Dominance hierarchy arising from the evolution of a complex small RNA regulatory network
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ABSTRACT: Self-pollen rejection in the Brassicaceae is determined by the diploid genotype of the pollen-producing plant, and it has long been known that the alleles show a dominance hierarchy. How this hierarchy is controlled and evolves has been a classical puzzle since the pre-molecular days of genetics. Here, we uncover the system of at least 17 small RNA (sRNA) producing loci and their multiple target sites that collectively control the dominance hierarchy among alleles of a self-incompatible Arabidopsis species. Our results demonstrate that natural selection shapes a dynamic repertoire of sRNA/targets interactions by jointly acting on sRNA genes, their processing precision and their target sites. It is remarkable that a single gene can evolve such a complex system of regulation among its own alleles.
Project description:Self-pollen rejection in the Brassicaceae is determined by the diploid genotype of the pollen-producing plant, and it has long been known that the alleles show a dominance hierarchy. How this hierarchy is controlled and evolves has been a classical puzzle since the pre-molecular days of genetics. Here, we uncover the system of at least 17 small RNA (sRNA) producing loci and their multiple target sites that collectively control the dominance hierarchy among alleles of a self-incompatible Arabidopsis species. Our results demonstrate that natural selection shapes a dynamic repertoire of sRNA/targets interactions by jointly acting on sRNA genes, their processing precision and their target sites. It is remarkable that a single gene can evolve such a complex system of regulation among its own alleles. Sequencing of small RNAs from A. halleri floral buds, with this single exception (Al14, from A. lyrata).
Project description:Self-incompatibility (SI) in flowering plants is a common mechanism that prevents self-fertilization and promotes outcrossing. In Brassicaceae, the locus controlling SI is highly diverse and dozens of distinct alleles are organized in a complex dominance hierarchy: the gene controlling SI specificity in pollen always shows monoallelic expression in heterozygote individuals, and this is achieved through the action of sRNA precursors that resemble miRNAs, although the mechanism behind this remains elusive. Here, we engineered Arabidopsis thaliana lines expressing components of the Arabidopsis halleri SI system and used a reverse genetics approach to pinpoint the pathways underlying the function of these sRNA precursors. We showed that they trigger a robust decrease in transcript abundance of the recessive pollen SI genes, but not through the canonical transcriptional or post transcriptional gene silencing pathways. Furthermore, we observed that single sRNA precursors are typically processed into hundreds of sRNA molecules, with distinct sizes, abundance levels and ARGONAUTE loading preferences. This heterogeneity closely resembles that of proto-miRNAs, the evolutionary ancestors of miRNAs. Our results suggest that these apparent arbitrary features, which are often associated with lack of effects in gene expression, are crucial in the context of the SI dominance hierarchy since they allow one sRNA precursor of a given allele to repress multiple other (more recessive) alleles. This study not only provides an in-depth characterization of the molecular features underlying complex dominance interactions, but also constitutes a unique example of how specific evolutionary constraints shape the progression of sRNA precursors within the proto-miRNA – miRNA evolutionary continuum.
Project description:Self-incompatibility (SI) in flowering plants is a common mechanism that prevents self-fertilization and promotes outcrossing. In Brassicaceae, the locus controlling SI is highly diverse and dozens of distinct alleles are organized in a complex dominance hierarchy: the gene controlling SI specificity in pollen always shows monoallelic expression in heterozygote individuals, and this is achieved through the action of sRNA precursors that resemble miRNAs, although the mechanism behind this remains elusive. Here, we engineered Arabidopsis thaliana lines expressing components of the Arabidopsis halleri SI system and used a reverse genetics approach to pinpoint the pathways underlying the function of these sRNA precursors. We showed that they trigger a robust decrease in transcript abundance of the recessive pollen SI genes, but not through the canonical transcriptional or post transcriptional gene silencing pathways. Furthermore, we observed that single sRNA precursors are typically processed into hundreds of sRNA molecules, with distinct sizes, abundance levels and ARGONAUTE loading preferences. This heterogeneity closely resembles that of proto-miRNAs, the evolutionary ancestors of miRNAs. Our results suggest that these apparent arbitrary features, which are often associated with lack of effects in gene expression, are crucial in the context of the SI dominance hierarchy since they allow one sRNA precursor of a given allele to repress multiple other (more recessive) alleles. This study not only provides an in-depth characterization of the molecular features underlying complex dominance interactions, but also constitutes a unique example of how specific evolutionary constraints shape the progression of sRNA precursors within the proto-miRNA – miRNA evolutionary continuum.
