TEACHING:

PP790-004/Special Topics: Phytonematology (formerly PP504) – 3 credits, Spring of alternate years



Prerequisite: PP 315 or Consent of Instructor.  I am the lead instructor for this introductory course in nematology. Phytonematodes are microscopic worms (often less than 1mm long) that are soil-dwelling, and they mainly attack plant roots. The course is designed for students with a background in plant pathology, biology, or agricultural sciences, however no prior experience in plant pathology or nematology is required (PP 315 or equivalent is preferred). Graduate students in majors related to plant pathology are welcome, and Phytonematology is open to upper-level undergraduate students with consent of the instructor. Strong emphasis is placed on the integration of classical nematology with modern approaches, from nematode identification and control to molecular biology and host-parasite interactions.  The class consists of 3 lectures per week — the first half of the course includes comprehensive background information in phytonematology provided by the instructor and then moves towards examinations of topic-based literature as selected and presented by students in the second half of the course.

PP502/Plant Disease: Methods & Diagnosis – 2 credits, Fall semester every year

Dr. Tim Sit is the primary instructor of this course that covers methods and diagnosis for plant diseases induced by four major pathogen groups – bacteria, fungi, nematodes, and viruses.  I teach the nematology portion of PP 502 that provides the basics in diagnosing and working with plant nematodes.

PP707/Host-Microbe Interactions – 3 credits, Spring semester every year

Dr. Ralph Dean is the primary instructor of this course that covers the fundamentals of cellular and molecular interactions of plant hosts with different pathogen groups  I teach the nematology portion of PP 707 that provides the basics in plant-nematode interactions on both the cellular and molecular levels.

RESEARCH:

Our lab’s primary interest is with plant-parasitic (phyto)nematodes, but we are also interested in all aspects of host-parasite interactions. The main objective of our research is to combine information that we generate in both basic and applied investigations towards the goal of improving the control of plant-parasitic nematodes in agriculture. Our present research projects involve:

1. Identification and functional analyses of secreted nematode effector proteins
2. Nematode genomics emphasizing parasitism gene expression and epigenetics
3. Plant host cellular and molecular targets and responses to nematode effectors
4. Identification of virus endosymbionts within plant nematodes
5. Management of plant nematodes, both conventional and novel

The majority of our research centers around the soybean cyst nematode (SCN), Heterodera glycines, the sugarbeet cyst nematode (BCN), Heterodera schachtii, the tobacco cyst nematode (TCN), Globodera tabacum, and the root-knot nematodes,Meloidogyne spp. Cyst nematodes have a very narrow plant host range, while root-knot nematodes have a very wide range of host plant species. Both types of nematodes enter plant roots completely and transform selected plant cells into elaborate feeding sites that act as permanent nutrient sinks for the rest of the nematode’s sedentary life cycle. Cyst and root-knot nematodes cause billions of dollars in damage each year to many different crops world-wide, and environmentally-safe means of their control are in great demand.

Our primary investigations focus on the effector (parasitism) proteins secreted from cyst nematodes and root-knot nematodes that are critical in the plant infection process, and we have employed multiple approaches to isolate the “parasitism genes” (Davis et al., 2000, 2004, 2008) that encode these molecular signals.  Greater than fifty parasitism genes have each been isolated from cyst and root-knot nematodes to date that include a majority of encoded novel effector proteins and limited similarities in the effector repertoires between cyst and root-knot nematodes. Current investigations use Arabidopsis thaliana as a plant model for the functional analyses of nematode effector proteins and their roles in plant parasitism by nematodes. Assays include analyses of effector expression in plants, interactions with host proteins. and parasitism gene silencing using plant host-derived RNA interference (RNAi). Some research highlights include:

1. Discovery of the first endogenous cellulases in animals – cyst nematodes (Smant et al., 1998)
2. Early evidence for horizontal gene transfer (HGT) from microbes to nematodes (Smant et al., 1998; Yan et al., 1998, 2001; Davis et al., 2000)
3. First report of a nematode effector protein that functionally mimics the bioactive plant CLAVATA3/ESR (CLE) peptides (Wang et al., 2001, 2005; Mitchum et al., 2008, 2012)
4. Use of plant host-derived RNAi to silence target nematode parasitism genes and reduce nematode infection of plants (Huang et al., 2006; Sindhu et al., 2008; Patel et al., 2008, 2010).
5. Identification of novel viruses that infect plant nematodes (Ruark et al., 2017, 2018, 2020).

Our lab collaborates closely on many projects with selected U.S and international scientists to form an International Molecular Plant-Nematode Interactions Group that includes the labs of Thomas J. Baum of Iowa State University; Richard S. Hussey of the University of Georgia; Melissa G. Mitchum of the University of Georgia; Tarek Hewezi of the University of Tennessee; Xiaohong Wang of Cornell University; Martin Wubben of USDA-ARS at Mississippi State; Godlieve Gheysen of the University of Gent, Belgium; John T. Jones of the James Hutton Institute, Scotland; Pierre Abad and Bruno Favery of INRA, France; Jaap Bakker, Aska Goverse and Geert Smant of Wageningen University, The Netherlands.

