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Nematode Effector Biology

Nematodes use a hollow mouth spear called a stylet to mechanically penetrate into the roots of host plants while simultaneously secreting effectors (i.e., pathogen proteins that alter host-cell structure and function) to facilitate their migration through root tissues. Once the infective juvenile nematode reaches the root vasculature, it selects a single cell and injects a cocktail of effectors that hijack cellular processes and transform it into a specialized feeding site.

A major focus of research in my lab has been directed at the functional characterization of nematode effector proteins using molecular, genetic, and biochemical approaches, including RNA interference (RNAi), ectopic expression in plants, and protein-protein interaction studies. Our efforts have led to the identification of several host protein targets of nematode effectors to shed light on their functions in parasitism. We hope our discoveries not only provide new insights into how plants recognize and respond to effector proteins secreted by nematodes to form essential feeding sites within host roots, but in turn, can ultimately be exploited to develop novel strategies to bioengineer crops with robust resistance to these parasites.

Current work is focused on characterizing the function of novel classes of effectors found to be highly expanded in cyst nematode genomes. We have also recently coupled computational approaches with transcriptome datasets to uncover a novel set of nuclear-targeted effectors with potential roles in manipulating gene regulation and other host nuclear functions.

Related Publications:

Masonbrink R, Maier TR, Muppirala U, Seetharam AS, Lord E, Juvale PS, Schmutz J, Johnson NT, Korkin D, Mitchum MG, Mimee B, Eves-vn den Akker S, Hudson M, Severin AJ, Baum TJ. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC Genomics 2019; 20:119. https://doi.org/10.1186/s12864-019-5485-8

Jones J, and Mitchum MG. Biology of effectors. Chapter 4 IN: R.N. Perry, M. Moens and J.T. Jones (Eds.) Cyst Nematodes CABI International; 2018, pp. 74-83. https://www.cabi.org/bookshop/book/9781786390837

Barnes SN, Wram CL, Mitchum MG, Baum TJ. The plant-parasitic cyst nematode effector GLAND4 is a DNA-binding protein. Molecular Plant Pathology 2018; 19:2263-2276. https://doi.org/10.1111/mpp.12697

Verma A, Lee C, Morriss S, Odu F, Kenning C, Rizzo N, Spollen WG, Lin M, McRae A, Givan SA, Hewezi T, Hussey R, Davis EL, Baum TJ, Mitchum MG. The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites. New Phytologist 2018; 219:697-713. https://doi.org/10.1111/nph.15179

Gardner M, Dhroso A, Johnson N, Davis EL, Baum TJ, Korkin D, Mitchum, MG. Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode Heterodera glycines. Scientific Reports 2018; 8:2505. https://doi.org/10.1038/s41598-018-20536-5

Noon J, Mingsheng Q, Sill D, Muppirala U, Eves-van den Akker S, Maier T, Dobbs D, Mitchum MG, Hewezi T, Baum TJ. A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. New Phytologist 2016; 212:444-460. https://doi.org/10.1111/nph.14047

Gardner M, Verma A, and Mitchum MG. Emerging roles of cyst nematode effectors in exploiting plant cellular processes. Chapter 11, In C. Escobar, & C. Fenoll (Eds.), Advances in Botanical Research Vol 73, Plant Nematode Interactions: A View on Compatible Interrelationships (pp. 259–291), Oxford: Elsevier, 2015 https://doi.org/10.1016/bs.abr.2014.12.009

Pogorelko G, Juvale PS, Rutter WB, Hewezi T, Hussey R, Davis EL, Mitchum MG, Baum TJ. A cyst nematode effector binds to diverse plant proteins, increases nematode susceptibility and affects root morphology. Molecular Plant Pathology 2015;17(6):832-44. https://doi.org/10.1111/mpp.12330

Noon JB, Hewezi T, Maier TR, Simmons C, Wei J-Z, Wu G, Llaca V, Deschamps S, Davis EL, Mitchum MG, Hussey RS, Baum TJ. Eighteen new candidate effectors of the phytonematode Heterodera glycines produced specifically in the secretory esophageal gland cells during parasitism. Phytopathology 2015;105(10):1362-72. https://doi.org/10.1094/PHYTO-02-15-0049-R

