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Gene expression changes elicited by a parasitic B chromosome in the grasshopper Eyprepocnemis plorans are consistent with its phenotypic effects

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Abstract

Parasitism evokes adaptive physiological changes in the host, many of which take place through gene expression changes. This response can be more or less local, depending on the organ or tissue affected by the parasite, or else systemic when the parasite affects the entire host body. The most extreme of the latter cases is intragenomic parasitism, where the parasite is present in all host nuclei as any other genomic element. Here, we show the molecular crosstalk between a parasitic chromosome (also named B chromosome) and the host genome, manifested through gene expression changes. The transcriptome analysis of 0B and 1B females of the grasshopper Eyprepocnemis plorans, validated by a microarray experiment performed on four B-lacking and five B-carrying females, revealed changes in gene expression for 188 unigenes being consistent in both experiments. Once discarded B-derived transcripts, there were 46 differentially expressed genes (30 up- and 16 downregulated) related with the adaptation of the host genome to the presence of the parasitic chromosome. Interestingly, the functions of these genes could explain some of the most important effects of B chromosomes, such as nucleotypic effects derived from the additional DNA they represent, chemical defense and detoxification, protein modification and response to stress, ovary function, and regulation of gene expression. Collectively, these changes uncover an intimate host-parasite interaction between A and B chromosomes during crucial steps of gene expression and protein function.

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Acknowledgments

We thank Rubén Martín-Blázquez and Mohammed Bakkali for their collaboration on the Illumina transcriptome reads sequencing and first assembly, Marco Pellino for his help on the microarray hybridization step, and Álvaro Enciso for informatics support.

Funding

This study was funded by the Spanish Ministerio de Economía y Competitividad (CGL2015-70750-P) and was partially performed by FEDER funds. Navarro-Domínguez was supported by a FPI fellowship from the Spanish Ministerio de Ciencia e Innovación (BES-2010-030016).

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Correspondence to Juan Pedro M. Camacho.

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All experiments comply with the current Spanish laws.

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The authors declare that they have no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Navarro-Domínguez, B., Martín-Peciña, M., Ruiz-Ruano, F.J. et al. Gene expression changes elicited by a parasitic B chromosome in the grasshopper Eyprepocnemis plorans are consistent with its phenotypic effects. Chromosoma 128, 53–67 (2019). https://doi.org/10.1007/s00412-018-00689-y

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  • DOI: https://doi.org/10.1007/s00412-018-00689-y

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