Selected Research Publications:

• Schwarz, T., Li, C., Yencho, C.G., Pecota, K.V., Heim, C., Davis, E.L. 2021. Screening sweetpotato genotypes for resistance to a North Carolina isolate of Meloidogyne enterolobii. Plant Disease 105:1101-1107.
• Wang, J., Dhroso, A., Liu, X., Baum, T.J., Hussey, R.S., Davis, E.L., Wang, X., Korkin, D., Mitchum, M.G. 2021. Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal. New Phytologist 229:563-574.
• Ruark, C.L., E.L. Davis, T.L. Sit. 2020. Localization of viral and host RNA within soybean cyst nematode via fluorescence in situ hybridization. Experimental Parasitology 211: doi.org/10.1016/j.exppara.2020.107866.
• Ruark, C.L., Gardner, M., Mitchum, M.G., Davis, E.L., Sit, T. 2018. Novel RNA viruses within plant parasitic cyst nematodes. PLoS One: doi.org/10.1371/journal.pone.0193881.
• Gardner, M., Dhroso, A., Johnson, N., Davis, E.L., Baum, T.J., Korkin, D., Mitchum, M.G. 2018. Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode, Heterodera glycines. Scientific Reports 8:2505 / DOI:10.1038/s41598-018-20536-5.
• Ruark, C.L., Koenning, S.R., Davis, E.L., Opperman, C.H., Lommel, S.A., Mitchum, M.G., Sit, T.L. 2017. Soybean cyst nematode culture collections and field populations from North Carolina and Missouri reveal high incidences of infection by viruses. PLoS One 12(1): e0171514.doi:10.1371/journal.pone.0171514
• Vang, L.E., Opperman, C.H., Schwarz, M.R., Davis, E.L. 2016. Spirotetramat causes an arrest of nematode juvenile development. Nematology 18:121-131.
• Hewezi, T., Juvale, P.S., Sarbottam, P., Maier, T.R., Rambani, A., Rice, J.H., Mitchum, M.G., Davis, E.L., Hussey, R.S., Baum, T.J. 2015. The novel cyst nematode effector protein 10A07 targets and recruits host post-translational machinery to mediate its nuclear trafficking and promote parasitism. Plant Cell 27:891-907.
• Rutter, W.B., Hewezi, T., Maier, T.R., Mitchum, M.G., Davis, E.L., Hussey, R.S., Baum, T.J. 2014. Members of the Meloidogyne avirulence gene family contain multiple plant ligand-like motifs. Phytopathology 104(8):879-885.
• 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 beta-1,3 endoglucanase may suppress host defence to promote parasitism. Journal of Experimental Botany 63(10):3683-3695.
• Lee, Chris, Demosthenis Chronis, Charlotte Kenning, Benjamin Peret, Tarek Hewezi, Eric L. Davis, Thomas J. Baum, Richard Hussey, Malcolm Bennett, and Melissa 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.
• Hamamouch, Noureddine, Chunying Li, Pil Joon Seo, Chung-Mo Park, and Eric L. Davis. 2011. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Molecular Plant Pathology 12:355-364.
• Replogle, Amy; Wang, Jianying; Bleckman, Andrea; Hussey, Richard; Baum, Thomas; Sawa, Shinichiro; Davis, Eric; Wang, Xiaohong; Simon, Rüdiger; Mitchum, Melissa. 2011. Nematode CLE Signaling in Arabidopsis Requires CLAVATA2 and CORYNE. Plant Journal 65:430-440.
• Wang, J., Lee, C., Replogle, A., Joshi, S., Korkin, D., Hussey, R. S., Baum, T.J., Davis, E.L., Wang,  X., and Mitchum, M.G. 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 schachtii. Plant Physiology 152:968-984.
• Patel, N., N. Hamamouch, C. Li, T. Hewezi, R. Hussey, T. Baum, M. Mitchum, and E.L. Davis.  2010. A nematode parasitism protein similar to annexins in host plants. Journal of Experimental Botany 61:235-248.
• Rehman, S., P. Butterbach, H. Popeijus, H. Overmars, E.L. Davis, J.T.Jones, A. Goverse, J. Bakker, and G. Smant. 2009. Identification and characterization of the most abundant cellulases in stylet secretions from Globodera rostochiensis.Phytopathology 99:194-202.
• Elling, A.A., M. Mitreva, X. Gai, J. Martin, J. Recknor, E.L. Davis, R.S. Hussey, D. Nettleton, J.P.   McCarter, and T.J. Baum. 2009.Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 10:58 doi:10.1186/1471-2164-10-58.
• Patel, N., N. Hamamouch, C. Li, R. Hussey, M. Mitchum, T. Baum, X. Wang, and E.L. Davis. 2008. Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. Journal of Nematology:40:299-310.
• 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.  Plant Cell 20:3080-3093 (doi;10.1105/tpc.108.063065).
• Abad, P., J. Aury, P. Castagnone-Sereno, E.G.J. Danchin, E. Deleury, J. Gouzy, V. Anthouard, F. Artiguenave, V.C. Blok, M.C. Caillaud, P.M. Coutinho, C. Dasilva, F. De Luca, F. Deau, M. Esquibet, B. Favery, T. Flutre, J.V. Goldstone, N. Hamamouch, T. Hewezi, O. Jaillon, C. Jubin, P. Leonetti, M. Magliano, T.R. Maier, G. Markov, P. McVeigh, L. Perfus-Barbeoch, G. Pesole, J. Poulain, M.  Robinson-Rechavi, M.N. Rosso, E. Sallet, B. Ségurens, G. Smant, D. Steinbach,   T. Tytgat, E. Ugarte, C. van Ghelder, P. Veronico, T.J. Baum, M. Blaxter, T. Bleve-Zacheo,   E. L. Davis, J.J. Ewbank, E. Grenier, B. Henrissat, J.T. Jones, V. Laudet, A. G. Maule, H. Quesneville, T. Schiex, J. Weissenbach, P. Wincker. 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26:909-915.
