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Model species continue to underpin groundbreaking plant science research. At the same time, the phylogenetic resolution of the land plant tree of life continues to improve. The intersection of these 2 research paths creates a unique opportunity to further extend the usefulness of model species across larger taxonomic groups. Here we promote the utility of the Arabidopsis thaliana model species, especially the ability to connect its genetic and functional resources, to species across the entire Brassicales order. We focus on the utility of using genomics and phylogenomics to bridge the evolution and diversification of several traits across the Brassicales to the resources in Arabidopsis, thereby extending scope from a model species by establishing a "model clade." These Brassicales-wide traits are discussed in the context of both the model species Arabidopsis and the family Brassicaceae. We promote the utility of such a "model clade" and make suggestions for building global networks to support future studies in the model order Brassicales., Competing Interests: Conflict of interest statement. None declared., (© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

The mustard family (Brassicaceae) is a scientifically and economically important family, containing the model plant Arabidopsis thaliana and numerous crop species that feed billions worldwide. Despite its relevance, most phylogenetic trees of the family are incompletely sampled and often contain poorly supported branches. Here, we present the most complete Brassicaceae genus-level family phylogenies to date (Brassicaceae Tree of Life or BrassiToL) based on nuclear (1,081 genes, 319 of the 349 genera; 57 of the 58 tribes) and plastome (60 genes, 265 genera; all tribes) data. We found cytonuclear discordance between the two, which is likely a result of rampant hybridization among closely and more distantly related lineages. To evaluate the impact of such hybridization on the nuclear phylogeny reconstruction, we performed five different gene sampling routines, which increasingly removed putatively paralog genes. Our cleaned subset of 297 genes revealed high support for the tribes, whereas support for the main lineages (supertribes) was moderate. Calibration based on the 20 most clock-like nuclear genes suggests a late Eocene to late Oligocene origin of the family. Finally, our results strongly support a recently published new family classification, dividing the family into two subfamilies (one with five supertribes), together representing 58 tribes. This includes five recently described or re-established tribes, including Arabidopsideae, a monogeneric tribe accommodating Arabidopsis without any close relatives. With a worldwide community of thousands of researchers working on Brassicaceae and its diverse members, our new genus-level family phylogeny will be an indispensable tool for studies on biodiversity and plant biology., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.)

Understanding how populations adapt to abrupt environmental change is necessary to predict responses to future challenges, but identifying specific adaptive variants, quantifying their responses to selection and reconstructing their detailed histories is challenging in natural populations. Here, we use Arabidopsis from the Cape Verde Islands as a model to investigate the mechanisms of adaptation after a sudden shift to a more arid climate. We find genome-wide evidence of adaptation after a multivariate change in selection pressures. In particular, time to flowering is reduced in parallel across islands, substantially increasing fitness. This change is mediated by convergent de novo loss of function of two core flowering time genes: FRI on one island and FLC on the other. Evolutionary reconstructions reveal a case where expansion of the new populations coincided with the emergence and proliferation of these variants, consistent with models of rapid adaptation and evolutionary rescue., (© 2022. The Author(s).)

Many model organisms were chosen and achieved prominence because of an advantageous combination of their life-history characteristics, genetic properties and also practical considerations. Discoveries made in Arabidopsis thaliana, the most renowned noncrop plant model species, have markedly stimulated studies in other species with different biology. Within the family Brassicaceae, the arctic-alpine Arabis alpina has become a model complementary to Arabidopsis thaliana to study the evolution of life-history traits, such as perenniality, and ecological genomics in harsh environments. In this review, we provide an overview of the properties that facilitated the rapid emergence of A. alpina as a plant model. We summarize the evolutionary history of A. alpina, including genomic aspects, the diversification of its mating system and demographic properties, and we discuss recent progress in the molecular dissection of developmental traits that are related to its perennial life history and environmental adaptation. From this published knowledge, we derive open questions that might inspire future research in A. alpina, other Brassicaceae species or more distantly related plant families., (© 2021 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.)

