Sequence Mining and Transcript Profiling to Explore Cyst Nematode Parasitism Axel A

Washington University School of Medicine Digital Commons@Becker Open Access Publications 2009 Sequence mining and transcript profiling to explore cyst nematode parasitism Axel A. Elling Iowa State University Makedonka Mitreva Washington University School of Medicine in St. Louis Xiaowu Gai Children's Hospital of Philadelphia John Martin Washington University School of Medicine in St. Louis Justin Recknor Iowa State University See next page for additional authors Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Part of the Medicine and Health Sciences Commons Recommended Citation Elling, Axel A.; Mitreva, Makedonka; Gai, Xiaowu; Martin, John; Recknor, Justin; Davis, Eric L.; Hussey, Richard S.; Nettleton, Dan; McCarter, James P.; and Baum, Thomas J., ,"Sequence mining and transcript profiling to explore cyst nematode parasitism." BMC Genomics.,. 58. (2009). https://digitalcommons.wustl.edu/open_access_pubs/324 This Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in Open Access Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact [email protected]. Authors Axel A. Elling, Makedonka Mitreva, Xiaowu Gai, John Martin, Justin Recknor, Eric L. Davis, Richard S. Hussey, Dan Nettleton, James P. McCarter, and Thomas J. Baum This open access publication is available at Digital Commons@Becker: https://digitalcommons.wustl.edu/open_access_pubs/324 BMC Genomics BioMed Central Research article Open Access Sequence mining and transcript profiling to explore cyst nematode parasitism Axel A Elling1,2,3, Makedonka Mitreva4, Xiaowu Gai5, John Martin4, Justin Recknor6,7, Eric L Davis8, Richard S Hussey9, Dan Nettleton6, James P McCarter4,10 and Thomas J Baum*1,2 Address: 1Interdepartmental Genetics Program, Iowa State University, Ames, IA 50011, USA, 2Department of Plant Pathology, Iowa State University, Ames, IA 50011, USA, 3Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520, USA, 4Genome Sequencing Center, Department of Genetics, Washington University School of Medicine, St. Louis, MO 63108, USA, 5Center for Biomedical Informatics, The Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA, 6Department of Statistics, Iowa State University, Ames, IA 50011, USA, 7Eli Lilly and Company, Lilly Research Laboratories, Greenfield, IN 46140, USA, 8Department of Plant Pathology, North Carolina State University, Raleigh, NC 27695, USA, 9Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA and 10Divergence Inc., St. Louis, MO 63141, USA Email: Axel A Elling - [email protected]; Makedonka Mitreva - [email protected]; Xiaowu Gai - [email protected]; John Martin - [email protected]; Justin Recknor - [email protected]; Eric L Davis - [email protected]; Richard S Hussey - [email protected]; Dan Nettleton - [email protected]; James P McCarter - [email protected]; Thomas J Baum* - [email protected] * Corresponding author Published: 30 January 2009 Received: 2 August 2008 Accepted: 30 January 2009 BMC Genomics 2009, 10:58 doi:10.1186/1471-2164-10-58 This article is available from: http://www.biomedcentral.com/1471-2164/10/58 © 2009 Elling et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Cyst nematodes are devastating plant parasites that become sedentary within plant roots and induce the transformation of normal plant cells into elaborate feeding cells with the help of secreted effectors, the parasitism proteins. These proteins are the translation products of parasitism genes and are secreted molecular tools that allow cyst nematodes to infect plants. Results: We present here the expression patterns of all previously described parasitism genes of the soybean cyst nematode, Heterodera glycines, in all major life stages except the adult male. These insights were gained by analyzing our gene expression dataset from experiments using the Affymetrix Soybean Genome Array GeneChip, which contains probeset sequences for 6,860 genes derived from preparasitic and parasitic H. glycines life stages. Targeting the identification of additional H. glycines parasitism-associated genes, we isolated 633 genes encoding secretory proteins using algorithms to predict secretory signal peptides. Furthermore, because some of the known H. glycines parasitism proteins have strongest similarity to proteins of plants and microbes, we searched for predicted protein sequences that showed their highest similarities to plant or microbial proteins and identified 156 H. glycines genes, some of which also contained a signal peptide. Analyses of the expression profiles of these