metabolism; D018749:RNA, Plant / Q000235:genetics
chemical_list: C100794:AUX1 protein, Arabidopsis; D029681:Arabidopsis Proteins; D015801:Helminth Proteins; D007210:Indoleacetic Acids; C531125:LAX3 protein, Arabidopsis; D026901:Membrane Transport Proteins; D010937:Plant Growth Regulators; D018749:RNA, Plant; D011096:Polygalacturonase