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Melissa G. Mitchum

Melissa Mitchum

Professor
Division of Plant Sciences

E-mail: goellnerm at missouri dot edu
Web site: Mitchum Lab
Office address: 371h Bond Life Sciences Center
Office phone: 573-882-6152
Lab address: 315 Bond Life Sciences Center
Lab phone: 573-882-6171

The major focus of research in the Mitchum Lab is the molecular basis of plant-nematode interactions with an emphasis on the interaction between the soybean cyst nematode (SCN; Heterodera glycines) and its host plant, soybean. Sedentary endoparasitic nematodes, such as SCN, are the most economically important group of plant-parasitic nematodes. SCN is consistently the most damaging pest of soybeans grown in Missouri and throughout the US, causing more than 1 billion dollars in crop losses annually.

After penetrating and migrating through soybean root tissue, SCN induces dramatic modifications of selected cells near the vasculature of the root to form an elaborate feeding cell (called a syncytium). Growth and development of the nematode is completely dependent on the formation of the syncytium from which it derives nutrients to complete its life cycle. We are studying the signal exchange that occurs between the nematode and its host for the formation of feeding cells. In addition to soybean, the Arabidopsis-beet cyst nematode pathosystem is used as a model system to dissect the mechanisms of pathogenesis and feeding cell formation. The aim of this research is to advance our understanding of the molecular basis of pathogenicity and host resistance to cyst nematodes with the long term goal of developing improved disease resistance strategies.

Research Areas

Host Plant Responses During Compatible and Incompatible Plant-Nematode Interactions

nematode

Nematodes induce multifaceted changes in plant cellular metabolism and gene expression during the infection process that ultimately gives rise to specialized feeding cells (syncytia) within host plant roots. The underlying molecular mechanisms controlling these processes remain largely unknown. We have used laser capture microdissection (LCM) to specifically isolate mRNA of nematode-induced feeding cells over a time-course of their development in soybean roots infected with SCN and coupled this with microarray analysis to develop the most comprehensive profile of syncytia-expressed genes to date. We are currently characterizing the function of genes up and down regulated in developing syncytia to assess for direct roles in syncytium induction, development and maintenance. This approach may also prove successful in identifying host targets for engineered resistance.

Little is known regarding the molecular mechanisms of soybean resistance to SCN. In resistant soybean, feeding cells degenerate and nematode development is impeded. We have been collaborating with the lab of Dr. Khalid Meksem (SIU) to confirm the identity and function of resistance genes underlying major SCN resistance QTL. We recently determined the soybean Rhg4 gene encodes a serine hydroxymethyltransferase, which points to a new mechanism of plant resistance to pathogens. We are currently using functional genomic, genetic, and biochemical approaches to elucidate the mechanism of resistance. We have also coupled LCM with microarray analysis to directly compare gene expression profiles in developing syncytia of resistant and susceptible soybean to identify components of the soybean resistance response to SCN. At present, we are characterizing the function of these genes to determine their role in resistance.

Identification and Functional Analysis of Nematode Effector Proteins

With regard to the nematode, we have been focusing on the identification and functional analysis of nematode parasitism genes expressed in the esophageal gland cells that code for stylet-secreted effector proteins, as part of a Molecular Nematology collaboration with the labs of Drs. Eric Davis (NCSU), Dick Hussey (UGA), Thomas Baum (ISU), and Xiaohong Wang (Cornell). Our group is interested in elucidating the underlying mechanisms of cyst nematode parasitism, in particular how cyst nematodes utilize effector proteins to modify plant cells during the formation of a complex feeding site (syncytium) within the host root.

