There are few examples of teams in the plant pathology scientific community that have made a greater impact on their field than that made by Richard Hussey, Eric Davis, and Thomas Baum on our understanding of how plantparasitic nematodes establish a parasitic relationship with their plant hosts. Hussey is widely recognized as a pioneer of molecular plant nematology. Davis and Baum received post-doctoral mentorship in the Hussey lab and while continuing a close collaborative relationship with the Hussey lab, each have established themselves in their own right in the field of molecular plant nematology as evidenced by publications and competitive grants received on their own. In addition to their individual and collective scholarly contributions to molecular nematology, they have also each made significant commitments to mentoring through graduate education and post-doctoral positions as evidenced by the number of scientists emanating from their programs that currently hold university faculty and USDA and industry research positions. Further evidence of their stature is the role these three play in an international union of plant nematologists that meets regularly to freely exchange information and publish together on selected topics. This team is the core of that group and provides the energy to maintain the productive associations.
The focus of their efforts is on the most economically important group of plant-parasitic nematodes. These are the root-knot and cyst nematodes that are sedentary, endoparasites of plants. They have developed innovative approaches to study the earliest stages of the parasitic relationship between the nematode and the plant. These efforts were directed at elucidating the components of stylet secretions (nematode equivalent of saliva) produced in the esophageal gland cells. They have not only adapted tools, such as micro-aspiration of the gland cell contents for cloning parasitism genes, and utilized classical techniques for enzyme isolation and characterization, but have also extended this research by using model systems such as the Arabidopsis–Heterodera schachtii and microarrays to profile the expression of known proteins and to identify new candidates involved in nematode pathogenesis. The results of these efforts have not only been published in the expected disciplinary journals such as the Journal of Nematology, International Journal for Parasitology, Molecular Plant Pathology, and Molecular Plant-Microbe Interactions, but have reached the wider audiences of Gene, Plant Cell, Plant Journal, and PNAS. They have also published analyses of this research in numerous reviews.
This research began to receive significant attention with the report of the first cellulase isolated from animals, a beta-1,4-endoglucanase. This was accomplished by the traditional approach of isolating candidate proteins with antibodies made against stylet secretion extracts. The subsequent group effort of isolation and characterization of the gene revealed a similarity to cellulases of bacterial origin and, thus, the suggestion of horizontal gene transfer between bacteria and nematodes. This seminal research spawned a body of literature on the isolation and characterization of cellulase genes from a variety of nematodes as well as in planta localization and developmental regulation of these genes during penetration and migration of the nematode. The global question of the role of these cell wall-degrading enzymes in nematode pathogenesis was resolved in a Plant Cell paper from the Davis laboratory demonstrating that the cellulases are secreted into plant roots only during the penetration and migration phases of nematode parasitism. Synthesis of these enzymes is turned off once syncytia formation is initiated. The body of pioneering information published by these investigators has identified over 60 cyst nematode and more than 50 root-knot nematode parasitism genes encoding a variety of secretory proteins including cellulose-binding proteins, pectate lyases, chitinases, venom allergen-like proteins, chorismate mutases, novel ubiquitin extension proteins, and signaling peptides. Over 65 of the parasitism genes have unknown functions and are unique to plant-parasitic nematodes. This team is now targeting functional analyses of the parasitism genes to dissect the molecular interactions of the root-knot and cyst nematodes with their host plants using gene expression analyses and RNA interference technology. In an MPMI paper, the Hussey laboratory recently demonstrated that a root-knot nematode secretory peptide stimulates root growth by directly interacting with a plant transcription factor. While early efforts focused on the nematode side of the equation, recent research from the Baum laboratory has utilized Arabidopsis mutants to investigate the host response to nematode parasitism in the Arabidopsis–H. schachtii pathosystem. They developed a high through-put system taking advantage of Arabidopsis microarrays to study plant gene expression. In a series of papers, they were able to demonstrate that Arabidopsis susceptibility to H. schachtii is modulated by the ethylene signal transduction pathway. Arabidopsis has also served as a model for the team to demonstrate that a cyst nematode parasitism gene product has a function similar to the CLAVATA3 signaling peptide that regulates plant stem cell fate.
Individually and collectively, these researchers have amassed an enviable record in the primary literature as well as reviews and book chapters. Collectively, the research from these three groups has advanced from a hypothesis focused on the role of nematode parasitism proteins to the elucidation of specific nematode enzymes and signaling peptides and the implication of plant metabolic pathways to provide a framework for understanding nematode parasitism. This effort began with the original biology and investigations of the root-knot nematode secretory proteins with Hussey and his mentorship of Davis and Baum (as well as others); however, these three have maintained dominant roles with Davis advancing the molecular biology and then Baum joining the efforts of the molecular investigations of the plant side of the relationship and more recently developing the functional genomics. While their collaborative spirit is widely known, it must also be acknowledged that they have maintained independence as evidenced by their independent records of competitive funding, publishing, and mentoring. The Hussey legacy of mentoring is also being continued by Davis with former students and post-docs in faculty or USDA positions at the University of Missouri and Cornell. Baum has placed a USDA scientist at Mississippi State University. This represents an effort not only in scholarship but also to the continuation of the discipline through mentoring of the next generation of scientists.
