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Rifkin, J. L.

Publications and source records attributed to Rifkin, J. L..

9 recordsLinked to original sources

The Dynamics of Long Terminal Repeat Proliferation in the Hesperis matronalis Genome

Genome sizes vary across four orders of magnitude in flowering plants, with consequences for evolution. Much of this variation is due to differences in transposable element content, particularly in long terminal repeat (LTR) retrotransposons. Despite their importance in plant genome evolution, LTRs have long been challenging to characterize because of their repetitive nature, but recent advances in sequencing allow more detailed explorations of their behavior. They are now known to occupy distinct genomic niches, and to evolve and proliferate over time as they escape host controls. In this study, we present a new genome sequence of the largest Brassicaceae genome, Hesperis matronalis, and describe its transposable element complement and how LTRs contributed to its genome expansion. We find evidence for both early proliferation of Ty3 elements and rapid recent expansion of Ty1-copia elements. In addition, we place the H. matronalis LTRs in a broader context of LTR evolution in the Brassicaceae, showing that the dominant copia families are part of an evolutionary radiation endemic to Hesperis. Finally, we describe differences in LTR age, proximity to genes, and apparent removal rate which suggest consistent genomic niches over the lifespan of a TE family. These results shed light on how LTRs evolve dynamically with host genomes, and have contributed to the expansion of the largest genome in the Brassicaceae. Significance StatementOrganisms differ in many ways, including the size of their genomes. Genome size, in turn, can affect many aspects of evolution, such as what kinds of mutations are available to natural selection and how effectively natural selection can act. The "complexity" of an organism does not predict its genome size; rather, much of this variation is explained by the amount of transposable elements, or "jumping genes," that inhabit a genome. This study describes the evolutionary history of the transposable elements in dames rocket (Hesperis matronalis), which has the largest genome of any plant in the mustard family (Brassicaceae). We find that the genome inflation in Hesperis is due to transposable elements that are not found elsewhere in the Brassicaceae, and likely diversified within Hesperis. Characterizing the evolution and behavior of transposable elements in this genome offers a better understanding of the forces that determine genome size and ultimately affect the evolution of life on earth.

genomics↗

Color, size, shape: The drivers of floral variation in Hesperis matronalis (Dames Rocket)

Evolutionary biologists have long been intrigued by the factors that sustain genetic and phenotypic variation within and among natural populations. Polymorphisms underlying components of floral display - such as floral color, size, and shape - are uniquely of interest since variation in these traits impact pollinator attraction, rates of visitation, and pollinator efficiency, which ultimately influence patterns of plant reproduction and therefore fitness. We leverage existing floral variation present within and among populations of Hesperis matronalis (Dames Rocket) to disentangle the relative influence of natural selection and genetic drift in shaping floral trait variation. We employ a multi-tiered approach: we determine if variation in floral traits (color, size, and petal shape) is influenced by geography or environmental variables such as temperature and precipitation, we evaluate whether selection underlies trait variation by comparing phenotypic divergence (PST) with neutral genetic structure (FST), and we perform a Lande-Arnold selection analysis to explore the relationship between fitness and floral trait variation within natural populations. We find that selection underlies the divergence of floral color, floral size, and petal width among H. matronalis populations, with PST > FST for each trait. We find no indication, however, that variation in size in this species is influenced by the environment, but some evidence that variation in floral color and petal shape may be influenced by temperature. Finally, selection analyses of contemporary populations indicate divergent selection affecting combinations of color, petal shape, and plant size. These results suggest that the variation in floral shape in this species may be maintained due to environmental pressures, whereas floral color is influenced by pollinator visibility and the presence of different pollinator groups.

evolutionary biology↗

Structure and sequence evolution in the pennycress (Thlaspi arvense) pangenome

O_LIEukaryotic genomes harbor many forms of variation, including nucleotide diversity and structural polymorphisms, which experience natural selection and contribute to genome evolution and biodiversity. However, harnessing this variation for agriculture hinges on our ability to detect, quantify, catalog, and utilize genetic diversity. C_LIO_LIHere, we explore seven complete genomes of the emerging biofuel crop pennycress (Thlaspi arvense) drawn from across the speciess current genetic diversity to catalogue variation in genome structure and content. C_LIO_LIAcross this new pangenome resource, we find contrasting evolutionary modes in different genomic regions. Gene-poor, repeat-rich pericentromeric regions experience frequent rearrangements, including repeated centromere repositioning. In contrast, conserved gene-dense chromosome arms maintain large-scale synteny across accessions, even in fast-evolving immune genes where microsynteny breaks down across species but the macrosynteny of gene cluster positioning is maintained. C_LIO_LIOur findings highlight that multiple elements of the genome experience dynamic evolution that conserves functional content on the chromosome scale but allows rearrangement and presence-absence variation on a local scale. This diversity is invisible to classical reference-based approaches and highlights the strength and utility of pangenomic resources. These results provide a valuable case study of rapid genomic structural evolution within a species and powerful resources for crop development in an emerging biofuel crop. C_LI