Arabidopsis thaliana is one of the prevailing plant model systems used for most facets of plant molecular, cell, and evolutionary biology. There are good reasons for that, such as easy cultivation, short generation time, a selfing reproductive system, and a wide geographic distribution with easy access to respective germplasm material. For the last two decades, the entire genus Arabidopsis with its various species has emerged as a model system allowing the study of additional traits and characters not found in A. thaliana. These species grow naturally under very different environmental conditions and mostly underwent independent evolutionary histories. Accordingly, consideration of their respective biogeographic and phylogenetic (taxonomic) context is important for any study aiming to explore fully the potential of comparative studies. Here, we review current understanding of spatio-temporal patterns of Arabidopsis evolutionary history and introduce the various taxa in more detail, including those traits well studied by the scientific community. The significance of polyploidization and interspecies gene flow is also discussed.

Edaphic conditions are important determinants of plant fitness. While much has been learnt in recent years about plant adaptation to heavy metal contaminated soils, the genomic basis underlying adaptation to calcareous and siliceous substrates remains largely unknown. We performed a reciprocal germination experiment and whole-genome resequencing in natural calcareous and siliceous populations of diploid Arabidopsis lyrata to test for edaphic adaptation and detect signatures of selection at loci associated with soil-mediated divergence. In parallel, genome scans on respective diploid ecotypes from the Arabidopsis arenosa species complex were undertaken, to search for shared patterns of adaptive genetic divergence. Soil ecotypes of A. lyrata display significant genotype-by-treatment responses for seed germination. Sequence (SNPs) and copy-number variants (CNVs) point towards loci involved in ion transport as the main targets of adaptive genetic divergence. Two genes exhibiting high differentiation among soil types in A. lyrata further share trans-specific single nucleotide polymorphisms with A. arenosa. This work applies experimental and genomic approaches to study edaphic adaptation in A. lyrata and suggests that physiological response to elemental toxicity and deficiency underlies the evolution of calcareous and siliceous ecotypes. The discovery of shared adaptive variation between sister species indicates that ancient polymorphisms contribute to adaptive evolution., (© 2018 John Wiley & Sons Ltd.)

Background: Genome scans based on outlier analyses have revolutionized detection of genes involved in adaptive processes, but reports of some forms of selection, such as balancing selection, are still limited. It is unclear whether high throughput genotyping approaches for identification of single nucleotide polymorphisms have sufficient power to detect modes of selection expected to result in reduced genetic differentiation among populations. In this study, we used Arabidopsis lyrata to investigate whether signatures of balancing selection can be detected based on genomic smoothing of Restriction Associated DNA sequencing (RAD-seq) data. We compared how different sampling approaches (both within and between subspecies) and different background levels of polymorphism (inbreeding or outcrossing populations) affected the ability to detect genomic regions showing key signatures of balancing selection, specifically elevated polymorphism, reduced differentiation and shifts towards intermediate allele frequencies. We then tested whether candidate genes associated with disease resistance (R-gene analogs) were detected more frequently in these regions compared to other regions of the genome., Results: We found that genomic regions showing elevated polymorphism contained a significantly higher density of R-gene analogs predicted to be under pathogen-mediated selection than regions of non-elevated polymorphism, and that many of these also showed evidence for an intermediate site-frequency spectrum based on Tajima's D. However, we found few genomic regions that showed both elevated polymorphism and reduced F ST among populations, despite strong background levels of genetic differentiation among populations. This suggests either insufficient power to detect the reduced population structure predicted for genes under balancing selection using sparsely distributed RAD markers, or that other forms of diversifying selection are more common for the R-gene analogs tested., Conclusions: Genome scans based on a small number of individuals sampled from a wide range of populations were sufficient to confirm the relative scarcity of signatures of balancing selection across the genome, but also identified new potential disease resistance candidates within genomic regions showing signatures of balancing selection that would be strong candidates for further sequencing efforts.

