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      Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle-Atlantic island lineages

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          Abstract

          Background

          Tribe Fabeae comprises about 380 legume species, including some of the most ancient and important crops like lentil, pea, and broad bean. Breeding efforts in legume crops rely on a detailed knowledge of closest wild relatives and geographic origin. Relationships within the tribe, however, are incompletely known and previous molecular results conflicted with the traditional morphology-based classification. Here we analyse the systematics, biogeography, and character evolution in the tribe based on plastid and nuclear DNA sequences.

          Results

          Phylogenetic analyses including c. 70% of the species in the tribe show that the genera Vicia and Lathyrus in their current circumscription are not monophyletic: Pisum and Vavilovia are nested in Lathyrus, the genus Lens is nested in Vicia. A small, well-supported clade including Vicia hirsuta, V. sylvatica, and some Mediterranean endemics, is the sister group to all remaining species in the tribe. Fabeae originated in the East Mediterranean region in the Miocene (23–16 million years ago (Ma)) and spread at least 39 times into Eurasia, seven times to the Americas, twice to tropical Africa and four times to Macaronesia. Broad bean ( V. faba) and its sister V. paucijuga originated in Asia and might be sister to V. oroboides. Lentil ( Lens culinaris ssp. culinaris) is of Mediterranean origin and together with eight very close relatives forms a clade that is nested in the core Vicia, where it evolved c. 14 Ma. The Pisum clade is nested in Lathyrus in a grade with the Mediterranean L. gloeosperma, L. neurolobus, and L. nissolia. The extinct Azorean endemic V. dennesiana belongs in section Cracca and is nested among Mediterranean species. According to our ancestral character state reconstruction results, ancestors of Fabeae had a basic chromosome number of 2n=14, an annual life form, and evenly hairy, dorsiventrally compressed styles.

          Conclusions

          Fabeae evolved in the Eastern Mediterranean in the middle Miocene and spread from there across Eurasia, into Tropical Africa, and at least seven times to the Americas. The middle-Atlantic islands were colonized four times but apparently did not serve as stepping-stones for Atlantic crossings. Long-distance dispersal events are relatively common in Fabeae (seven per ten million years). Current generic and infrageneric circumscriptions in Fabeae do not reflect monophyletic groups and should be revised. Suggestions for generic level delimitation are offered.

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          Most cited references 36

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          Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae).

          The coding region of the mat K gene and two intergenic spacers, psb A-trn H and trn L(UAA)-trn F(GAA), of cpDNA were sequenced to study phylogenetic relationships of 32 Paeonia species. In the psb A-trn H intergenic spacer, short sequences bordered by long inverted repeats have undergone inversions that are often homoplasious mutations. Insertions/deletions found in the two intergenic spacers, mostly resulting from slipped-strand mispairing, provided relatively reliable phylogenetic information. The mat K coding region, evolving more rapidly than the trnL-trn F spacer and more slowly than the psb A-trn H spacer, produced the best resolved phylogenetic tree. The mat K phylogeny was compared with the phylogeny obtained from sequences of internal transcribed spacers (ITS) of nuclear ribosomal DNA. A refined hypothesis of species phylogeny of section Paeonia was proposed by considering the discordance between the nuclear and cpDNA phylogenies to be results of hybrid speciation followed by inheritance of cpDNA of one parent and fixation of ITS sequences of another parent. The Eurasian and western North American disjunct distribution of the genus may have resulted from interrruption of the continuous distribution of ancestral populations of extant peony species across the Bering land bridge during the Miocene. Pleistocene glaciation may have played an important role in triggering extensive reticulate evolution within section Paeonia and shifting distributional ranges of both parental and hybrid species.
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            Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire.

            The relative importance of local ecological and larger-scale historical processes in causing differences in species richness across the globe remains keenly debated. To gain insight into these questions, we investigated the assembly of plant diversity in the Cerrado in South America, the world's most species-rich tropical savanna. Time-calibrated phylogenies suggest that Cerrado lineages started to diversify less than 10 Mya, with most lineages diversifying at 4 Mya or less, coinciding with the rise to dominance of flammable C4 grasses and expansion of the savanna biome worldwide. These plant phylogenies show that Cerrado lineages are strongly associated with adaptations to fire and have sister groups in largely fire-free nearby wet forest, seasonally dry forest, subtropical grassland, or wetland vegetation. These findings imply that the Cerrado formed in situ via recent and frequent adaptive shifts to resist fire, rather than via dispersal of lineages already adapted to fire. The location of the Cerrado surrounded by a diverse array of species-rich biomes, and the apparently modest adaptive barrier posed by fire, are likely to have contributed to its striking species richness. These findings add to growing evidence that the origins and historical assembly of species-rich biomes have been idiosyncratic, driven in large part by unique features of regional- and continental-scale geohistory and that different historical processes can lead to similar levels of modern species richness.
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              Localized hypermutation and associated gene losses in legume chloroplast genomes.

              Point mutations result from errors made during DNA replication or repair, so they are usually expected to be homogeneous across all regions of a genome. However, we have found a region of chloroplast DNA in plants related to sweetpea (Lathyrus) whose local point mutation rate is at least 20 times higher than elsewhere in the same molecule. There are very few precedents for such heterogeneity in any genome, and we suspect that the hypermutable region may be subject to an unusual process such as repeated DNA breakage and repair. The region is 1.5 kb long and coincides with a gene, ycf4, whose rate of evolution has increased dramatically. The product of ycf4, a photosystem I assembly protein, is more divergent within the single genus Lathyrus than between cyanobacteria and other angiosperms. Moreover, ycf4 has been lost from the chloroplast genome in Lathyrus odoratus and separately in three other groups of legumes. Each of the four consecutive genes ycf4-psaI-accD-rps16 has been lost in at least one member of the legume "inverted repeat loss" clade, despite the rarity of chloroplast gene losses in angiosperms. We established that accD has relocated to the nucleus in Trifolium species, but were unable to find nuclear copies of ycf4 or psaI in Lathyrus. Our results suggest that, as well as accelerating sequence evolution, localized hypermutation has contributed to the phenomenon of gene loss or relocation to the nucleus.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2012
                25 December 2012
                : 12
                : 250
                Affiliations
                [1 ]Plant Biodiversity Research, Technische Universität München, Maximus-von-Imhof Forum 2, Freising, D-85354, Germany
                [2 ]Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, United Kingdom
                [3 ]Unidad de Botánica (ICIA). C/Retama, 2, 38400, Puerto de La Cruz, Tenerife, Islas, Canarias, Spain
                [4 ]Universidade da Madeira, Centro de Ciências da Vida, Funchal, Madeira, Portugal
                [5 ]Plants Division, Department of Life Sciences, The Natural History Museum, Cromwell Road, London, SW7 5BD, United Kingdom
                Article
                1471-2148-12-250
                10.1186/1471-2148-12-250
                3547781
                23267563
                Copyright ©2012 Schaefer et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Categories
                Research Article

                Evolutionary Biology

                lathyrus, legumes, lentil, long-distance dispersal, macaronesia, pea, pisum, vicia

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