• Sindhu, Anoop S., Tom R. Maier, Melissa G. Mitchum, Richard S. Hussey, Eric L. Davis, Thomas J. Baum. 2008. Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. Journal of Experimental Botany 60:315-324 (doi:10.1093/jxb/ern289).
• Wong, M.Y., J.S. Huang, and E.L. Davis. 2007. Isolation and characterization of a nitric oxide synthase (NOS)-like protein of pea (Pisum sativum L.). Journal of Bioscience 18(2):1-14.
•  Elling, A.A., M. Mitreva, J. Recknor, X. Gai, J. Martin, T.R. Maier, J.P. McDermott, T. Hewezi, D. M. 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 ofCaenorhabditis elegans and the infective stage of Heterodera glycines. Genome Biology 8:R211.
• McCuiston, J.L., L.C. Hudson, S.A. Subbotin, E.L. Davis, and C.Y. Warfield. 2007. Conventional and PCR detection ofAphelenchoides fragariae in diverse ornamental host plant species. Journal of Nematology 39:343-355.
• Sukno, S.A., McCuiston, J., Wong, M.Y., Wang,  X., Thon,  M.R., Hussey,  R.S., Baum, T.J., and    Davis,  E.L. 2007. Quantitative detection of double-stranded RNA-mediated gene silencing of parasitism genes in Heterodera glycines. Journal of Nematology39:145-152.
• * Elling, A.A., Davis, E.L., Hussey, R.S., Baum T.J.  2007. Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. International Journal for Parasitology 37:1269-1279.
•  Wang, X., Replogle, A., Davis, E.L., Mitchum, M.G. 2007. The tobacco NtCel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Molecular Plant Pathology 8:423-436.
• 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 103:14302-14306.
•  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.  Molecular Plant  Microbe Interactions 19:463-470.
• Wang X., Mitchum M.G., Gao B., Li C., Diab H., Baum T.J., Hussey R.S., Davis E.L. 2005. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology 6:187-191.
• Gao, B., R. Allen, T. Maier, E. L. Davis, T. J. Baum, and R. S. Hussey. 2003. The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 16:270-276.
• 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.  Molecular Plant-Microbe Interactions16: 376-381.
• * Cervantes-Flores, J.C., G.C. Yencho, and E.L. Davis. 2002. Host reactions of sweetpotato genotypes to root-knot nematodes and variation in virulence of Meloidogyne incognita populations.  HortScience 37(7):1112-1116.
• 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 cloned from esophageal gland cell of Heterodera
  glycines. Molecular Plant Pathology 3(4):261-270.
•  Yan, Y., and E. L. Davis.  2002.  Characterisation of guanylyl cyclase genes in the soybean cyst nematode, Heterodera glycines.  International Journal for Parasitology 32:65-72.
•  Goellner, M., X. Wang, and Davis, E. L.  2001.  Endo-beta-1,4-glucanase expression in compatible  plant-nematode interactions.  Plant Cell 13: 2241-2255.
• 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.  Molecular Plant-Microbe Interactions 14:1247-1254.
• Wang, X., R. Allen, X. Ding, M. Goellner, T. Maier, J. M. de Boer, T. J. Baum, R. S. Hussey, and   E. L. Davis.  2001. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode, Heterodera glycines.Molecular Plant-Microbe Interactions14: 536-544.
• Yan, Y., G. Smant, and E. L. Davis.  2001.  Functional screening yields a new beta-1,4 endoglucanase gene from Heterodera glycines that may be the product of a recent gene duplication.  Molecular Plant-Microbe Interactions14:63-71.
• Wang, X., D.M. Meyers, T. J. Baum,  G., Smant, R. S. Hussey, and E. L. Davis. 1999.  In planta localization of a ß-1,4-endoglucanse secreted by Heterodera glycines.  Molecular Plant-Microbe Interactions 12:64-67
• De Boer, J. M., Y. Yan, J. Bakker, E. L. Davis, and T. J. Baum.  1998.  In situ hybridization to messenger RNA of Heterodera glycines. Journal of Nematology: 30:309-312.
• Davis, E. L., D. M. Meyers, J. W. Burton, and K. R. Barker.  1998.  Resistance to root-knot, reniform, and soybean cyst nematodes in selected soybean breeding lines.  Journal of Nematology 30(4S): 530-541.
• Yan, Y., G. Smant, J. Stokkermans, L. Qin, J. Helder, T. Baum, A. Schots, and E. Davis.  1998. Genominc organization of four ß-1,4-endoglucanase genes in plant-parasitic cyst nematodes and its evolutionary implications.  Gene 220: 61-70.
• Smant, G., J. Stokkermans, Y. Yan, J.M. de Boer, T. Baum, X. Wang, R. S. Hussey, E.L. Davis, F.  J. Gommers, B. Henrissat, J. Helder, A. Schots, and J. Bakker.  1998.  Endogenous cellulases in animals: cloning of expressed ß-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proceedings of the National Academy of Sciences 95: 4906-4911.

