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Plant Pathology: Personnel

Richard Hussey picture of Richard Hussey on a horse

Distinguished Research Professor
2309 Miller Plant Science Bldg.
Athens, GA 30602-7274
Phone: (706) 542-1254
hussey@uga.edu

ACADEMIC BACKGROUND

Ph.D. in Botany (Plant Pathology), University of Maryland, 1970
M.S. in Botany (Plant Pathology), University of Maryland, 1968
B.A. in Botany, Miami University, 1965

RESEARCH INTERESTS AND CURRENT EFFORTS

Our research goal is to define what makes a nematode a plant parasite. Our focus is the molecular and functional characterization of parasitism genes in root-knot and cyst nematodes. These highly successful parasites, which have the most evolutionarily advanced mode of parasitism of the plant-parasitic nematodes, have very specialized and complex feeding relationships with their host plants. Parasitism genes expressed in the nematode's esophageal gland cells encode secretory proteins that are released through its stylet to direct the interactions of the nematode with its host plants. The products, collectively called the parasitome, of parasitism genes secreted into susceptible host tissue modulate complex changes in morphology, function, and gene expression in recipient root cells to form elaborate, discrete feeding cells (Fig. 1, Model of nematode parasitism of a plant cell). Our approach is a direct molecular analysis of genes encoding secretory proteins expressed in the esophageal gland cells of the nematode. Gland-specific cDNA libraries are constructed by RT-PCR from expressed mRNA in cytoplasm microaspirated directly from the gland cells. We are developing a comprehensive profile of parasitism genes expressed in the gland cells during the nematode parasitic cycle, which is greatly expanding our knowledge about nematode parasitism genes and the function of the gene products in plant parasitism, ultimately defining what makes a nematode a plant parasite so it can attack plants and cause crop damage. Our parasitism gene analysis reveals a large number of novel protein sequences and paints a more complex picture of host cellular events under specific control by the nematode than previously hypothesized. Stylet secretions of these nematodes mimic bioactive plant peptide signals and include novel ubiquitin extension proteins and an arsenal of cell-wall degrading enzymes. Remarkably, over 70% of the parasitism genes have no homology with functionally annotated genes in the databases. In a broader context, these newly discovered parasitism genes are providing targets for intervention in the parasitic process for the development of novel strategies for managing these economically important crop pathogens in the future.
Appointment: 100% Research

PUBLICATIONS

Mitchum, M. G., R. S. Hussey, T. J. Baum, X. Wang, A. A. Elling, M. Wubben, and E. L. Davis. 2013. Nematode effector proteins: an emerging paradigm of parasitism. (Tansley Review). New Phytologist 199:678--698. (View article in pdf format)

Xue, B., N. Hamamouch, C. Li, G. Huang, R. S. Hussey, T. J. Baum, and E. L. Davis. 2013. The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103:175-181.

Hamamouch, N., C. Li, T. Hewezi, T. J. Baum, M. G. Mitchum, R. S. Hussey, L. O. Vodkin, and E. L. Davis. 2012. The interaction of the novel 30C02 cyst nematode effector protein with a plant β -1,3-endoglucanase may suppress host defence to promote parasitism. J. Expt. Bot. 63:3683-3696.

Vieira, P. , E. G. J. Danchin, C. Neveu, C. Crozat, S. Jaubert, R. S. Hussey, G. Enbler, P. Abad, J. De Almeida-Engler, P Castagnone-Sereno, and M. N. Rosso. 2011. The plant apoplasm is an important recipient compartment for nematode secreted proteins. J. Exp. Bot. 62:1241-1253.

Replogle, A., J.Wang, A. Bleckmann, R. S. Hussey, T. J. Baum, S. Shinichiro, E. L. Davis, X. Wang, R. Simon, and M. G. Mitchum. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant Journal 65:430-440.

Wang, J., A. Replogle, R. Hussey, T. Baum, X. Wang, E. L. Davis, and M. G. Mitchum. 2011. Identification of potential host plant mimics of CLV3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Molecular Plant Pathology 12:177-186.

Lee, C., D. Chronis, C. Kenning,, B. Peret, T. Hewezi, E. L. Davis, T. J. Baum, R. S. Hussey, M. Bennett, and M. G. Mitchum. 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.

Wang, J., C. Lee, A. Replogle, S. Joshi, D. Korkin, R. Hussey, T. J. Baum, E. L. Davis, X. Wang, and M. G. Mitchum. 2010. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytologist 187:1003-1017.

Hewezi, T., P. Howe, T. R. Maier, R. S. Hussey, M. G. Mitchum, E. L. Davis, and T. J. Baum. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera glycines. Plant Physiology 152:968-984.

