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Multiple Alr genes exhibit allorecognition-associated variation in the colonial cnidarian Hydractinia

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Abstract

The genetics of allorecognition has been studied extensively in inbred lines of Hydractinia symbiolongicarpus, in which genetic control is attributed mainly to the highly polymorphic loci allorecognition 1 (Alr1) and allorecognition 2 (Alr2), located within the Allorecognition Complex (ARC). While allelic variation at Alr1 and Alr2 can predict the phenotypes in inbred lines, these two loci do not entirely predict the allorecognition phenotypes in wild-type colonies and their progeny, suggesting the presence of additional uncharacterized genes that are involved in the regulation of allorecognition in this species. Comparative genomics analyses were used to identify coding sequence differences from assembled chromosomal intervals of the ARC and from genomic scaffold sequences between two incompatible H. symbiolongicarpus siblings from a backcross population. New immunoglobulin superfamily (Igsf) genes are reported for the ARC, where five of these genes are closely related to the Alr1 and Alr2 genes, suggesting the presence of multiple Alr-like genes within this complex. Complementary DNA sequence evidence revealed that the allelic polymorphism of eight Igsf genes is associated with allorecognition phenotypes in a backcross population of H. symbiolongicarpus, yet that association was not found between parental colonies and their offspring. Alternative splicing was found as a mechanism that contributes to the variability of these genes by changing putative activating receptors to inhibitory receptors or generating secreted isoforms of allorecognition proteins. Our findings demonstrate that allorecognition in H. symbiolongicarpus is a multigenic phenomenon controlled by genetic variation in at least eight genes in the ARC complex.

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Acknowledgements

We thank Dr. Andrés Pinzón for his computing support to handle the genomic and transcriptomic data of Hydractinia. We would also like to thank Dr. Uri Frank for sharing the high-molecular weight DNA isolation protocol used in his laboratory. This study was funded by grant numbers 014-2013 from COLCIENCIAS, and Hermes 37463 from the Universidad Nacional de Colombia to Luis F. Cadavid.

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Correspondence to Henry Rodriguez-Valbuena.

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The original online version of this article was revised: The missing data for Table S6, Table S9 and Table S10 has been uploaded.

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Rodriguez-Valbuena, H., Gonzalez-Muñoz, A. & Cadavid, L.F. Multiple Alr genes exhibit allorecognition-associated variation in the colonial cnidarian Hydractinia. Immunogenetics 74, 559–581 (2022). https://doi.org/10.1007/s00251-022-01268-3

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  • DOI: https://doi.org/10.1007/s00251-022-01268-3

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