Klaus Mummenhoff

Molecular phylogenetics, temporal diversification and principles of evolution in the mustard family (Brassicaceae)

Brassicaceae is an important family at both the agronomic and scientific level. The family not only includes several model species, but it is also becoming an evolutionary model at the family level. However, resolving the phylogenetic relationships within the family has been problematic, and a large-scale molecular phylogeny in terms of generic sampling and number of genes is still lacking. In particular, the deeper relationships within the family, for example between the three major recognized lineages, prove particularly hard to resolve. Using a slow-evolving mitochondrial marker (nad4 intron 1), we reconstructed a comprehensive phylogeny in generic representation for the family. In addition, and because resolution was very low in previous single marker phylogenies, we adopted a supermatrix approach by concatenating all checked and reliable sequences available on GenBank as well as new sequences for a total 207 currently recognized genera and eight molecular markers representing a comprehensive coverage of all three genomes. The supermatrix was dated under an uncorrelated relaxed molecular clock using a direct fossil calibration approach. Finally, a lineage-through-time-plot and rates of diversification for the family were generated. The resulting tree, the largest in number of genera and markers sampled to date and covering the whole family in a representative way, provides important insights into the evolution of the family on a broad scale. The backbone of the tree remained largely unresolved and is interpreted as the consequence of early rapid radiation within the family. The age of the family was inferred to be 37.6 (24.2-49.4) Ma, which largely agrees with previous studies. The ages of all major lineages and tribes are also reported. Analysis of diversification suggests that Brassicaceae underwent a rapid period of diversification, after the split with the early diverging tribe Aethionemeae. Given the dates found here, the family appears to have originated under a warm and humid climate approximately 37 Ma. We suggest that the rapid radiation detected was caused by a global cooling during the Oligocene coupled with a genome duplication event. This duplication could have allowed the family to rapidly adapt to the changing climate.

Cabbage family affairs: the evolutionary history of Brassicaceae

Life without the mustard family (Brassicaceae) would be a world without many crop species and the model organism Arabidopsis (Arabidopsis thaliana) that has revolutionized our knowledge in almost every field of modern plant biology. Despite this importance, research breakthroughs in understanding family-wide evolutionary patterns and processes within this flowering plant family were not achieved until the past few years. In this review, we examine recent outcomes from diverse botanical disciplines (taxonomy, systematics, genomics, paleobotany and other fields) to synthesize for the first time a holistic view on the evolutionary history of the mustard family.

Genetic consequences of Pleistocene range shifts: contrast between the Arctic, the Alps and the East African mountains

In wide‐ranging species, the genetic consequences of range shifts in response to climate change during the Pleistocene can be predicted to differ among different parts of the distribution area. We used amplified fragment length polymorphism data to compare the genetic structure of Arabis alpina, a widespread arctic‐alpine and afro‐alpine plant, in three distinct parts of its range: the North Atlantic region, which was recolonized after the last ice age, the European Alps, where range shifts were probably primarily altitudinal, and the high mountains of East Africa, where the contemporary mountain top populations result from range contraction. Genetic structure was inferred using clustering analyses and estimates of genetic diversity within and between populations. There was virtually no diversity in the vast North Atlantic region, which was probably recolonized from a single refugial population, possibly located between the Alps and the northern ice sheets. In the European mountains, genetic diversity was high and distinct genetic groups had a patchy and sometimes disjunct distribution. In the African mountains, genetic diversity was high, clearly structured and partially in accordance with a previous chloroplast phylogeography. The fragmented structure in the European and African mountains indicated that A. alpina disperses little among established populations. Occasional long‐distance dispersal events were, however, suggested in all regions. The lack of genetic diversity in the north may be explained by leading‐edge colonization by this pioneer plant in glacier forelands, closely following the retracting glaciers. Overall, the genetic structure observed corresponded to the expectations based on the environmental history of the different regions.

Three times out of Asia Minor: the phylogeography of Arabis alpina L. (Brassicaceae)

