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Transcriptomic Analysis of Male Black Tiger Shrimp (Penaeus monodon) After Polychaete Feeding to Enhance Testicular Maturation

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Abstract

To reveal molecular mechanism of how polychaetes enhanced reproductive maturation in the male black tiger shrimp (Penaeus monodon), transcriptomic profiles of male reproductive organs (testes and vas deferens) between polychaete-fed and commercial pellet-fed male brooders were compared using cDNA microarray. The overall profiles were distinguishingly different between the two feed groups as well as between testes and vas deferens. Additionally, six of 11 differentially expressed gene identified by the microarray (HNRPUL1 and GCP4 in testes, MAT2B, CDC16, and CSN5 in vas deferens, and SLD5 in both organs) were validated by quantitative real-time PCR (qPCR) and found to exhibit significantly higher expression levels in polychaete-fed shrimp than those in commercial pellet-fed shrimp. From microarray and qPCR results, the differentially expressed transcripts in both testes and vas deferens between different feeds belonged to DNA replication and microtubule nucleation pathways. Interestingly, while the transcripts involved in nutrient uptake and nucleotide biosynthesis were increased only in testes, those involved in protein refolding and apoptosis were increased only in vas deferens. These findings suggest that polychaetes may enhance spermatogenesis by increasing spermatogonia proliferation in testes and by regulating mature spermatozoa in vas deferens.

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Acknowledgements

The financial support for this work was from Cluster and Program Management Office (CPM), National Science and Technology Development Agency (Thailand), under the grant number P-10-10467 and Thailand Research Fund under the grant number TRG5780018. We would like to express our gratitude to Mr. Bunjonk Nissapawanich at Bunjonk farm (Chachoengsao, Thailand) for facility to conduct feed experiment and invaluable advice and Mr. Chaiwat Bhutthong, Mr. Kwanchai Kachanethong, Mr. Yutthana Oatngam, Mr. Krisada Sukjarern, and Mr. Kaitisak Jonetep at the Shrimp Genetic Improvement Center (SGIC, Thailand) for providing technical help in this experiment. We are also grateful to Prof. Dr. Morakot Tanticharoen and Dr. Kanyawim Kirtikara for their mentorship in the black tiger shrimp research program.

Authors’ Contributions

RL and NK conceived the work. RL, UU, AK, JK, SP, SW, and NK conducted experiments. UU and NK constructed cDNA microarray chips. RL, UU, AK, and NK carried out microarray experiment and data analysis. RL performed gene expression analysis. RL, UU, and NK wrote the manuscript. All authors read and approved this manuscript.

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Authors and Affiliations

  1. Microarray Laboratory, National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency, Khlong Luang, Pathum Thani, Thailand

    Rungnapa Leelatanawit, Umaporn Uawisetwathana, Amornpan Klanchui & Nitsara Karoonuthaisiri

  2. Shrimp Genetic Improvement Center (SGIC), National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency, Surat Thani, Thailand

    Jutatip Khudet, Suwanchai Phomklad & Somjai Wongtriphop

  3. Aquatic Molecular Genetics and Biotechnology Laboratory, National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency, Khlong Luang, Pathum Thani, Thailand

    Pikul Jiravanichpaisal

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  1. Rungnapa Leelatanawit
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  2. Umaporn Uawisetwathana
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Correspondence to Rungnapa Leelatanawit.

Electronic supplementary material

Supplementary Fig. S1

Distribution of the three principles Gene Ontology (GO) categories of all features of UniShrimpChips (a), and differentially expressed transcripts of testes (b) and vas deferens (c) between the two feed groups. (GIF 118 kb)

High Resolution Image (TIFF 413 kb)

Supplementary Fig. S2

Comparison of the up- and down-regulated transcripts of testes and vas deferens between feed groups at the second level of three Gene Ontology (GO) categories: biological processes (a), molecular functions (b), and cellular components (c). (GIF 103 kb)

High Resolution Image (TIFF 1048 kb)

Supplementary Table S1

Second level gene ontology (GO) categories and number of differentially expressed genes in testes (TT) and vas deferens (VD). (DOCX 18 kb)

Supplementary Table S2

Lists of genes significant change between shrimp fed with fresh polychaetes and shrimp fed with commercial pellet analyzed by Significance Analysis of Microarrays (SAM). (DOCX 39 kb)

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Leelatanawit, R., Uawisetwathana, U., Klanchui, A. et al. Transcriptomic Analysis of Male Black Tiger Shrimp (Penaeus monodon) After Polychaete Feeding to Enhance Testicular Maturation. Mar Biotechnol 19, 125–135 (2017). https://doi.org/10.1007/s10126-017-9738-8

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