Hussey, R. S. 2010. Go where the science leads you. Annu. Rev. Phytopathol. 48:1-19. (View article in pdf format)

Patel, N., N. Hamamouch, C. Li, T. Hewezi, R. S. Hussey, T. J. Baum, M. G. Mitchum and E. L. Davis. 2009. A nematode effector protein similar to annexins in host plants. J. Exper. Bot. 60:4510-4524. (View article in pdf format)

Atkinson, H. J., P. Urwin, and R. S. Hussey. 2009. Plant biotechnology and control. Pp. 338-362. In Perry, R. N., M. Moens, and J. Starr. (Eds.) Root-knot Nematodes. CAB International Publishing, Wallingford, UK.

Elling, A. A., M. Mitreva, X. Gai, J. Martin, J. Recknor, T. R. Maier, J. P. McDermott, R. S. Hussey, E. L. Davis, D. Nettleton, J. P. McCarter, and T. J. Baum. 2009. Sequence mining and transcript profiling to explore cyst nematode parasitism. BCM Genomics 10:58-75. (View article in pdf format)

Sindhu, A. S., T. R. Maier, M. G. Mitchum, R. S. Hussey, E. L. Davis and T. J. Baum. 2009. Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J. Exper. Botany 60:315-324. (View article in pdf format)

Hewezi, T., P. Howe, T. R. Maier, R. S. Hussey, M. G. Mitchum, E. L. Davis, and T. J. Baum. 2008. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. The Plant Cell 20:3080-3093. (View article in pdf format)

Davis, E. L., R. S. Hussey, M. G. Mitchum, and T. J. Baum. 2008. Parasitism proteins in nematode-plant interactions. Current Opinion Plant Biology 11:1-7. (View article in pdf format)

Davis, E. L., R. S. Hussey, and T. J. Baum. 2008. Parasitism genes: what they are revealing about parasitism. Pp. 17-44. In Berg, H. R. and Taylor, C. G. (eds). Cell biology of plant-nematode interactions. Springer-Verlag, Germany.

Elling, A. A., M. Mitreva, J. Recknor, X. Gai, J. Martin, T. R. Maier, J. P McDermott, T. Hewezi, D. Mck. Bird, E. L. Davis, R. S. Hussey, D. Nettleton, J. P. McCarter, and T. J. Baum. 2007. Divergent evolution of arrested development in the dauer stage of Caenorhabditis elegans and the infective stage of Heterodera glycines. Genome Biol. 8:R211.1–211.19. (View article in pdf format)

Elling, A. A., E. L. Davis, R. S. Hussey, and T. J. Baum. 2007. Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. Int. J. Parasitol. 37:1269-1279. (View article in pdf format)

Sukno, S. A., J. mcCuiston, M. Y. Wong, X. Want, M. R. Thon, R. S. Hussey, T. J. Baum, and E. L. Davis. 2007. Quantitative detection of double-stranded RNA-mediated gene silencing of parasitism genes in Heterodera glycines. J. Nematol. 39:145-152.

Mitchum, M., R. S. Hussey, E. L. Davis, and T. J. Baum. 2007. Chapter 3: Application of biotechnology to understand pathogenesis in nematode plant pathogens. Pp. 58-86. In Punja, Z. K., DeBoer, S., and Sanfacon, H. (Eds). Biotechnology and Plant Disease Management. CABI Publishing.

Baum, T. J., E. L. Davis, and R. S. Hussey. 2007. Root-knot and cyst nematode parasitism genes: the molecular basis of plant parasitism. Genetic Engineering, Principles and Methods, Volume 28:17-43. (View article in pdf format)

Huang, G, R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2006. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proceedings of the National Academy of Sciences USA 103:14302-14306. (View article in pdf format)

Huang, G, R. Dong, R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2006.  A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant-Microbe Interact.  19:463-470. (View article in pdf format)

Huang, G., R. Dong, R. Allen, E. L. Davis, T. J. Baum, and R. S. Husey. 2005. Two chorismate mutase genes from the root-knot nematode Meloidogyne incognita. Mol. Plant Pathology 6:23-30. (View article in pdf format)

Huang, G., R. Dong, R. Allen, E. L. Davis, T. J. Baum, and R. S. Husey. 2005. Developmental expression and molecular analysis of two Meloidogyne incognita pectate lyase genes. Int. J. Parasitol. 35:685-692. (View article in pdf format)

Wang, Xiaohong, M. G. Mitchum, Bingli Gao, Chunying Li, Hanane Diab, Thomas J. Baum, Richard S. Hussey, and Eric L. Davis. 2005. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathology 6:187-191. (View article in pdf format)

Gao, B., R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2004. Molecular characterization and developmental expression of a cellulose-binding protein gene in the soybean cyst nematode Heterodera glycines. Int. J. Parasitol. 34:1377-1383. (View article in pdf format)

