Nora Hohmann

VAL- and AtBMI1-Mediated H2Aub Initiate the Switch from Embryonic to Postgerminative Growth in Arabidopsis

Plant B3-domain transcription factors have an important role in regulating seed development, in particular seed maturation and germination. Among the B3 factors, the AFL (ABSCISIC ACID INSENSITIVE3 [ABI3], FUSCA3 [FUS3], and LEAFY COTYLEDON2 [LEC2]) proteins activate the seed maturation program in a complex network, while the VAL (VP1/ABI3-LIKE) 1/2/3 proteins suppress AFL action in order to initiate germination and vegetative development through an as yet unknown mechanism. In addition, the AFL genes and LEAFY COTYLEDON1 (LEC1), referred as seed maturation genes, are epigenetically repressed after germination by the Polycomb group (PcG) machinery via its histone-modifying activities: the histone H3 lysine 27 trimethyltransferase activity of the PcG repressive complex 2 (PRC2) and the E3 H2A monoubiquitin ligase activity of the PRC1. Both histone modifications are required for the repression; however, the underlying mechanism is far from clear, because the localization and the role of H2Aub marks are still unknown. In this work, we demonstrate that VAL proteins and AtBMI1-mediated H2Aub initiate repression of seed maturation genes. After the initial off switch, the repression is maintained by PRC2-mediated H3K27me3. Our results indicate that the regulation of seed maturation genes does not follow the classic hierarchical model proposed for animal PcG-mediated repression, since the PRC1 activity is required for the H3K27me3 modification of these genes. Furthermore, we show different mechanisms to achieve PcG repression in plants, as the repression of genes involved in other processes has different requirements for H2Aub and H3K27me3 marking.

A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History

The time-calibrated evolutionary history of Brassicaceae is characterized by polyploidization and rapid genomic stabilization indicating polyploidization as driver for future diversification. The Brassicaceae include several major crop plants and numerous important model species in comparative evolutionary research such as Arabidopsis, Brassica, Boechera, Thellungiella, and Arabis species. As any evolutionary hypothesis needs to be placed in a temporal context, reliably dated major splits within the evolution of Brassicaceae are essential. We present a comprehensive time-calibrated framework with important divergence time estimates based on whole-chloroplast sequence data for 29 Brassicaceae species. Diversification of the Brassicaceae crown group started at the Eocene-to-Oligocene transition. Subsequent major evolutionary splits are dated to ∼20 million years ago, coinciding with the Oligocene-to-Miocene transition, with increasing drought and aridity and transient glaciation events. The age of the Arabidopsis thaliana crown group is 6 million years ago, at the Miocene and Pliocene border. The overall species richness of the family is well explained by high levels of neopolyploidy (43% in total), but this trend is neither directly associated with an increase in genome size nor is there a general lineage-specific constraint. Our results highlight polyploidization as an important source for generating new evolutionary lineages adapted to changing environments. We conclude that species radiation, paralleled by high levels of neopolyploidization, follows genome size decrease, stabilization, and genetic diploidization.

Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism

The notion of species as reproductively isolated units related through a bifurcating tree implies that gene trees should generally agree with the species tree and that sister taxa should not share polymorphisms unless they diverged recently and should be equally closely related to outgroups. It is now possible to evaluate this model systematically. We sequenced multiple individuals from 27 described taxa representing the entire Arabidopsis genus. Cluster analysis identified seven groups, corresponding to described species that capture the structure of the genus. However, at the level of gene trees, only the separation of Arabidopsis thaliana from the remaining species was universally supported, and, overall, the amount of shared polymorphism demonstrated that reproductive isolation was considerably more recent than the estimated divergence times. We uncovered multiple cases of past gene flow that contradict a bifurcating species tree. Finally, we showed that the pattern of divergence differs between gene ontologies, suggesting a role for selection.

Taming the wild: resolving the gene pools of non-model Arabidopsis lineages

BackgroundWild relatives in the genus Arabidopsis are recognized as useful model systems to study traits and evolutionary processes in outcrossing species, which are often difficult or even impossible to investigate in the selfing and annual Arabidopsis thaliana. However, Arabidopsis as a genus is littered with sub-species and ecotypes which make realizing the potential of these non-model Arabidopsis lineages problematic. There are relatively few evolutionary studies which comprehensively characterize the gene pools across all of the Arabidopsis supra-groups and hypothesized evolutionary lineages and none include sampling at a world-wide scale. Here we explore the gene pools of these various taxa using various molecular markers and cytological analyses.ResultsBased on ITS, microsatellite, chloroplast and nuclear DNA content data we demonstrate the presence of three major evolutionary groups broadly characterized as A. lyrata group, A. halleri group and A. arenosa group. All are composed of further species and sub-species forming larger aggregates. Depending on the resolution of the marker, a few closely related taxa such as A. pedemontana, A. cebennensis and A. croatica are also clearly distinct evolutionary lineages. ITS sequences and a population-based screen based on microsatellites were highly concordant. The major gene pools identified by ITS sequences were also significantly differentiated by their homoploid nuclear DNA content estimated by flow cytometry. The chloroplast genome provided less resolution than the nuclear data, and it remains unclear whether the extensive haplotype sharing apparent between taxa results from gene flow or incomplete lineage sorting in this relatively young group of species with Pleistocene origins.ConclusionsOur study provides a comprehensive overview of the genetic variation within and among the various taxa of the genus Arabidopsis. The resolved gene pools and evolutionary lineages will set the framework for future comparative studies on genetic diversity. Extensive population-based phylogeographic studies will also be required, however, in particular for A. arenosa and their affiliated taxa and cytotypes.

