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Gene expression analysis distinguishes tissue-specific and gender-related functions among adult Ascaris suum tissues

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Abstract

Over a billion people are infected by Ascaris spp. intestinal parasites. To clarify functional differences among tissues of adult A. suum, we compared gene expression by various tissues of these worms by expression microarray methods. The A. suum genome was sequenced and assembled to allow generation of microarray elements. Expression of over 40,000 60-mer elements was investigated in a variety of tissues from both male and female adult worms. Nearly 50 percent of the elements for which signal was detected exhibited differential expression among different tissues. The unique profile of transcripts identified for each tissue clarified functional distinctions among tissues, such as chitin binding in the ovary and peptidase activity in the intestines. Interestingly, hundreds of gender-specific elements were characterized in multiple non-reproductive tissues of female or male worms, with most prominence of gender differences in intestinal tissue. A. suum genes from the same family were frequently expressed differently among tissues. Transcript abundance for genes specific to A. suum, by comparison to Caenorhabditis elegans, varied to a greater extent among tissues than for genes conserved between A. suum and C. elegans. Analysis using C. elegans protein interaction data identified functional modules conserved between these two nematodes, resulting in identification of functional predictions of essential subnetworks of protein interactions and how these networks may vary among nematode tissues. A notable finding was very high module similarity between adult reproductive tissues and intestine. Our results provide the most comprehensive assessment of gene expression among tissues of a parasitic nematode to date.

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Acknowledgments

The analysis presented in this study was supported by NIH/NAIAD and NIH/NIGMS grants to M.M. We thank the Washington University microarray core Dr. Seth Crosby and Michael Heinz for their service and technical assistance and Dr. Richard Komuniecki for providing the A. suum tissues.

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  1. Yong Yin

    Present address: Monsanto Company, St. Louis, MO, 63167, USA

Authors and Affiliations

  1. The Genome Institute, Washington University School of Medicine, St. Louis, MO, 63108, USA

    Zhengyuan Wang, Xin Gao, John Martin, Yong Yin, Sahar Abubucker, Bill Nash, Kym Hallsworth-Pepin & Makedonka Mitreva

  2. Department of Internal Medicine, Washington University School of Medicine, St. Louis, MO, 63110, USA

    Amy C. Rash, Ben-Wen Li & Makedonka Mitreva

  3. Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA, 99164, USA

    Douglas P. Jasmer

  4. Department of Genetics, Washington University School of Medicine, St. Louis, MO, 63108, USA

    Makedonka Mitreva

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Correspondence to Makedonka Mitreva.

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Communicated by S. Hekimi.

Z. Wang and X. Gao contributed equally.

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438_2013_743_MOESM1_ESM.tif

Supplementary material 1 Fig. S1 Top scored active modules identified from (a) adult male A. suum tissues only or (b) adult female A. suum tissues only. Rows represent the identified active modules and columns represent the individual tissues (Hea, head; Int, intestine; Pha, pharynx; Ova, ovary; SemVes, seminal vesicle; Ute, uterus; Tes, testis). Each black filled area indicates the existence of an active module in a specific tissue. Modules are sorted according to the descending z scores (TIFF 83 kb)

438_2013_743_MOESM2_ESM.tif

Supplementary material 2 Fig. S2 Examples of the active modules common to the adult male A. suum tissues only that are centered at gene gei-4. Node indicates the protein members in the active module. Edge indicates the interaction between protein members. Conserved protein members between A. suum and C. elegans are highlighted by grey color. Interaction files for modules a, b and c are available at www.nematode.net (http://nematode.net/Ascaris_suum.html) (TIFF 313 kb)

438_2013_743_MOESM3_ESM.tif

Supplementary material 3 Fig. S3 Examples of the active modules common to the adult female A. suum tissues only that are centered at gene pgn-4. Node indicates the protein members in the active module. Edge indicates the interaction between protein members. Conserved protein members between A. suum and C. elegans are highlighted by grey color. Interaction files for modules a, b and c are available at www.nematode.net (http://nematode.net/Ascaris_suum.html) (TIFF 415 kb)

438_2013_743_MOESM4_ESM.tiff

Supplementary material 4 Fig. S4. Heatmap showing expression data for the 214 nucleotide sequence contigs that collectively formed 95 different A. suum intestinal gene families (Yin et al. 2008) found to be differentially expressed among the ten tissues investigated. Rows represent genes and columns represent different tissues. The gradation from green (highest similarity) to red (lowest similarity) depicts distance in relation to individual contigs and overall expression profiles among tissues. FemPha, female pharynx; MalPha, male pharynx; FemHea, female head; MalHea, male head; FemInt, female intestine; MalInt, male intestine; SemVes, seminal vesicle; Tes, testis; Ova, ovary; Ute, uterus (TIFF 1521 kb)

Supplementary material 5 Table S1 Primer sequences for qRT-PCR (XLS 32 kb)

Supplementary material 6 Table S2 Coefficients of microarray elements and the functional annotation (TXT 10893 kb)

438_2013_743_MOESM7_ESM.xls

Supplementary material 7 Table S3 qPCR validation of selected genes that showed the highest level of expression differences in microarray assays (XLS 21 kb)

Supplementary material 8 Table S4 Interpro annotations of top 20 tissues specific expressed genes (XLS 47 kb)

Supplementary material 9 Table S5 IDs of family members expressed significantly differently (XLS 2567 kb)

Supplementary material 10 Table S6 GO associations of A. suum elements represented on the microarray (XLS 99 kb)

438_2013_743_MOESM11_ESM.xls

Supplementary material 11 Table S7 Example genes that directly interact with gei-4 that are not included in Table 6 and display differential expression across adult A. suum tissues (XLS 29 kb)

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Wang, Z., Gao, X., Martin, J. et al. Gene expression analysis distinguishes tissue-specific and gender-related functions among adult Ascaris suum tissues. Mol Genet Genomics 288, 243–260 (2013). https://doi.org/10.1007/s00438-013-0743-y

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