Gene expression reveals the pancreas of Aselli as a critical organ for plasma cell differentiation in the common shrew

Abstract

Almost all mammals rely on the thymus and bone marrow to generate and differentiate B- and T cells essential for adaptive immunity. A few members of the family Soricidae, or true shrews, have also evolved the pancreas of Aselli, a kidney-sized organ hypothesized to serve this primary immune role, and whose gene expression profile is unknown. Here we introduce transcriptomes of juvenile Sorex araneus pancreas of Aselli, compare them to those of the spleen and chick bursa of Fabricius, an analogous and bird-specific organ, and explore differential expression overlaps with positively selected genes. While differential gene expression analyses revealed overexpression of genes that regulate the differentiation of B cells into long-term plasma cells (e.g., IRF4, XBP1, PRDM1) compared to the spleen and more convergent expression with the bursa of Fabricius than expected by chance (including IRF4), overlaps with positive selection were as expected and included PTPRCAP, which regulates both T and B cell antigen responses and lymph node size. Our results support the specialized role of the pancreas of Aselli in adaptive immunity, and we propose this unique organ evolved at the intersection between extreme metabolic demands and high parasite burdens in tiny yet very active shrews.