Selected Review and Chapters:

• Mitchum, M.G., Hussey, R.S., Baum, T.J., Wang, X., Elling, A.A., Wubben, M., Davis, E.L. 2013. Tansley Review – Nematode effector proteins: an emerging paradigm of parasitism. New Phytologist 199:879-894.
• Mitchum, M.G., X. Wang, J. Wang, and E.L. Davis. 2012.  Role of nematode peptides and other small molecules in plant parasitism. Annual Review of Phytopathology 50:175-195.
• Rosso, M.N., R.S. Hussey, E.L. Davis, G. Smant, T.J. Baum, P. Abad, and M.G. Mitchum. 2012. Nematode effector proteins: Targets and functions in plant parasitism. Pp 329-356 In Martin, F., and S. Kamoun, eds. Effectors in Plant-Microbe Interactions. Wiley-Blackwell, NY.
• Davis, E.L., R.S. Hussey, and Baum, T.J.  2009. Parasitism genes: what they reveal about parasitism. Pp 15-44 In: Berg, R.H. and Taylor, C.G., eds. Plant Cell Monographs: Cell Biology of Plant-Nematode Interactions, Springer, Heidelberg.
• Davis, E.L., R.S. Hussey, M.G. Mitchum, and Baum, T.J.  2008. Parasitism proteins in nematode-plant interactions. Current Opinion in Plant Biology 11:360-366.
• Mitchum, M.G., X. Wang, and E.L. Davis.  2008.  Diverse and conserved roles of CLE peptides. Current Opinion in Plant Biology11(1):75-81.
• Hudson, L.H., C.H. Haigler, and E.L. Davis. 2006. Analysis of cell wall synthesis in feeding cells formed by root-knot nematodes.Pp 281-286 In Sanchez, F., C. Quinto, I.M. Lopez-Lara, O. Geiger, eds., Biology of Plant-Microbe Interactions, Volume 5, ISMPI, St. Paul, MN.
• Davis, E.L., and M.G. Mitchum. 2005.  Nematodes: sophisticated parasites of legumes.  Plant Physiology 137:1182-1188.
• Davis, E.L., R.S. Hussey, and T.J. Baum.  2004.  Getting to the roots of parasitism by nematodes. Trends in Parasitology 20 (3):134-141.
• Davis, E. L., R. S. Hussey, T. J. Baum, J. Bakker, A. Schots, M. N. Rosso, and P. Abad.  2000. Nematode parasitism genes. Annual Review of Phytopathology 38: 365-396.
• Davis, E. L. and A. E. MacGuidwin.  2000.  Lesion nematode disease.  Plant Health Instructor. DOI:10.1094/PHI-I-2000-1030-02.http://www.apsnet.org/edcenter/intropp/lessons/Nematodes/Pages/LesionNem…
• Davis, E. L. and G. L. Tylka.  2000.  Soybean cyst nematode disease.  Plant Health Instructor. DOI:10.1094/PHI-I-2000-0725-01. http://www.apsnet.org/edcenter/intropp/lessons/Nematodes/Pages/SoyCystNe…