Background: Gene flow between species, across ploidal levels, and even between evolutionary lineages is a common phenomenon in the genus Arabidopsis. However, apart from two genetically fully stabilized allotetraploid species that have been investigated in detail, the extent and temporal dynamics of hybridization are not well understood. An introgression zone, with tetraploid A. arenosa introgressing into A. lyrata subsp. petraea in the Eastern Austrian Forealps and subsequent expansion towards pannonical lowlands, was described previously based on morphological observations as well as molecular data using microsatellite and plastid DNA markers. Here we investigate the spatio-temporal context of this suture zone, making use of the potential of next-generation sequencing and whole-genome data. By utilizing a combination of nuclear and plastid genomic data, the extent, direction and temporal dynamics of gene flow are elucidated in detail and Late Pleistocene evolutionary processes are resolved., Results: Analysis of nuclear genomic data significantly recognizes the clinal structure of the introgression zone, but also reveals that hybridization and introgression is more common and substantial than previously thought. Also tetraploid A. lyrata and A. arenosa subsp. borbasii from outside the previously defined suture zone show genomic signals of past introgression. A. lyrata is shown to serve usually as the maternal parent in these hybridizations, but one exception is identified from plastome-based phylogenetic reconstruction. Using plastid phylogenomics with secondary time calibration, the origin of A. lyrata and A. arenosa lineages is pre-dating the last three glaciation complexes (approx. 550,000 years ago). Hybridization and introgression followed during the last two glacial-interglacial periods (since approx. 300,000 years ago) with later secondary contact at the northern and southern border of the introgression zone during the Holocene., Conclusions: Footprints of adaptive introgression in the Northeastern Forealps are older than expected and predate the Last Glaciation Maximum. This correlates well with high genetic diversity found within areas that served as refuge area multiple times. Our data also provide some first hints that early introgressed and presumably preadapted populations account for successful and rapid postglacial re-colonization and range expansion.

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.

Results of research in life sciences acquire a deeper meaning if they can also be discussed in temporal contexts of evolution. Despite the importance of the mustard family (Brassicaceae) as a prominent angiosperm model family, a robust, generally accepted hypothesis for a family-wide temporal framework does not yet exist. The main cause for this situation is a poor fossil record of the family. We suggest that the few known fossils require a critical re-evaluation of phylogenetic and temporal assignments as a prerequisite for appropriate molecular dating analyses within the family. In addition, (palaeo)biogeographical calibrations, not explored so far in the family, should be integrated in a synthesis of various dating approaches, with each contributing their specific possibilities and limitations., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Background: Wild 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., Results: Based 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., Conclusions: Our 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.

The Arabidopsis arenosa complex is closely related to the model plant Arabidopsis thaliana. Species and subspecies in the complex are mainly biennial, predominantly outcrossing, herbaceous, and with a distribution range covering most parts of latitudes and the eastern reaches of Europe. In this study we present the first comprehensive evolutionary history of the A. arenosa species complex, covering its natural range, by using chromosome counts, nuclear AFLP data, and a maternally inherited marker from the chloroplast genome [trnL intron (trnL) and trnL/F intergenic spacer (trnL/F-IGS) of tRNA(Leu) and tRNA(Phe), respectively]. We unravel the broad-scale cytogeographic and phylogeographic patterns of diploids and tetraploids. Diploid cytotypes were exclusively found on the Balkan Peninsula and in the Carpathians while tetraploid cytotypes were found throughout the remaining distribution range of the A. arenosa complex. Three centers of genetic diversity were identified: the Balkan Peninsula, the Carpathians, and the unglaciated Eastern and Southeastern Alps. All three could have served as long-term refugia during Pleistocene climate oscillations. We hypothesize that the Western Carpathians were and still are the cradle of speciation within the A. arenosa complex due to the high species number and genetic diversity and the concurrence of both cytotypes there.

