Complete Plastome Sequences from Glycine syndetika, and Six Additional Perennial Wild Relatives of Soybean

Organelle sequences have a long history of utility in phylogenetic analyses. Chloroplast sequences when combined with nuclear data can help resolve relationships among flowering plant genera, and within genera incongruence can point to reticulate evolution. Plastome sequences are becoming plentiful because they are increasingly easier to obtain. Complete plastome sequences allow us to detect rare rearrangements and test the tempo of sequence evolution. Chloroplast sequences are generally considered a nuisance to be kept to a minimum in bacterial artificial chromosome libraries. Here, we sequenced two bacterial artificial chromosomes per species to generate complete plastome sequences from seven species. The plastome sequences from Glycine syndetika and six other perennial Glycine species are similar in arrangement and gene content to the previously published soybean plastome. Repetitive sequences were detected in high frequencies as in soybean, but further analysis showed that repeat sequence numbers are inflated. Previous chloroplast-based phylogenetic trees for perennial Glycine were incongruent with nuclear gene\u2013based phylogenetic trees. We tested whether the hypothesis of introgression was supported by the complete plastomes. Alignment of complete plastome sequences and Bayesian analysis allowed us to date putative hybridization events supporting the hypothesis of introgression and chloroplast \u201ccapture.\u201

Expression and trans-specific polymorphism of self-incompatibility RNases in Coffea (Rubiaceae)

Self-incompatibility (SI) is widespread in the angiosperms, but identifying the biochemical components of SI mechanisms has proven to be difficult in most lineages. Coffea (coffee; Rubiaceae) is a genus of old-world tropical understory trees in which the vast majority of diploid species utilize a mechanism of gametophytic self-incompatibility (GSI). The S-RNase GSI system was one of the first SI mechanisms to be biochemically characterized, and likely represents the ancestral Eudicot condition as evidenced by its functional characterization in both asterid (Solanaceae, Plantaginaceae) and rosid (Rosaceae) lineages. The S-RNase GSI mechanism employs the activity of class III RNase T2 proteins to terminate the growth of "self" pollen tubes. Here, we investigate the mechanism of Coffea GSI and specifically examine the potential for homology to S-RNase GSI by sequencing class III RNase T2 genes in populations of 14 African and Madagascan Coffea species and the closely related self-compatible species Psilanthus ebracteolatus. Phylogenetic analyses of these sequences aligned to a diverse sample of plant RNase T2 genes show that the Coffea genome contains at least three class III RNase T2 genes. Patterns of tissue-specific gene expression identify one of these RNase T2 genes as the putative Coffea S-RNase gene. We show that populations of SI Coffea are remarkably polymorphic for putative S-RNase alleles, and exhibit a persistent pattern of trans-specific polymorphism characteristic of all S-RNase genes previously isolated from GSI Eudicot lineages. We thus conclude that Coffea GSI is most likely homologous to the classic Eudicot S-RNase system, which was retained since the divergence of the Rubiaceae lineage from an ancient SI Eudicot ancestor, nearly 90 million years ago.United States National Science Foundation [0849186]; Society of Systematic Biologists; American Society of Plant Taxonomists; Duke University Graduate Schoolinfo:eu-repo/semantics/publishedVersio

On the Evolutionary Modification of Self-Incompatibility: Implications of Partial Clonality for Allelic Diversity and Genealogical Structure

Experimental investigations of homomorphic self-incompatibility (SI) have revealed an unanticipated level of complexity in its expression, permitting fine regulation over the course of a lifetime or a range of environmental conditions. Many flowering plants express some level of clonal reproduction, and phylogenetic analyses suggest that clonality evolves in a correlated fashion with SI in Solanum (Solanaceae). Here, we use a diffusion approximation to explore the effects on the evolutionary dynamics of SI of vegetative propagation with SI restricted to reproduction through seed. While clonality reduces the strength of frequency-dependent selection maintaining S-allele diversity, much of the great depth typical of S-allele genealogies is preserved. Our results suggest that clonality can play an important role in the evolution of SI systems, and may afford insight into unexplained features of allele genealogies in the Solanaceae

