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A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution.

ABSTRACT: Throughout their evolution, plant nucleotide-binding leucine-rich-repeat receptors (NLRs) have acquired widely divergent unconventional integrated domains that enhance their ability to detect pathogen effectors. However, the functional dynamics that drive the evolution of NLRs with integrated domains (NLR-IDs) remain poorly understood. Here, we reconstructed the evolutionary history of an NLR locus prone to unconventional domain integration and experimentally tested hypotheses about the evolution of NLR-IDs. We show that the rice (Oryza sativa) NLR Pias recognizes the effector AVR-Pias of the blast fungal pathogen Magnaporthe oryzae. Pias consists of a functionally specialized NLR pair, the helper Pias-1 and the sensor Pias-2, that is allelic to the previously characterized Pia pair of NLRs: the helper RGA4 and the sensor RGA5. Remarkably, Pias-2 carries a C-terminal DUF761 domain at a similar position to the heavy metal-associated (HMA) domain of RGA5. Phylogenomic analysis showed that Pias-2/RGA5 sensor NLRs have undergone recurrent genomic recombination within the genus Oryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained transspecies in different Oryza lineages to detect sequence-divergent pathogen effectors. By contrast, Pias-1 has retained its NLR helper activity throughout evolution and is capable of functioning together with the divergent sensor-NLR RGA5 to respond to AVR-Pia. These results suggest that opposite selective forces have driven the evolution of paired NLRs: highly dynamic domain integration events maintained by balancing selection for sensor NLRs, in sharp contrast to purifying selection and functional conservation of immune signaling for helper NLRs.

SUBMITTER: Shimizu M

PROVIDER: S-EPMC9271155 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundGerm lines are the cell lineages that give rise to the sperm and eggs in animals. The germ lines first arise from primordial germ cells (PGCs) during embryogenesis: these form from either a presumed derived mode of preformed germ plasm (inheritance) or from an ancestral mechanism of inductive cell-cell signalling (induction). Numerous genes involved in germ line specification and development have been identified and functionally studied. However, little is known about the molecular evolutionary dynamics of germ line genes in metazoan model systems.ResultsHere, we studied the molecular evolution of germ line genes within three metazoan model systems. These include the genus Drosophila (N=34 genes, inheritance), the fellow insect Apis (N=30, induction), and their more distant relative Caenorhabditis (N=23, inheritance). Using multiple species and established phylogenies in each genus, we report that germ line genes exhibited marked variation in the constraint on protein sequence divergence (dN/dS) and codon usage bias (CUB) within each genus. Importantly, we found that de novo lineage-specific inheritance (LSI) genes in Drosophila (osk, pgc) and in Caenorhabditis (pie-1, pgl-1), which are essential to germ plasm functions under the derived inheritance mode, displayed rapid protein sequence divergence relative to the other germ line genes within each respective genus. We show this may reflect the evolution of specialized germ plasm functions and/or low pleiotropy of LSI genes, features not shared with other germ line genes. In addition, we observed that the relative ranking of dN/dS and of CUB between genera were each more strongly correlated between Drosophila and Caenorhabditis, from different phyla, than between Drosophila and its insect relative Apis, suggesting taxonomic differences in how germ line genes have evolved.ConclusionsTaken together, the present results advance our understanding of the evolution of animal germ line genes within three well-known metazoan models. Further, the findings provide insights to the molecular evolution of germ line genes with respect to LSI status, pleiotropy, adaptive evolution as well as PGC-specification mode.

Project description:BackgroundComparative phylogeography enables the study of historical and evolutionary processes that have contributed to shaping patterns of contemporary genetic diversity across co-distributed species. In this study, we explored genetic structure and historical demography in a range of coastal marine species across the northeast Atlantic to assess whether there are commonalities in phylogeographic patterns across taxa and to evaluate whether the timings of population expansions were linked to the Last Glacial Maximum (LGM).MethodsA literature search was conducted using Web of Science. Search terms were chosen to maximise the inclusion of articles reporting on population structure and phylogeography from the northeast Atlantic; titles and abstracts were screened to identify suitable articles within the scope of this study. Given the proven utility of mtDNA in comparative phylogeography and the availability of these data in the public domain, a meta-analysis was conducted using published mtDNA gene sequences. A standardised methodology was implemented to ensure that the genealogy and demographic history of all mtDNA datasets were reanalysed in a consistent and directly comparable manner.ResultsMitochondrial DNA datasets were built for 21 species. The meta-analysis revealed significant population differentiation in 16 species and four main types of haplotype network were found, with haplotypes in some species unique to specific geographical locations. A signal of rapid expansion was detected in 16 species, whereas five species showed evidence of a stable population size. Corrected mutation rates indicated that the majority of expansions were estimated to have occurred after the earliest estimate for the LGM (∼26.5 Kyr), while few expansions were estimated to have pre-dated the LGM.ConclusionThis study suggests that post-LGM expansion appeared to be common in a range of marine taxa, supporting the concept of rapid expansions after the LGM as the ice sheets started to retreat. However, despite the commonality of expansion patterns in many of these taxa, phylogeographic patterns appear to differ in the species included in this study. This suggests that species-specific evolutionary processes, as well as historical events, have likely influenced the distribution of genetic diversity of marine taxa in the northeast Atlantic.

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A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution.

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