@article{wang_replogle_hussey_baum_wang_davis_mitchum_2011, title={Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii}, volume={12}, ISSN={["1364-3703"]}, DOI={10.1111/j.1364-3703.2010.00660.x}, abstractNote={SUMMARY In this article, we present the cloning of two CLAVATA3/ESR ( CLE )‐like genes, HsCLE1 and HsCLE2 , from the beet cyst nematode Heterodera schachtii , a plant‐parasitic cyst nematode with a relatively broad host range that includes the model plant Arabidopsis. CLEs are small secreted peptide ligands that play important roles in plant growth and development. By secreting peptide mimics of plant CLEs, the nematode can developmentally reprogramme root cells for the formation of unique feeding sites within host roots for its own benefit. Both HsCLE1 and HsCLE2 encode small secreted polypeptides with a conserved C‐terminal CLE domain sharing highest similarity to Arabidopsis CLEs 1–7. Moreover, HsCLE2 contains a 12‐amino‐acid CLE motif that is identical to AtCLE5 and AtCLE6. Like all other plant and nematode CLEs identified to date, HsCLEs caused wuschel ‐like phenotypes when overexpressed in Arabidopsis, and this activity was abolished when the proteins were expressed without the CLE motif. HsCLEs could also function in planta without a signal peptide, highlighting the unique, yet conserved function of nematode CLE variable domains in trafficking CLE peptides for secretion. In a direct comparison of HsCLE2 overexpression phenotypes with those of AtCLE5 and AtCLE6, similar shoot and root phenotypes were observed. Exogenous application of 12‐amino‐acid synthetic peptides corresponding to the CLE motifs of HsCLEs and AtCLE5/6 suggests that the function of this class of CLEs may be subject to complex endogenous regulation. When seedlings were grown on high concentrations of peptide (10 µ m ), root growth was suppressed; however, when seedlings were grown on low concentrations of peptide (0.1 µ m ), root growth was stimulated. Together, these findings indicate that AtCLEs1–7 may be the target peptides mimicked by HsCLEs to promote parasitism.}, number={2}, journal={MOLECULAR PLANT PATHOLOGY}, author={Wang, Jianying and Replogle, Amy and Hussey, Richard and Baum, Thomas and Wang, Xiaohong and Davis, Eric L. and Mitchum, Melissa G.}, year={2011}, month={Feb}, pages={177–186} }
 @article{replogle_wang_bleckmann_hussey_baum_sawa_davis_wang_simon_mitchum_2011, title={Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE}, volume={65}, ISSN={["1365-313X"]}, DOI={10.1111/j.1365-313x.2010.04433.x}, abstractNote={Plant-parasitic cyst nematodes secrete CLAVATA3 (CLV3)/ESR (CLE)-like effector proteins. These proteins have been shown to act as ligand mimics of plant CLE peptides and are required for successful nematode infection; however, the receptors for nematode CLE-like peptides have not been identified. Here we demonstrate that CLV2 and CORYNE (CRN), members of the receptor kinase family, are required for nematode CLE signaling. Exogenous peptide assays and overexpression of nematode CLEs in Arabidopsis demonstrated that CLV2 and CRN are required for perception of nematode CLEs. In addition, promoter–reporter assays showed that both receptors are expressed in nematode-induced syncytia. Lastly, infection assays with receptor mutants revealed a decrease in both nematode infection and syncytium size. Taken together, our results indicate that perception of nematode CLEs by CLV2 and CRN is not only required for successful nematode infection but is also involved in the formation and/or maintenance of nematode-induced syncytia.}, number={3}, journal={PLANT JOURNAL}, author={Replogle, Amy and Wang, Jianying and Bleckmann, Andrea and Hussey, Richard S. and Baum, Thomas J. and Sawa, Shinichiro and Davis, Eric L. and Wang, Xiaohong and Simon, Ruediger and Mitchum, Melissa G.}, year={2011}, month={Feb}, pages={430–440} }
 @article{wang_lee_replogle_joshi_korkin_hussey_baum_davis_wang_mitchum_2010, title={Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins}, volume={187}, ISSN={["1469-8137"]}, DOI={10.1111/j.1469-8137.2010.03300.x}, abstractNote={*Soybean cyst nematodes (Heterodera glycines) produce secreted effector proteins that function as peptide mimics of plant CLAVATA3/ESR (CLE)-like peptides probably involved in the developmental reprogramming of root cells to form specialized feeding cells called syncytia. *The site of action and mechanism of delivery of CLE effectors to host plant cells by the nematode, however, have not been established. In this study, immunologic, genetic and biochemical approaches were used to reveal the localization and site of action of H. glycines-secreted CLE proteins in planta. *We present evidence indicating that the nematode CLE propeptides are delivered to the cytoplasm of syncytial cells, but ultimately function in the apoplast, consistent with their proposed role as ligand mimics of plant CLE peptides. We determined that the nematode 12-amino-acid CLE motif peptide is not sufficient for biological activity in vivo, pointing to an important role for sequences upstream of the CLE motif in function. *Genetic and biochemical analysis confirmed the requirement of the variable domain in planta for host-specific recognition and revealed a novel role in trafficking cytoplasmically delivered CLEs to the apoplast in order to function as ligand mimics.}, number={4}, journal={NEW PHYTOLOGIST}, author={Wang, Jianying and Lee, Chris and Replogle, Amy and Joshi, Sneha and Korkin, Dmitry and Hussey, Richard and Baum, Thomas J. and Davis, Eric L. and Wang, Xiaohong and Mitchum, Melissa G.}, year={2010}, pages={1003–1017} }