Arabis alpina is a characteristic plant in arctic‐alpine habitats and serves as a classical example to demonstrate biology, ecology and biogeography of arctic‐alpine disjuncts. It has a wider distribution than most other arctic‐alpine plants, covering all European mountain systems, the Canary Islands, North Africa, the high mountains of East Africa and Ethiopia, the Arabian Peninsula and mountain ranges of Central Asia in Iran and Iraq. Additionally it is found in the northern amphi‐Atlantic area including northeastern North America, Greenland, Iceland, Svalbard and northwestern Europe. We used markers from the nuclear (internal transcribed spacer of ribosomal DNA) and chloroplast genome (trnL‐F region) to reconstruct its phylogeographic history. Both markers revealed clear phylogeographic structure. We suggest that A. alpina originated in Asia Minor less than 2 million years ago based on synonymous mutation rates of different genes (plastidic matK, nuclear adh and chs). From the Asian ancestral stock one group migrated via the Arabian Peninsula to the East African high mountains. A second group gave rise to all European and northern populations, and also served as source for the northwest African populations. A third group, which is still centred in Asia, migrated independently southwards and came into secondary contact with the East African lineage in Ethiopia, resulting in high genetic diversity in this area. In the Mediterranean regions, the genetic diversity was relatively high with numerous unique haplotypes, but almost without geographic structure. In contrast, the populations in the northern amphi‐Atlantic area were extremely depauperate, suggesting very recent (postglacial) expansion into this vast area from the south.

Origin and diversification of the Greater Cape flora: Ancient species repository, hot-bed of recent radiation, or both?

Like island-endemic taxa, whose origins are expected to postdate the appearance of the islands on which they occur, biome-endemic taxa should be younger than the biomes to which they are endemic. Accordingly, the ages of biome-endemic lineages may offer insights into biome history. In this study, we used the ages of multiple lineages to explore the origin and diversification of two southern African biomes whose remarkable floristic richness and endemism has identified them as global biodiversity hotspots (succulent karoo and fynbos). We used parsimony optimization to identify succulent karoo- and fynbos-endemic lineages across 17 groups of plants, for which dated phylogenies had been inferred using a relaxed Bayesian (BEAST) approach. All succulent karoo-endemic lineages were less than 17.5 My old, the majority being younger than 10 My. This is largely consistent with suggestions that this biome is the product of recent radiation, probably triggered by climatic deterioration since the late Miocene. In contrast, fynbos-endemic lineages showed a broader age distribution, with some lineages originating in the Oligocene, but most being more recent. Also, in groups having both succulent karoo- and fynbos-endemic lineages, there was a tendency for the latter to be older. These patterns reflect the greater antiquity of fynbos, but also indicate considerable recent speciation, probably through a combination of climatically-induced refugium fragmentation and adaptive radiation.

Molecular Systematics, Evolution, and Population Biology in the Mustard Family (Brassicaceae)

The present review summarizes results from the past decade on the systematics, population genetics, and evolutionary biology of the mustard family, Brassicaceae (Cruciferae). The research of various authors is discussed and presented in the context of ongoing and accumulating studies. The review is useful in view of the immensely increasing work on Arabidopsis thaliana, the model species of plant molecular biology, and on important crop plants such as species of Brassica. Traditional and molecular-based phylogenies are critically discussed, new generic alignments are proposed, and groups in need of molecular studies are identified. Unfortunately, knowledge obtained from molecular genetics and development of A. thaliana is only very slowly creeping into the systematics of Brassicaceae. Future directions of research should move beyond assessing generic relationships or limits, and should also address character development and evolution, the molecular basis of various homoplastic characters, the nature of the genome, and many other new challenges that are emerging from detailed molecular studies of A. thaliana.

Chloroplast DNA phylogeny and biogeography of Lepidium (Brassicaceae)

Two intergenic spacers, trnT-trnL and trnL-trnF, and the trnL intron of cpDNA were sequenced to study phylogenetic relationships and biogeography of 73 Lepidium taxa. Insertions/deletions of ≥3 bp (base pairs) provided reliable phylogenetic information whereas indels ≤2 bp, probably originating from slipped-strand mispairing, are prone to parallelism in the context of our phylogenetic framework. For the first time, an hypothesis of the genus Lepidium is proposed based on molecular phylogeny, in contrast to previous classification schemes into sections and greges (the latter category represents groups of related species within a given geographic region), which are based mainly on fruit characters. Only a few of the taxa as delimited in the traditional systems represent monophyletic lineages. The proposed phylogeny would suggest three main lineages, corresponding to (1) sections Lepia and Cardaria, (2) grex Monoplocoidea from Australia, and (3) remaining taxa, representing the bulk of Lepidium species with more or less resolved sublineages that sometimes represent geographical correspondence. The fossil data, easily dispersible mucilaginous seeds, widespread autogamous breeding systems, and low levels of sequence divergence between species from different continents or islands suggest a rapid radiation of Lepidium by long-distance dispersal in the Pliocene/Pleistocene. As a consequence of climatic changes in this geological epoch, arid/semiarid areas were established, providing favorable conditions for the radiation of Lepidium by which the genus attained its worldwide distribution.

Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region

Sequence data from the nuclear encoded ribosomal internal transcribed spacer (ITS) region were used to determine monophyly of tribes, tribal limits, and tribal relationships of 96 so far unassigned or tentatively assigned genera (represented by 101 taxa/accessions) within the Brassicaceae. Maximum-parsimony and maximum-likelihood analyses of 185 ITS Brassicaceae sequences, which also included representatives of each of the 34 currently recognized tribes, supported the separate phylogenetic distinctness of these tribes and permitted the tribal assignment of all but 12 of the unassigned genera into tribal clades. The data support the recognition of eight new, well-resolved, uni- or oligogeneric tribes recognized herein as the Alyssopsideae [96% bootstrap support (BS); including the central and southwestern Asian Alyssopsis and Calymmatium], Asteae (100% BS; including the Mexican Asta), Eudemeae (97% BS; South American Brayopsis, Eudema, and Xerodraba), Kernereae (96% BS; European Kernera and Rhizobotrya), Notothlaspideae (100% BS; New Zealandic Notothlaspi), Oreophytoneae (100% BS; eastern African Oreophyton and southern European Murbeckiella), and Yinshanieae (100% BS; Chinese Yinshania), as well as the moderately supported Microlepidieae (75% BS; Australian Microlepidium and Carinavalva). Furthermore, the results fully support the recent findings that the tribes Schizopetaleae and Thelypodieae ought to be recognized as two distinct tribes instead of a single tribe, as well as provide some support for the re-establishment of the tribe Cremolobeae, bringing the total number to 44 tribes in the family. Nearly 92% (308) of the 336 genera in the family have been assigned to a tribe. The earlier-published Anastaticeae is taken here to replace the Malcolmieae.

Molecular evidence for bicontinental hybridogenous genomic constitution in Lepidium sensu stricto (Brassicaceae) species from Australia and New Zealand.

Lepidium sensu stricto (s.s.) (Brassicaceae) (ca. 150 species) is distributed worldwide with endemic species on every continent. It is represented in Australia and New Zealand by 19 and seven native species, respectively. In the present study we used a nuclear ribosomal internal transcribed spacer (ITS) phylogeny in comparison with a cpDNA phylogeny to unravel the origin of Australian/New Zealand species. Although phylogenetic relationships within Lepidium s.s. were not fully resolved, the cpDNA data were in agreement with a Californian origin of Lepidium species from Australia/New Zealand. Strongly conflicting signals between the cp- and nuclear DNA phylogenetic analysis clearly indicated hybridogenous genomic constitution of Australian Lepidium s.s. species: All 18 studied Australian/New Zealand Lepidium s.s. species examined shared a Californian cpDNA type. While eleven Australian/New Zealand species appeared to harbor a Californian ITS type, a group of seven species shared a South African ITS type. This pattern is most likely explained by two trans-oceanic dispersals of Lepidium from California and Africa to Australia/New Zealand and subsequent hybridization followed by homogenization of the ribosomal DNA either to the Californian or South African ITS type in the two different lineages. Calibration of our molecular trees indicates a Pliocene/Pleistocene origin of Lepidium in Australia/New Zealand. Low levels of cpDNA and ITS sequence divergence and unresolved topologies within Australian/New Zealand species suggest a rapid and recent radiation of Lepidium after the hybridization event. This coincides with dramatic climatic changes in that geological epoch shaping the composition of the vegetation.

Fast Diploidization in Close Mesopolyploid Relatives of Arabidopsis

The genome evolution of land plants is characterized by multiple waves of whole-genome duplications (WGDs). This cytogenetic and molecular phylogenetic analysis revealed an unexpected WGD event in the ancestry of Australian crucifer species with diploid-like chromosome complements. Mesopolyploid whole-genome duplication (WGD) was revealed in the ancestry of Australian Brassicaceae species with diploid-like chromosome numbers (n = 4 to 6). Multicolor comparative chromosome painting was used to reconstruct complete cytogenetic maps of the cryptic ancient polyploids. Cytogenetic analysis showed that the karyotype of the Australian Camelineae species descended from the eight ancestral chromosomes (n = 8) through allopolyploid WGD followed by the extensive reduction of chromosome number. Nuclear and maternal gene phylogenies corroborated the hybrid origin of the mesotetraploid ancestor and suggest that the hybridization event occurred ~6 to 9 million years ago. The four, five, and six fusion chromosome pairs of the analyzed close relatives of Arabidopsis thaliana represent complex mosaics of duplicated ancestral genomic blocks reshuffled by numerous chromosome rearrangements. Unequal reciprocal translocations with or without preceeding pericentric inversions and purported end-to-end chromosome fusions accompanied by inactivation and/or loss of centromeres are hypothesized to be the main pathways for the observed chromosome number reduction. Our results underline the significance of multiple rounds of WGD in the angiosperm genome evolution and demonstrate that chromosome number per se is not a reliable indicator of ploidy level.