Background: Effects of polyploidisation on gene flow between natural populations are little known. Central European diploid and tetraploid populations of Arabidopsis arenosa and A. lyrata are here used to study interspecific and interploidal gene flow, using a combination of nuclear and plastid markers., Results: Ploidal levels were confirmed by flow cytometry. Network analyses clearly separated diploids according to species. Tetraploids and diploids were highly intermingled within species, and some tetraploids intermingled with the other species, as well. Isolation with migration analyses suggested interspecific introgression from tetraploid A. arenosa to tetraploid A. lyrata and vice versa, and some interploidal gene flow, which was unidirectional from diploid to tetraploid in A. arenosa and bidirectional in A. lyrata., Conclusions: Interspecific genetic isolation at diploid level combined with introgression at tetraploid level indicates that polyploidy may buffer against negative consequences of interspecific hybridisation. The role of introgression in polyploid systems may, however, differ between plant species, and even within the small genus Arabidopsis, we find very different evolutionary fates when it comes to introgression.

The genus Arabidopsis provides a unique opportunity to study fundamental biological questions in plant sciences using the diploid model species Arabidopsis thaliana and Arabidopsis lyrata. However, only a few studies have focused on introgression and hybrid speciation in Arabidopsis, although polyploidy is a common phenomenon within this genus. More recently, there is growing evidence of significant gene flow between the various Arabidopsis species. So far, we know Arabidopsis suecica and Arabidopsis kamchatica as fully stabilized allopolyploid species. Both species evolved during Pleistocene glaciation and deglaciation cycles in Fennoscandinavia and the amphi-Beringian region, respectively. These hybrid studies were conducted either on a phylogeographic scale or reconstructed experimentally in the laboratory. In our study we focus at a regional and population level. Our research area is located in the foothills of the eastern Austrian Alps, where two Arabidopsis species, Arabidopsis arenosa and A. lyrata ssp. petraea, are sympatrically distributed. Our hypothesis of genetic introgression, migration, and adaptation to the changing environment during the Pleistocene has been confirmed: We observed significant, mainly unidirectional gene flow between the two species, which has given rise to the tetraploid A. lyrata. This cytotype was able to escape from the narrow ecological niche occupied by diploid A. lyrata ssp. petraea on limestone outcrops by migrating northward into siliceous areas, leaving behind a trail of genetic differentiation.

Background: The genomes of higher plants are, on the majority, polyploid, and hybridisation is more frequent in plants than in animals. Both polyploidisation and hybridisation contribute to increased variability within species, and may transfer adaptations between species in a changing environment. Studying these aspects of evolution within a diversified species complex could help to clarify overall spatial and temporal patterns of plant speciation. The Arabidopsis lyrata complex, which is closely related to the model plant Arabidopsis thaliana, is a perennial, outcrossing, herbaceous species complex with a circumpolar distribution in the Northern Hemisphere as well as a disjunct Central European distribution in relictual habitats. This species complex comprises three species and four subspecies, mainly diploids but also several tetraploids, including one natural hybrid. The complex is ecologically, but not fully geographically, separated from members of the closely related species complex of Arabidopsis halleri, and the evolutionary histories of both species compexes have largely been influenced by Pleistocene climate oscillations., Results: Using DNA sequence data from the nuclear encoded cytosolic phosphoglucoisomerase and Internal Transcribed Spacers 1 and 2 of the ribosomal DNA, as well as the trnL/F region from the chloroplast genome, we unravelled the phylogeography of the various taxonomic units of the A. lyrata complex. We demonstrate the existence of two major gene pools in Central Europe and Northern America. These two major gene pools are constructed from different taxonomic units. We also confirmed that A. kamchatica is the allotetraploid hybrid between A. lyrata and A. halleri, occupying the amphi-Beringian area in Eastern Asia and Northern America. This species closes the large distribution gap of the various other A. lyrata segregates. Furthermore, we revealed a threefold independent allopolyploid origin of this hybrid species in Japan, China, and Kamchatka., Conclusions: Unglaciated parts of the Eastern Austrian Alps and arctic Eurasia, including Beringia, served as major glacial refugia of the Eurasian A. lyrata lineage, whereas A. halleri and its various subspecies probably survived in refuges in Central Europe and Eastern Asia with a large distribution gap in between. The North American A. lyrata lineage probably survived the glaciation in the southeast of North America. The dramatic climatic changes during glaciation and deglaciation cycles promoted not only secondary contact and formation of the allopolyploid hybrid A. kamchatica, but also provided the environment that allowed this species to fill a large geographic gap separating the two genetically different A. lyrata lineages from Eurasia and North America. With our example focusing on the evolutionary history of the A. lyrata species complex, we add substantial information to a broad evolutionary framework for future investigations within this emerging model system in molecular and evolutionary biology.