nematode

Stylet-secreted effectors are key molecules involved in initiating the interaction and modifying plant cells for parasitism. Notable progress has been made to determine the identity of stylet-secreted effectors involved in establishing the parasitic interaction. Previously, nematode esophageal gland cell-specific cDNA libraries were constructed from microaspirated gland cell mRNA, sequenced, and subjected to bioinformatics analysis. We are conducting functional analyses of several effector proteins to determine their role in plant parasitism. Approaches include RNA interference, ectopic expression in plants, and protein-protein interaction studies. Of particular focus is a class of parasitism genes encoding secreted CLAVATA3/ESR-like (CLE) peptides. These are the first CLE genes identified outside the plant kingdom. In plants, CLE peptides serve as ligands for receptors to mediate plant signaling regulating the balance between stem cell proliferation and differentiation. We are currently conducting detailed functional studies to assess the role of peptide hormone mimicry in nematode parasitism. We are also investigating differences in effector proteins among SCN populations differing in virulence on resistant soybean to elucidate a potential role for these proteins in eliciting, suppressing or evading host plant resistance mechanisms.

The Role of Phytohormones in Plant-Nematode Interactions

nematode feeding cell

Phytohormones have been known for decades to modulate plant development and we continue to make progress in our understanding of the molecular mechanisms controlling these processes. Considerable interplay among various phytohormones for the modulation of plant growth has been identified. Several lines of evidence have shown that local phytohormone levels and hormone response pathways are altered in nematode-infected roots and play a significant role in nematode feeding cell formation. Phytohormone imbalances induced by nematodes likely result in altered expression of cell wall modifying enzymes with a central role in the controlled cell wall architechural modifications observed during feeding cell development, and may play a variety of other roles. Hormone-responsive plant gene promoters have been shown to be upregulated in feeding cells and both auxin and ethylene-insensitive mutants are less susceptible to cyst nematodes due to impairments in feeding cell development. It remains to be determined whether the nematode secretes phytohormone mimics into plant cells, and/or modulates the level of host phytohormone levels by affecting transport or redirecting normal plant biosynthetic and signaling pathways. We are using the model plant, Arabidopsis thaliana, to dissect the role of phytohormones during plant-nematode interactions. We recently identified a nematode stylet-secreted effector that interacts with the auxin influx transporter LAX3, suggesting that nematodes use their effectors to directly regulate aspects of phytohormone transport to form feeding cells. Several ongoing projects are directed at determining how nematodes alter phytohormone biosynthetic and signaling networks for the development of nematode feeding cells in plant roots.

 

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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.

Kandoth PK and Mitchum MG. War of the worms: how plants fight underground attacks. Current Opinion in Plant Biology 2013;16: 457-463.

Kandoth P, Heinz R, Yeckel G, Gross NW, Juvale PS, Hill J, Whitham SA, Baum TJ, Mitchum MG.  A virus-induced gene silencing method to study soybean cyst nematode parasitism in Glycine max. BMC Research Notes 2013;6:255.

Replogle A, Wang J, Paolillo V, Smeda J, Kinoshita A, Durbak A, Tax FE, Wang X, Sawa S, and Mitchum MG. Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis. Molecular Plant-Microbe Interactions 2013;26(1):87-96.

*Liu S, *Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, †Mitchum MG, and †Meksem K. A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 2012;492:256-260. doi:10.1038/nature11651. *†equal contributors

Mitchum MG, Wang X, Wang J, and Davis EL. The role of peptides and other small molecules in nematode parasitism. Annual Review of Phytopathology 2012; 50:175-195.

Juvale PS, Hewezi T, Zhang C, Kandoth PK, Mitchum MG, Hill JH, Whitham SA, and Baum TJ. Temporal and spatial Bean pod mottle virus-induced gene silencing in soybean. Molecular Plant Pathology 2012;13(9):1140-1148.

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.

Gheysen G and Mitchum MG. How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology 2011;14:1-7.

*Kandoth PK, *Ithal N, Recknor J, Maier T, Nettleton D, Baum TJ, and Mitchum MG. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiology 2011;155:1960-1975. *equal contributors

*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.*equal contributors

Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ, Shinichiro S, Davis EL, Wang X, Simon R, and Mitchum MG. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant Journal 2011;65(3):430-440.