genomics↗

Phylogenomics resolves key relationships in Rumex and uncovers a dynamic history of independently evolving sex chromosomes

Sex chromosomes have evolved independently many times across eukaryotes. Despite a considerable body of literature on the evolution of sex chromosomes, the causes and consequences of variation in the formation, degeneration, and turnover of sex chromosomes remain poorly understood. Comparative approaches in groups with sexual system variation can be valuable for understanding these questions. Plants are well-suited to such comparative studies, with many lineages containing relatively recent origins of dioecy and sex chromosomes as well as hermaphroditic close relatives. Rumex is a diverse genus of flowering plants harboring significant sexual system variation, including hermaphroditic and dioecious clades with XY sex chromosomes. Previous disagreement in the phylogenetic relationships among key species have rendered the history of sex chromosome evolution uncertain. Resolving this history is important to the development of Rumex as a system for the comparative study of sex chromosome evolution. Here, we leverage new transcriptome assemblies from 11 species representing the major clades in the genus, along with a whole-genome assembly generated for a pivotal hermaphroditic species, to further resolve the phylogeny and history of sex chromosome evolution in Rumex. Using phylogenomic approaches, we find evidence for two independent origins of sex chromosomes and introgression from unsampled taxa in the genus. Comparative genomics reveals massive chromosomal rearrangements in a dioecious species, with evidence for a complex origin of the sex chromosomes through multiple chromosomal fusions. However, we see no evidence of elevated rates of fusion on the sex chromosome in comparison with autosomes, providing no support for an adaptive hypothesis for the sex chromosome expansion. Overall, our results highlight the dynamic nature of sex chromosome systems in Rumex and illustrate the utility of the genus as a model for the comparative study of sex chromosome evolution.

evolutionary biology↗

Genomic signatures of hybridization on the neo-X chromosome of Rumex hastatulus

Natural hybrid zones provide opportunities for studies of the evolution of reproductive isolation in wild populations. Although several recent investigations have found that the formation of neo-sex chromosomes is associated with reproductive isolation, the mechanisms remain unclear in most cases. Here, we assess the contemporary structure of gene flow in the contact zone between largely allopatric cytotypes of the dioecious plant Rumex hastatulus, a species in which there is evidence of sex chromosome turn-over. Males to the west of the Mississippi river, USA, have an X and a single Y chromosome, whereas populations to the east of the river have undergone a chromosomal rearrangement giving rise to a larger X and two Y chromosomes. Using reduced-representation sequencing, we provide evidence that hybrids form readily and survive multiple backcross generations in the field, demonstrating the potential for ongoing gene flow between the cytotypes. At the scale of chromosomes, cline analysis of each chromosome separately captured no signals of difference in cline shape between chromosomes. However, when comparing SNPs, principal component regression revealed a significant increase in the contribution of individual SNPs to inter-cytotype differentiation on the neo-X, but no correlation with recombination rate. Cline analysis revealed that the only SNPs with significantly shallower clines than the genome-average were located on the neo-X. Our data are consistent with a role for the neo-sex chromosome in reproductive isolation between R. hastatulus cytotypes. Our investigation highlights the importance of studying plant hybrid zones in species with sex chromosomes for understanding mechanisms of reproductive isolation and for understanding the role of gene flow in governing the spread of the neo-X chromosomes.

evolutionary biology↗

Recombination landscape dimorphism contributes to sexchromosome evolution in the dioecious plant Rumexhastatulus

