Bento Gilberto, Routtu Jarkko, Fields Peter D, Bourgeois Yann, Du Pasquier Louis, Ebert Dieter
Basel University, Zoological Institute, Vesalgasse 1, Basel, Switzerland.
PLoS Genet. 2017 Feb 21;13(2):e1006596. doi: 10.1371/journal.pgen.1006596. eCollection 2017 Feb.
Negative frequency-dependent selection (NFDS) is an evolutionary mechanism suggested to govern host-parasite coevolution and the maintenance of genetic diversity at host resistance loci, such as the vertebrate MHC and R-genes in plants. Matching-allele interactions of hosts and parasites that prevent the emergence of host and parasite genotypes that are universally resistant and infective are a genetic mechanism predicted to underpin NFDS. The underlying genetics of matching-allele interactions are unknown even in host-parasite systems with empirical support for coevolution by NFDS, as is the case for the planktonic crustacean Daphnia magna and the bacterial pathogen Pasteuria ramosa. We fine-map one locus associated with D. magna resistance to P. ramosa and genetically characterize two haplotypes of the Pasteuria resistance (PR-) locus using de novo genome and transcriptome sequencing. Sequence comparison of PR-locus haplotypes finds dramatic structural polymorphisms between PR-locus haplotypes including a large portion of each haplotype being composed of non-homologous sequences resulting in haplotypes differing in size by 66 kb. The high divergence of PR-locus haplotypes suggest a history of multiple, diverse and repeated instances of structural mutation events and restricted recombination. Annotation of the haplotypes reveals striking differences in gene content. In particular, a group of glycosyltransferase genes that is present in the susceptible but absent in the resistant haplotype. Moreover, in natural populations, we find that the PR-locus polymorphism is associated with variation in resistance to different P. ramosa genotypes, pointing to the PR-locus polymorphism as being responsible for the matching-allele interactions that have been previously described for this system. Our results conclusively identify a genetic basis for the matching-allele interaction observed in a coevolving host-parasite system and provide a first insight into its molecular basis.
负频率依赖选择（NFDS）是一种进化机制，被认为可调控宿主 - 寄生虫的协同进化以及宿主抗性位点（如脊椎动物的主要组织相容性复合体（MHC）和植物中的R基因）的遗传多样性维持。宿主和寄生虫的匹配等位基因相互作用可防止普遍抗性和感染性的宿主和寄生虫基因型出现，这是一种预计为NFDS提供支撑的遗传机制。即使在有经验证据支持NFDS介导协同进化的宿主 - 寄生虫系统中，如浮游甲壳动物大型溞（Daphnia magna）和细菌病原体枝原体巴斯德氏菌（Pasteuria ramosa）的系统，匹配等位基因相互作用的潜在遗传学仍不为人所知。我们精细定位了一个与大型溞对枝原体巴斯德氏菌抗性相关的位点，并使用从头基因组和转录组测序对巴斯德氏菌抗性（PR -）位点的两个单倍型进行了遗传特征分析。PR - 位点单倍型的序列比较发现，PR - 位点单倍型之间存在显著的结构多态性，包括每个单倍型的很大一部分由非同源序列组成，导致单倍型大小相差66 kb。PR - 位点单倍型的高度差异表明存在多次、多样且重复的结构突变事件以及有限的重组历史。单倍型注释揭示了基因含量的显著差异。特别是，一组糖基转移酶基因存在于易感单倍型中，但在抗性单倍型中缺失。此外，在自然种群中，我们发现PR - 位点多态性与对不同枝原体巴斯德氏菌基因型的抗性变异相关，表明PR - 位点多态性是此前描述的该系统中匹配等位基因相互作用的原因。我们的结果最终确定了在协同进化的宿主 - 寄生虫系统中观察到的匹配等位基因相互作用的遗传基础，并首次深入了解了其分子基础。