Project description:This SuperSeries is composed of the following subset Series: GSE36822: Clonal competition with alternating dominance in multiple myeloma [244kCGH] GSE36823: Clonal competition with alternating dominance in multiple myeloma [44kCGH] GSE36824: Clonal competition with alternating dominance in multiple myeloma [GEP] Refer to individual Series
Project description:Aggression among group housed male mice continues to challenge laboratory animal researchers because mitigation strategies are generally applied at the cage level without a good understanding of how it affects the dominance hierarchy. Aggression is typically displayed by the dominant mouse, targeting lower ranking subordinates, thus strategies may be more successful if applied specifically to the dominant mouse. Unfortunately, dominance rank is often not assessed because of time intensive observations or tests. Several dominance measures have been developed, but none directly compared to home cage behavior in standard housing. This study assessed the convergent validity of three dominance measures (urinary darcin, tube test score, preputial gland to body length ratio) with wound severity and rankings based on home cage behavior, using factor analysis. Discriminant validity with open field measures was assessed to determine if tube test scores are independent from anxiety. Cages were equally split between SJL and albino C57BL/6 strains and group sizes of 3 or 5 (N=24). During the first week, home cage behavior was observed, and the dominance measures were recorded over the second week. After controlling for strain and group size, darcin and preputial ratio had strong loadings on the same factor as home cage ranking and were significant predictors of home cage ranking showing strong convergent validity. Tube test scores were not significantly impacted by open field data, showing discriminant validity. Social network analysis was also done to reveal that despotic power structures were prevalent, aggressors were typically more active and rested away from cage mates, and the amount of social investigation and aggression performed by an individual were highly correlated. Data from this study show that darcin and preputial ratio are representative of home cage aggression and provide further insight on individual behavior patterns in group housed male mice.
Project description:The goal of the project is to produce a standard annotation of the loci producing small RNAs in the maize genome. To achieve this goal we produced small RNA libraries from four different maize tissues, which will allow the identification of tissue-specific small RNA expression. The availability of bilogical replicates for three of the four tissues analyzed will guarantee robustness in the small RNA genes identification process. sRNA profile of maize expanded leaf, wrapped leaf, pollen and embryo, collected from B73 wt plants grown under control conditions. Leaves and pollen samples are replicated three times, embryo one time.
Project description:In Arabidopsis thaliana, DNA-dependent RNA polymerase IV (Pol IV) is required for the formation of transposable element (TE)-derived small RNA (sRNA) transcripts. These transcripts are processed by DICER-LIKE3 into 24-nt small interfering RNAs (siRNAs) that guide RNA-directed DNA methylation. In the pollen grain, Pol IV is also required for the accumulation of 21/22-nt epigenetically activated siRNAs (easiRNAs), which likely silence TEs via post-transcriptional mechanisms. Despite this proposed role of Pol IV, its loss of function in Arabidopsis does not cause a discernable pollen defect. Here, we show that the knockout of NRPD1, encoding the largest subunit of Pol IV in the Brassicaceae species Capsella rubella, caused post-meiotic arrest of pollen development at the microspore stage. As in Arabidopsis, all TE-derived siRNAs were 2 depleted in Capsella nrpd1 microspores. In the wild-type background, the same TEs produced 21/22-nt and 24-nt siRNAs; these processes required Pol IV activity. Arrest of Capsella nrpd1 microspores was accompanied by the deregulation of genes targeted by Pol IV-dependent siRNAs. TEs were much closer to genes in Capsella rubella compared to Arabidopsis thaliana, perhaps explaining the essential role of Pol IV in pollen development in Capsella. Our discovery that Pol IV is functionally required in Capsella microspores emphasizes the relevance of investigating different plant models.
Project description:Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that differences in dominance are also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated so far, potentially due to variation in the predictors and energetic consequences of dominant status. To test this possibility, we investigated the association between social status and gene expression in the blood of wild meerkats in the Kalahari Desert of South Africa, including in response to lipopolysaccharide, Gardiquimod, and glucocorticoid stimulation (n=740 samples; 113 meerkats). Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females and reproductive skew is high. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex-specific signature of dominance, including 1,045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways, as well as an exacerbated immune response to LPS challenge. Female meerkats therefore resemble male baboons, where physical competition is also central to determining rank hierarchies and mating effort is high, but differ from female primates in which social status is determined by nepotism. Our results support the hypothesis that the gene regulatory signature of social status depends on the determinants and energetic costs of social dominance. They also support potential life history trade-offs between investment in reproduction versus somatic maintenance.