Independent S-Locus Mutations Caused Self-Fertility in Arabidopsis thaliana

A common yet poorly understood evolutionary transition among flowering plants is a switch from outbreeding to an inbreeding mode of mating. The model plant Arabidopsis thaliana evolved to an inbreeding state through the loss of self-incompatibility, a pollen-rejection system in which pollen recognition by the stigma is determined by tightly linked and co-evolving alleles of the S-locus receptor kinase (SRK) and its S-locus cysteine-rich ligand (SCR). Transformation of A. thaliana, with a functional AlSRKb-SCRb gene pair from its outcrossing relative A. lyrata, demonstrated that A. thaliana accessions harbor different sets of cryptic self-fertility–promoting mutations, not only in S-locus genes, but also in other loci required for self-incompatibility. However, it is still not known how many times and in what manner the switch to self-fertility occurred in the A. thaliana lineage. Here, we report on our identification of four accessions that are reverted to full self-incompatibility by transformation with AlSRKb-SCRb, bringing to five the number of accessions in which self-fertility is due to, and was likely caused by, S-locus inactivation. Analysis of S-haplotype organization reveals that inter-haplotypic recombination events, rearrangements, and deletions have restructured the S locus and its genes in these accessions. We also perform a Quantitative Trait Loci (QTL) analysis to identify modifier loci associated with self-fertility in the Col-0 reference accession, which cannot be reverted to full self-incompatibility. Our results indicate that the transition to inbreeding occurred by at least two, and possibly more, independent S-locus mutations, and identify a novel unstable modifier locus that contributes to self-fertility in Col-0

Does Speciation between Arabidopsis halleri and Arabidopsis lyrata Coincide with Major Changes in a Molecular Target of Adaptation?

Ever since Darwin proposed natural selection as the driving force for the origin of species, the role of adaptive processes in speciation has remained controversial. In particular, a largely unsolved issue is whether key divergent ecological adaptations are associated with speciation events or evolve secondarily within sister species after the split. The plant Arabidopsis halleri is one of the few species able to colonize soils highly enriched in zinc and cadmium. Recent advances in the molecular genetics of adaptation show that the physiology of this derived ecological trait involves copy number expansions of the AhHMA4 gene, for which orthologs are found in single copy in the closely related A. lyrata and the outgroup A. thaliana. To gain insight into the speciation process, we ask whether adaptive molecular changes at this candidate gene were contemporary with important stages of the speciation process. We first inferred the scenario and timescale of speciation by comparing patterns of variation across the genomic backgrounds of A. halleri and A. lyrata. Then, we estimated the timing of the first duplication of AhHMA4 in A. halleri. Our analysis suggests that the historical split between the two species closely coincides with major changes in this molecular target of adaptation in the A. halleri lineage. These results clearly indicate that these changes evolved in A. halleri well before industrial activities fostered the spread of Zn- and Cd-polluted areas, and suggest that adaptive processes related to heavy-metal homeostasis played a major role in the speciation process

Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis

Self-incompatibility has been considered by geneticists a model system for reproductive biology and balancing selection, but our understanding of the genetic basis and evolution of this molecular lock-and-key system has remained limited by the extreme level of sequence divergence among haplotypes, resulting in a lack of appropriate genomic sequences. In this study, we report and analyze the full sequence of eleven distinct haplotypes of the self-incompatibility locus (S-locus) in two closely related Arabidopsis species, obtained from individual BAC libraries. We use this extensive dataset to highlight sharply contrasted patterns of molecular evolution of each of the two genes controlling self-incompatibility themselves, as well as of the genomic region surrounding them. We find strong collinearity of the flanking regions among haplotypes on each side of the S-locus together with high levels of sequence similarity. In contrast, the S-locus region itself shows spectacularly deep gene genealogies, high variability in size and gene organization, as well as complete absence of sequence similarity in intergenic sequences and striking accumulation of transposable elements. Of particular interest, we demonstrate that dominant and recessive S-haplotypes experience sharply contrasted patterns of molecular evolution. Indeed, dominant haplotypes exhibit larger size and a much higher density of transposable elements, being matched only by that in the centromere. Overall, these properties highlight that the S-locus presents many striking similarities with other regions involved in the determination of mating-types, such as sex chromosomes in animals or in plants, or the mating-type locus in fungi and green algae

The evolution of selfing in Arabidopsis thaliana

Unlike most of its close relatives, Arabidopsis thaliana is capable of self-pollination. In other members of the mustard family, outcrossing is ensured by the complex self-incompatibility (S) locus,which harbors multiple diverged specificity haplotypes that effectively prevent selfing. We investigated the role of the S locus in the evolution of and transition to selfing in A. thaliana. We found that the S locus of A. thaliana harbored considerable diversity, which is an apparent remnant of polymorphism in the outcrossing ancestor. Thus, the fixation of a single inactivated S-locus allele cannot have been a key step in the transition to selfing. An analysis of the genome-wide pattern of linkage disequilibrium suggests that selfing most likely evolved roughly a million years ago or more