Gao, B., R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2004. Developmental expression and biochemical properties of a beta-1,4-endoglucanase family in the soybean cyst nematode Heterodera glycines. Mol. Plant Pathol. 5: 93-104. (View article in pdf format)

Davis, E. L., R. S. Hussey, and T. J. Baum. 2004. Getting to the roots of parasitism by nematodes. Trends in Parasitol. 20:134-141. (View article in pdf format)

Huang, G, R. Dong, T. Maier, R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2004. Use of solid-phase subtractive hybridization for the identification of parasitism gene candidates from the root-knot nematode Meloidogyne incognita. Mol. Plant Pathol. 5:217-222. (View article in pdf format)

Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2003. The parasitome of the phytonematode Heterodera glycines. Mol. Plant-Microbe Interact. 16:720-726. (View article in pdf format)

Huang, G, B. Gao, T. Maier, R. Allen, E. L. Davis, T. J. Baum, and R. S. Hussey. 2003. A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 16:376-381. (View article in pdf format)

Hussey, R. S., E. L. Davis, and T. J. Baum. 2002. Secrets in secretions: genes that control nematode parasitism of plants. Braz. J. Plant Physiol. 14:183-194. (View article in pdf format)

Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2002. Identification of a new beta-1,4-endoglucanase expressed in the subventral gland cells of Heterodera glycines. J. Nematol. 33:12-15.

Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2002. Characterization and developmental expression of a chitinase gene in Heterodera glycines. Int. J. Parasitol. 32:1293-1300. (View article in pdf format)

De Boer, J. M., J. P. McDermott, E. L. Davis, R. S. Hussey, G. Smant, and T. J. Baum. 2002. Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. J. Nematol. 33:9-11.

De Boer, J. M., J. P. McDermott, X. Wang, T. Maier, F. Qui, R. S. Hussey, E. L. Davis, and T. J. Baum. 2002. The use of DNA microarrays for the developmental expression analysis of cDNAs from esophageal gland cell region of Heterodera glycines. Mol. Plant Pathol. 3:261-270.

Hussey, R. S., and G. J. W. Janssen. 2002. Chapter 3: Root-knot nematodes: Meloidogyne species. Pp. 43-70. In J. L. Starr, R. Cook, and J. Bridge (eds). Plant Resistance to Parasitic Nematodes. CAB International, United Kingdom.

Gao, B., T. Maier, E. Davis, T. Baum, and R. Hussey. 2002. Defining a plant-parasitic nematode: a profile of putative parasitism genes expressed in the esophageal glands of Heterodera glycines. Fourth International Congress of Nematology Poster (in Adobe Acrobat format).

Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2001. Molecular characterization and expression of two venom allergen-like secretory proteins from the soybean cyst nematode, Heterodera glycines. Int. J. Parasitol. 31:1617-1625. (View article in pdf format)

Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2001. Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode, Heterodera glycines. Mol. Plant-Microbe Interact. 14:1247-1254. (View article in pdf format)

Semblat, J-P., N. Rosso, R. S. Hussey, P. Abad and P. Castagnone-Sereno. 2001. Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 14:72-79.

Wang, X., Allen, R., Ding, X., Goellner, M., Maier, T., de Boer, J.M., Baum., T.J., Hussey, R.S., and Davis, E.L. 2001. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nemtode Heterodera glycines. Mol. Plant-Microbe Interact. 14:536-544.

Davis, E. L., R. S. Hussey, T. J. Baum, J. Bakker, A. Schots, M-N. Rosso, and P. Abad. 2000. Nematode parasitism genes. Annu. Rev. Phytopathol. 38:365-396. (View article in pdf format)

Hussey, R. S. and F. M. W. Grundler. 1998. Chapter 9: Nematode parasitism of plants. Pp. 213-243. In R. N. Perry and D. J. Wright (Eds.) Physiology and Biochemistry of Free-living and Plant-parasitic Nematodes. CAB International Press, England.

Ding, X., J. Shields, R. Allen, and R. S. Hussey. 1998. A secretory cellulose-binding protein cDNA cloned from root-knot nematode (Meloidogyne incognita). Mol. Plant-Microbe Interact. 11:952-959. (View article in pdf format)

Smant, G., J.P.W.G. Stokkermans, Y. Yan, J.M. deBoer, T.J. Baum, X. Wang, R.S. Hussey, F.J. Gommers, B. Henrissat, E. L. Davis, J. Helder, A. Schots, and J. Bakker. 1998. Endogenous cellulases in animals: Isolation of beta-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proceedings of the National Academy of Sciences USA 95:4906-4911.

Williamson, V. M. and R. S. Hussey. 1996. Nematode pathogenesis and resistance in plants. The Plant Cell. 8:1735-1745. (View article in pdf format)

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