NOD-Like Receptor Genes Undergo Diversity-Enhancing Evolution in a Fungal Species Complex

Le résumé fourni par la source

Fungi harbor diverse arrays of genes encoding NOD-like receptors (NLRs), key intracellular immune proteins found in plants, animals, and bacteria. Some fungal NLRs are known to control regulated cell death in the context of allorecognition, the capacity to recognize conspecific nonself. However, the function of most fungal NLR genes remains unknown. Here, we characterize the evolution of the NLRs repertoire in the Podospora anserina species complex. We show that the vast majority of the NLRs display effector domains known to be involved in regulated cell death execution. Moreover, NLRs undergo more rapid gene turnover than random genes, show higher dN/dS values, and faster evolutionary rates. A subgroup of NLRs, distinguished by superstructure-forming repeats with very high sequence identity (high internal conservation), evolved independently multiple times. We found that high internal conservation NLRs are more associated with transposable elements, exhibit higher nucleotide diversity partially driven by repeat-induced point mutation, and show elevated Tajima's D values indicative of balancing selection. Furthermore, high internal conservation NLR phylogenies do not recapitulate species relationships, which we determined is caused by both balancing selection and introgression. In addition, we identified cases of repeat exchange between distinct high internal conservation NLR genes, implying that novel binding specificities may evolve through repeat shuffling, thereby increasing allelic diversity. Finally, we determined that NLR genes with high internal conservation repeats exist outside of the fungal realm, arguing for similar dynamics in other taxa. Overall, these findings suggest that fungal NLRs evolve under diversity-enhancing mechanisms and display selective signatures consistent with a general immune function.

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