Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/20/2011
Publication Date: 2/1/2011
Citation: Lee,, C., Chronis, D.N., Kenning,, C., Peret,, B., Hewezi,, T., Davis,, E.L., Baum,, T.J., Hussey,, R., Bennett,, M., Mitchum,, M.G. 2011. The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiology. 155:866-880. Interpretive Summary: Plant cyst nematodes are obligate endoparasites that hatch in the soil, locate and penetrate a root, then select a cell to transform into a specialized feeding site, the syncytium. Cyst nematodes dedifferentiate the host cell, and incorporate neighboring cells into the growing syncytium. Current hypotheses suggest this process is controlled by injection of nematode stylet secretions containing esophageal gland cell effector proteins into the host cell. The dorsal esophageal gland protein 19C07 is expressed in parasitic life stages and presumably secreted into host cells, potentially playing a role in syncytium development. This work reports the cloning and characterization of 19C07 gene from the beet cyst nematode, Heterodera schachti. We show that 19C07 interacts with the auxin influx transporter, LAX3. Because cellular auxin concentrations increase in the developing syncytium, this interaction was explored. Hs19C07 most likely increases the activity of LAX3 auxin transport and may provide a mechanism for cyst nematodes to modulate auxin flow into the developing syncytium.
Technical 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 thaliana auxin influx transporter LAX3. LAX3 is expressed in cells overlying lateral root primordia, providing auxin signaling that triggers expression of cell wall modifying enzymes (CWMEs), allowing lateral roots to emerge. We found that LAX3 and polygalacturonase, a LAX3-induced CWME, 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 and the aux1lax1lax2lax3 quadruple mutants. 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.