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

genetics↗

GENETIC ARCHITECTURE OF DIVERGENCE: THE SELFING SYNDROME IN IPOMOEA LACUNOSA

Premise of the studyHighly selfing plant species frequently display a distinctive suite of traits termed the "selfing syndrome." This study tests the hypothesis that these traits are grouped into correlated evolutionary modules and determines the degree of independence between such modules. MethodsWe evaluated phenotypic correlations and QTL overlaps in F2 offspring of a cross between the morning glories Ipomoea lacunosa and I. cordatotriloba and investigated how traits clustered into modules at both the phenotypic and genetic level. We then compared our findings to other QTL studies of the selfing syndrome. Key resultsIn the I. lacunosa selfing syndrome, traits group into modules that display correlated evolution within but not between modules. QTL overlap predicts phenotypic correlations, and QTLs affecting the same trait module are significantly physically clustered in the genome. The genetic architecture of the selfing syndrome varies across systems, but the pattern of stronger within-than between-module correlation is widespread. ConclusionsThe genetic architecture we observe in the selfing syndrome is consistent with a growing understanding of floral morphological integration achieved via pleiotropy in clustered traits. This view of floral evolution is consistent with resource limitation or predation driving the evolution of the selfing syndrome, but invites further research into both the selective causes of the selfing syndrome and how genetic architecture itself evolves in response to changes in mating system.

evolutionary biology↗

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

1Classical models suggest recombination rates on sex chromosomes evolve in a stepwise manner to localize the inheritance of sexually antagonistic variation in the sex where it is beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with pre-existing recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus, a species with a young neo-sex chromosome found in part of its geographical range. We found that the ancestral sex-linked region is located in a large region characterized by low recombination. Furthermore, comparison between the recombination landscape of the neo-sex chromosome and its autosomal homologue indicates that low recombination rates preceded sex linkage. Our findings suggest that ancestrally low rates of recombination have facilitated the formation and evolution of heteromorphic sex chromosomes.

evolutionary biology↗

Asymmetric gene flow causes cascading reproductive isolation

Hybridization between species can affect the strength of the reproductive barriers that separate those species. Two extensions of this effect are: (1) the expectation that asymmetric hybridization will have asymmetric effects on reproductive barrier strength and (2) the expectation that local hybridization will affect only local reproductive barrier strength and could therefore alter within-species compatibility. We tested these hypotheses in a pair of morning glory species that exhibit asymmetric gene flow from highly selfing Ipomoea lacunosa into mixed mating I. cordatotriloba in regions where they co-occur. Because of the direction of this gene flow, we predicted that reproductive barrier strength would be more strongly affected in I. cordatotriloba than I. lacunosa. We also predicted that changes to reproductive barriers in sympatric I. cordatotriloba populations would affect compatibility with allopatric populations of that species. We tested these predictions by measuring the strength of a reproductive barrier to seed set across the species ranges. Consistent with our first prediction, we found that sympatric and allopatric I. lacunosa produce the same number of seeds in crosses with I. cordatotriloba, whereas crosses between sympatric I. cordatotriloba and I. lacunosa are more successful than crosses between allopatric I. cordatotriloba and I. lacunosa. This difference in compatibility appears to reflect an asymmetric decrease in the strength of the barrier to seed set in sympatric I. cordatotriloba, which could be caused by I. lacunosa alleles that have introgressed into I. cordatotriloba. We further demonstrated that changes to sympatric I. cordatotriloba have decreased its ability to produce seeds with allopatric populations of the same species, in line with our second prediction. Thus, in a manner analogous to cascade reinforcement, we suggest that introgression associated with hybridization not only influences between-species isolation but can also contribute to isolation within a species. Impact StatementBiological diversity depends on traits that prevent different species from successfully interbreeding. However, these reproductive barriers are often imperfect, leading to hybrid matings and possible genetic exchange between species where they occur together. When this happens, the reproductive barriers that separate species can themselves evolve to become stronger or weaker. Understanding the effects of hybridization on reproductive barriers is key to predicting the potential for future hybridization between species and ultimately whether hybridizing species will diverge, persist, or merge in regions where they co-occur. Here we hypothesize and show that hybridization in only one direction causes unidirectional changes to reproductive barrier strength and that geographically restricted hybridization causes local changes to barrier strength that can affect interbreeding within a species. Specifically, we found that gene flow from one species of morning glory into another likely caused a reproductive barrier to decrease in regions where they co-occur. The decreased reproductive barrier is caused by changes in only the species that received gene flow. We also found that the locally reduced barriers in the species that received gene flow affected reproductive compatibility between populations within that species. Thus, a breakdown of barriers between species can cause a build-up of barriers within a species. Our work demonstrates critical and rarely explored interactions at species boundaries.

evolutionary biology↗