genes allowed the formulation of hypotheses about potential roles in parasitism. This is the first study combining sequence analyses of a substantial EST dataset with microarray expression data of all major life stages (except adult males) for the identification and characterization of putative parasitism-associated proteins in any parasitic nematode. Page 1 of 17 (page number not for citation purposes) BMC Genomics 2009, 10:58 http://www.biomedcentral.com/1471-2164/10/58 Conclusion: We have established an expression atlas for all known H. glycines parasitism genes. Furthermore, in an effort to identify additional H. glycines genes with putative functions in parasitism, we have reduced the currently known 6,860 H. glycines genes to a pool of 788 most promising candidate genes (including known parasitism genes) and documented their expression profiles. Using our approach to pre-select genes likely involved in parasitism now allows detailed functional analyses in a manner not feasible for larger numbers of genes. The generation of the candidate pool described here is an important enabling advance because it will significantly facilitate the unraveling of fascinating plant-animal interactions and deliver knowledge that can be transferred to other pathogen-host systems. Ultimately, the exploration of true parasitism genes verified from the gene pool delineated here will identify weaknesses in the nematode life cycle that can be exploited by novel anti-nematode efforts. Background enzymes like beta-1,4-endoglucanase [9,10], pectate lyase Heterodera glycines, the soybean cyst nematode, is a devas- [11,12], a putative arabinogalactan endo-1,4-beta-galac- tating pathogen of soybean production. Upon hatching as tosidase [13] and an expansin [14] as members of the par- second-stage juveniles (J2), these nematodes migrate asitome. Apart from genes related to cell wall through the soil as infective J2, invade roots of soybean modifications, other genes whose products likely alter the plants to become parasitic J2, and move intracellulary normal host cell physiology to establish and maintain a through the root tissue until they reach the vicinity of the syncytium belong to the parasitome, e.g., chorismate vascular system, where they become sedentary and induce mutases [15,16], ubiquitin extension proteins [16,17], as the formation of a feeding site, the syncytium [1-3]. H. gly- well as S phase kinetochore-associated protein 1 (SKP1) cines completely depends on syncytia for nutrition. Fol- and RING-like proteins [16]. While a few more parasitism lowing the development through two more juvenile stages proteins have similarity to known proteins, like the (J3, J4), the nematodes reach adulthood. While adult venom allergen-like proteins [18] or a chitinase [19], for females remain sedentary, adult males regain motility and most H. glycines parasitism proteins no clear function can leave the root to fertilize females, whose posterior bodies be ascribed [16], although it has been shown that some have broken out of the root into the rhizosphere during are imported into plant cell nuclei [20]. To date, more the course of growth and development. Ultimately, the than sixty parasitism genes have been identified in H. gly- females die and their body walls harden to protect the cines. Most likely, however, the H. glycines parasitome is eggs, which are mostly retained in utero, until the environ- even larger. Furthermore, there may be proteins produced ment is favorable again for a new generation of nema- in organs/tissues other than the esophageal glands or pro- todes to hatch [1,4]. teins released by means other than the signal peptide- dependent secretory pathway that play critical roles in Secreted proteins are key molecular interfaces between mediating cyst nematode parasitism. While secretory parasite and host and enable H. glycines to infect soybean parasitism proteins that are released into plant host tissue plants, which results in an estimated annual damage of are key factors to understand host-parasite interactions, $800 million to soybean production in the USA alone [5]. many secretory proteins exist that do not leave the body of More specifically, secretory proteins that are produced in the nematode. These secretory proteins are involved in a three large esophageal gland cells (one dorsal and two vast array of non-parasitic signaling events within the subventral) and that are injected into host plant cells nematode and can be found for example in the extracellu- through the

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