 @article{sindhu_maier_mitchum_hussey_davis_baum_2009, title={Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success}, volume={60}, ISSN={["1460-2431"]}, DOI={10.1093/jxb/ern289}, abstractNote={Cyst nematodes are highly evolved sedentary plant endoparasites that use parasitism proteins injected through the stylet into host tissues to successfully parasitize plants. These secretory proteins likely are essential for parasitism as they are involved in a variety of parasitic events leading to the establishment of specialized feeding cells required by the nematode to obtain nourishment. With the advent of RNA interference (RNAi) technology and the demonstration of host-induced gene silencing in parasites, a new strategy to control pests and pathogens has become available, particularly in root-knot nematodes. Plant host-induced silencing of cyst nematode genes so far has had only limited success but similarly should disrupt the parasitic cycle and render the host plant resistant. Additional in planta RNAi data for cyst nematodes are being provided by targeting four parasitism genes through host-induced RNAi gene silencing in transgenic Arabidopsis thaliana, which is a host for the sugar beet cyst nematode Heterodera schachtii. Here it is reported that mRNA abundances of targeted nematode genes were specifically reduced in nematodes feeding on plants expressing corresponding RNAi constructs. Furthermore, this host-induced RNAi of all four nematode parasitism genes led to a reduction in the number of mature nematode females. Although no complete resistance was observed, the reduction of developing females ranged from 23% to 64% in different RNAi lines. These observations demonstrate the relevance of the targeted parasitism genes during the nematode life cycle and, potentially more importantly, suggest that a viable level of resistance in crop plants may be accomplished in the future using this technology against cyst nematodes.}, number={1}, journal={JOURNAL OF EXPERIMENTAL BOTANY}, author={Sindhu, Anoop S. and Maier, Tom R. and Mitchum, Melissa G. and Hussey, Richard S. and Davis, Eric L. and Baum, Thomas J.}, year={2009}, month={Jan}, pages={315–324} }
 @article{hewezi_howe_maier_hussey_mitchum_davis_baum_2008, title={Cellulose Binding Protein from the Parasitic Nematode Heterodera schachtii Interacts with Arabidopsis Pectin Methylesterase: Cooperative Cell Wall Modification during Parasitism}, volume={20}, ISSN={["1532-298X"]}, DOI={10.1105/tpc.108.063065}, abstractNote={Plant-parasitic cyst nematodes secrete a complex of cell wall-digesting enzymes, which aid in root penetration and migration. The soybean cyst nematode Heterodera glycines also produces a cellulose binding protein (Hg CBP) secretory protein. To determine the function of CBP, an orthologous cDNA clone (Hs CBP) was isolated from the sugar beet cyst nematode Heterodera schachtii, which is able to infect Arabidopsis thaliana. CBP is expressed only in the early phases of feeding cell formation and not during the migratory phase. Transgenic Arabidopsis expressing Hs CBP developed longer roots and exhibited enhanced susceptibility to H. schachtii. A yeast two-hybrid screen identified Arabidopsis pectin methylesterase protein 3 (PME3) as strongly and specifically interacting with Hs CBP. Transgenic plants overexpressing PME3 also produced longer roots and exhibited increased susceptibility to H. schachtii, while a pme3 knockout mutant showed opposite phenotypes. Moreover, CBP overexpression increases PME3 activity in planta. Localization studies support the mode of action of PME3 as a cell wall-modifying enzyme. Expression of CBP in the pme3 knockout mutant revealed that PME3 is required but not the sole mechanism for CBP overexpression phenotype. These data indicate that CBP directly interacts with PME3 thereby activating and potentially targeting this enzyme to aid cyst nematode parasitism.}, number={11}, journal={PLANT CELL}, author={Hewezi, Tarek and Howe, Peter and Maier, Tom R. and Hussey, Richard S. and Mitchum, Melissa Goellner and Davis, Eric L. and Baum, Thomas J.}, year={2008}, month={Nov}, pages={3080–3093} }
 @article{hussey_barker_1976, title={Influence of nematodes and light sources on growth and nodulation of soybean}, volume={8}, number={1}, journal={Journal of Nematology}, author={Hussey, R. S. and Barker, K. R.}, year={1976}, pages={48} }