Arabidopsis thaliana is one of the most intensively studied plant species. More recently, information is accumulating about its closest relatives, the former genus Cardaminopsis. A. thaliana diverged from these relatives, actually treated within three major lineages (Arabidopsis lyrata, Arabidopsis halleri, and Arabidopsis arenosa), approximately 5 mya. Significant karyotype evolution in A. thaliana with base chromosome number reduction from x=8 to x=5 might indicate and favor effective genetic isolation from these other species, although hybrids are occurring naturally and have been also constituted under controlled conditions. We tested the evolutionary significance to separate the x=5 from the x=8 lineage using DNA sequence data from the plastome and the nuclear ribosomal DNA based on an extensive, representative worldwide sampling of nearly all taxonomic entities. We conclude that (i) A. thaliana is clearly separated phylogenetically from the x=8 lineage, (ii) five major lineages outside A. thaliana can be identified (A. lyrata, A. arenosa, A. halleri, Arabidopsis croatica, and Arabidopsis pedemontana) together with Arabidopsis cebennensis, and (iii) centers of genetic and morphological diversity are mostly in congruence and are located close to the Balkans in Austria and Slovakia outside glaciated and permafrost regions with few notable exceptions.

Non-model Arabidopsis species have been widely used as outgroup taxa in studies of molecular evolution. In Arabidopsis lyrata, Arabidopsis halleri and Arabidopsis arenosa, traits pertaining to self-incompatibility, heavy metal tolerance and inter-specific hybridization have been subjected to detailed genetic analysis. However, the full potential for exploring the causes and consequences of natural variation in complex traits within the genus Arabidopsis has not been widely appreciated or realized. Here, we draw on broadly dispersed information to characterize the basic biology, ecology, population genetics and molecular evolution for these three non-model Arabidopsis species. We illustrate how the wealth of functional and genomic tools pioneered in A. thaliana can be applied to gain insights into adaptive evolution of ecologically important traits and genome-wide processes, such as polyploidy, speciation and reticulate evolution, within and among Arabidopsis species.

Recently, we used the 5'-trnL(UAA)-trnF(GAA) region of the chloroplast DNA for phylogeographic reconstructions and phylogenetic analysis among the genera Arabidopsis, Boechera, Rorippa, Nasturtium, and Cardamine. Despite the fact that extensive gene duplications are rare among the chloroplast genome of higher plants, within these taxa the anticodon domain of the trnF(GAA) gene exhibit extensive gene duplications with one to eight tandemly repeated copies in close 5' proximity of the functional gene. Interestingly, even in Arabidopsis thaliana we found six putative pseudogenic copies of the functional trnF gene within the 5'-intergenic trnL-trnF spacer. A reexamination of trnL(UAA)-trnF(GAA) regions from numerous published phylogenetic studies among halimolobine, cardaminoid, and other cruciferous taxa revealed not only extensive trnF gene duplications but also favor the hypothesis about a single origin of trnF pseudogene formation during evolution of the Brassicaceae family 16-21 MYA. Conserved sequence motifs from this tandemly repeated region are codistributed nonrandomly throughout the plastome, and we found some similarities with a DNA sequence duplication in the rps7 gene and its adjacent spacer. Our results demonstrate the potential evolutionary dynamics of a plastidic region generally regarded as highly conserved and probably cotranscribed and, as shown here for several genera among cruciferous plants, greatly characterized by parallel gains and losses of duplicated trnF copies.