Wang J, Replogle A, Hussey R, Baum T, Wang X, Davis EL, and Mitchum MG. Identification of potential host plant mimics of CLV3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtiiMolecular Plant Pathology 2011;12(2):177-186.

*Liu X, *Liu S, Jamai A, Bendahmane A, Lightfoot D, Mitchum MG and Meksem K. Soybean cyst nematode resistance in soybean is independent of the Rhg4 locus LRR-RLK gene. Functional and Integrative Genomics 2011;11(4):539-549. *equal contributors

*Brown S, *Yeckel G, *Heinz R, Clark K, Sleper D, and Mitchum MG. A high-throughput automated technique for counting females of Heterodera glycines using a fluorescence-based imaging system. Journal of Nematology 2010;42(3):201-206. *equal contributors

Wang J, Joshi S, Korkin D, and Mitchum MG. Variable domain I of nematode CLEs directs post-translational targeting of CLE peptides to the extracellular space. Plant Signaling and Behavior 2010;5(12):1-3.

Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey R, Baum TJ, Davis EL, Wang X and Mitchum MG. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytologist 2010;187(4):1003-1017.

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.

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 schachtiiPlant Physiology 2010;152(2):968-984.

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.

Lu SW, Chen S, Wang J, Yu H, Chronis D, Mitchum MG and Wang X. Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Molecular Plant-Microbe Interactions 2009;22(9):1128-1142.

Mitchum MG, Wang X and Davis EL. Diverse and conserved roles of CLE peptides. Current Opinion in Plant Biology 2008;11(1):75-81.

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.

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.

*Hu J, *Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai WC, Hanada A, Alonso JM, Ecker JR, Swain SM, Yamaguchi S, Kamiya Y and Sun TP. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 2008;20(2):320-336.*equal contributors

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. Plant Cell 2008;20(11):3080-3093.

Wang X, Replogle A, Davis EL and Mitchum MG. The tobacco Cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Molecular Plant Pathology 2007;8(4):423-436.

Mitchum MG, Wrather JA, Heinz RD, Shannon JG and Danekas G. Variability in distribution and virulence phenotypes of Heterodera glycines in Missouri during 2005. Plant Disease 2007;91(11):1473-1476.

Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ and Mitchum MG. Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Molecular Plant-Microbe Interactions 2007;20(5):510-525.

Ithal N, Recknor J, Nettleton D, Hearne L, Maier T, Baum TJ and Mitchum MG. Parallel genome-wide expression profiling of host and pathogen during soybean cyst nematode infection of soybean. Molecular Plant-Microbe Interactions 2007;20(3):293-305.

*Mitchum MG, *Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y and Sun TP. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant Journal 2006;45(5):804-818. *equal contributors

Wang X, Mitchum MG, Gao B, Li C, Diab H, Baum TJ, Hussey RS and Davis EL. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Molecular Plant Pathology 2005;6(2):187-191.

Davis EL and Mitchum MG. Nematodes. Sophisticated parasites of legumes. Plant Physiology 2005;137(4):1182-1188.

Mitchum MG, Sukno S, Wang X, Shani Z, Tsabary G, Shoseyov O and Davis EL. The promoter of the Arabidopsis thaliana Cel1 endo-1,4-beta glucanase gene is differentially expressed in plant feeding cells induced by root-knot and cyst nematodes. Molecular Plant Pathology 2004;5(3):175-181.

Goellner M, Wang X, and Davis EL. Endo-β-1,4-glucanase expression in compatible plant-nematode interactions. The Plant Cell 2001; 13:2241-2255.

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.

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.

 

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  • Recipient of the Syngeta Award, American Phytopathological Society (2015)
  • Outstanding Senior Teacher, Universty of Missouri College of Agriculture, Food and Natural Resrouces (2014)