Hewezi T, Juvale P, Piya S, Maier TR, Rambani A, Hollis Rice J, Mitchum MG, Davis EL, Hussey RS, Baum TJ. The novel cyst nematode effector protein 10A07 targets and recruits host post-translational machinery to mediate its nuclear trafficking and promote parasitism. The Plant Cell 2015;27(3):891-907 https://doi.org/10.1105/tpc.114.135327

Mitchum MG, Hussey RS, Davis EL, Baum TJ, Wang X, Elling AA, Wubbin M. Nematode effector proteins: an emerging paradigm of parasitism. Tansley Review, New Phytologist 2013;199: 879–894. https://doi.org/10.1111/nph.12323

Hogenhout S, Mitchum MG, Smant G. Focus on molecular plant-nematode and plant-insect interactions. Molecular Plant Microbe Interactions 2013;26(1):8. https://doi.org/10.1094/MPMI-26-01-0008

Hamamouch N, Li C, Hewezi T, Baum TJ, Mitchum MG, Hussey RS, Vodkin LO, and Davis EL. 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 2012;63(10):3683-3696. https://dx.doi.org/10.1093%2Fjxb%2Fers058

Rosso M-N, Hussey RS, Davis EL, Smant G, Baum TJ, Abad P, and Mitchum MG. Nematode effector proteins: targets and functions in plant parasitism. Chapter 13 IN: F Martin and S Kamoun (Eds.) Effectors in Plant-Microbe Interactions (pp. 327-354) Weinheim: Wiley-Blackwell, 2011. https://doi.org/10.1002/9781119949138.ch13

Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey RS, Bennett M and Mitchum MG. The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiology 2011;155:866-880.*co-first authors https://doi.org/10.1104/pp.110.167197

Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, Baum TJ, Mitchum MG and Davis EL. A nematode effector protein similar to annexins in host plants. Journal of Experimental Botany 2010;61(1):235-248. https://doi.org/10.1093/jxb/erp293

Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL and Baum TJ. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiology 2010;152(2):968-984. https://doi.org/10.1104/pp.109.150557

Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL and Baum TJ. Effective and specific in planta RNAi in cyst nematodes: Expression interference of four parasitism genes reduces parasitic success. Journal of Experimental Botany 2009;60(1):315-324. https://doi.org/10.1093/jxb/ern289

Davis EL, Hussey RS, Mitchum MG and Baum TJ. Parasitism proteins in nematode-plant interactions. Current Opinion in Plant Biology 2008;11(4):360-366. https://doi.org/10.1016/j.pbi.2008.04.003

Patel N, Hamamouch N, Li C, Hussey R, Mitchum M, Baum T, Wang X and Davis EL. Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. Journal of Nematology 2008;40(4):299-310.

Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL and Baum TJ. Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: Cooperative cell wall modification during parasitism. The Plant Cell 2008;20(11):3080-3093. https://doi.org/10.1105/tpc.108.063065

Mitchum MG, Hussey RS, Davis EL, and Baum TJ. Application of biotechnology to understand pathogenesis of nematode plant pathogens. IN: ZK Punja, S DeBoer, and H Sanfacon (Eds.), Biotechnology and Plant Disease Management (pp. 58-86). Cambridge, MA: Cabi Pub, 2007. http://dx.doi.org/10.1079/9781845932886.0058

Davis EL and Mitchum MG. Nematodes. Sophisticated parasites of legumes. Plant Physiology 2005;137(4):1182-1188. https://dx.doi.org/10.1104%2Fpp.104.054973

Wang X, Allen R, Ding X, Goellner M, Maier T, De Boer J, Baum T, Hussey R, and Davis EL. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Molecular Plant-Microbe Interactions 2001; 14:536-544. https://doi.org/10.1094/MPMI.2001.14.4.536

Goellner M, Smant G, De Boer JM, Baum TJ, and Davis EL. Isolation of β-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. Journal of Nematology 2000; 32(2):154-165. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2620441/