Evolution of cryptic gene pools in Hypericum perforatum: the influence of reproductive system and gene flow

BACKGROUND AND AIMS Hypericum perforatum (St. Johns wort) is a widespread Eurasian perennial plant species with remarkable variation in its morphology, ploidy and breeding system, which ranges from sex to apomixis. Here, hypotheses on the evolutionary origin of St. Johns wort are tested and contrasted with the subsequent history of interspecific gene flow. METHODS Extensive field collections were analysed for quantitative morphological variation, ploidy, chromosome numbers and genetic diversity using nuclear (amplified fragment length polymorphism) and plastid (trnL-trnF) markers. The mode of reproduction was analysed by FCSS (flow cytometric seed screen). KEY RESULTS It is demonstrated that H. perforatum is not of hybrid origin, and for the first time wild diploid populations are documented. Pseudogamous facultative apomictic reproduction is prevalent in the polyploids, whereas diploids are predominantly sexual, a phenomenon which also characterizes its sister species H. maculatum. Both molecular markers characterize identical major gene pools, distinguishing H. perforatum from H. maculatum and two genetic groups in H. perforatum. All three gene pools are in close geographical contact. Extensive gene flow and hybridization throughout Europe within and between gene pools and species is exemplified by the molecular data and confirmed by morphometric analyses. CONCLUSIONS Hypericum perforatum is of a single evolutionary origin and later split into two major gene pools. Subsequently, independent and recurrent polyploidization occurred in all lineages and was accompanied by substantial gene flow within and between H. perforatum and H. maculatum. These processes are highly influenced by the reproductive system in both species, with a switch to predominantly apomictic reproduction in polyploids, irrespective of their origin.

Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids.

Reciprocal crosses between species often display an asymmetry in the fitness of F1 hybrids. This pattern, referred to as isolation asymmetry or Darwins corollary to Haldanes rule, is a general feature of reproductive isolation in plants, yet factors determining its magnitude and direction remain unclear. We evaluated reciprocal species crosses between two naturally hybridizing diploid species of Arabidopsis to assess the degree of isolation asymmetry at different postmating life stages. We found that pollen from Arabidopsis arenosa will usually fertilize ovules from Arabidopsis lyrata; the reverse receptivity being less complete. Maternal A. lyrata parents set more F1 hybrid seed, but germinate at lower frequency, reversing the asymmetry. As predicted by theory, A. lyrata (the maternal parent with lower seed viability in crosses) exhibited accelerated chloroplast evolution, indicating that cytonuclear incompatibilities may play a role in reproductive isolation. However, this direction of asymmetrical reproductive isolation is not replicated in natural suture zones, where delayed hybrid breakdown of fertility at later developmental stages, or later-acting selection against A. arenosa maternal hybrids (unrelated to hybrid fertility, e.g., substrate adaptation) may be responsible for an excess of A. lyrata maternal hybrids. Exogenous selection rather than cytonuclear incompatibilities thus shapes the asymmetrical postmating isolation in nature.

Levels and patterns of genetic diversity differ between two closely related endemic Arabidopsis species

Theory predicts that a small effective population size leads to slower accumulation of mutations, increased levels of genetic drift and reduction in the efficiency of natural selection. Therefore endemic species should harbor low levels of genetic diversity and exhibit a reduced ability of adaptation to environmental changes. Arabidopsis pedemontana and Arabidopsis cebennensis, two endemic species from Italy and France respectively, provide an excellent model to study the adaptive potential of species with small distribution ranges. To evaluate the genome-wide levels and patterns of genetic variation, effective population size and demographic history of both species, we genotyped 53 A. pedemontana and 28 A. cebennensis individuals across the entire species ranges with Genotyping-by-Sequencing. SNPs data confirmed a low genetic diversity for A. pedemontana although its effective population size is relatively high. Only a weak population structure was observed over the small distribution range of A. pedemontana, resulting from an isolation-by-distance pattern of gene flow. In contrary, A. cebennensis individuals clustered in three populations according to their geographic distribution. Despite this and a larger distribution, the overall genetic diversity was even lower for A. cebennensis than for A. pedemontana. A demographic analysis demonstrated that both endemics have undergone a strong population size decline in the past, without recovery. The more drastic decline observed in A. cebennensis partially explains the very small effective population size observed in the present population. In light of these results, we discuss the adaptive potential of these endemic species in the context of rapid climate change.