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1.  Chloroplast genes as genetic markers for inferring patterns of change, maternal ancestry and phylogenetic relationships among Eleusine species 
AoB Plants  2013;6:plt056.
Phylogenetic relationship between the nine species of Eleusine was investigated based on RFLP of the seven amplified chloroplast genes/intergenic spacers, trnK gene sequence and cpSSR markers. The maternal genome donor (E. indica, 2n=2x=18) of the allotetraploid (2n=4x=36, 2n=2x=38) Eleusine species, and the phylogenetic relationships between cultivated E. coracana (2n=4x=36) and wild species have been successfully resolved. The species-specific markers were also identified. The explicit identification of the maternal parent and that of the immediate wild progenitor of finger millet will be immensely useful for future genetic improvement and biotechnological program(s) of the crop species.
Assessment of phylogenetic relationships is an important component of any successful crop improvement programme, as wild relatives of the crop species often carry agronomically beneficial traits. Since its domestication in East Africa, Eleusine coracana (2n = 4x = 36), a species belonging to the genus Eleusine (x = 8, 9, 10), has held a prominent place in the semi-arid regions of India, Nepal and Africa. The patterns of variation between the cultivated and wild species reported so far and the interpretations based upon them have been considered primarily in terms of nuclear events. We analysed, for the first time, the phylogenetic relationship between finger millet (E. coracana) and its wild relatives by species-specific chloroplast deoxyribonucleic acid (cpDNA) polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) and chloroplast simple sequence repeat (cpSSR) markers/sequences. Restriction fragment length polymorphism of the seven amplified chloroplast genes/intergenic spacers (trnK, psbD, psaA, trnH–trnK, trnL–trnF, 16S and trnS–psbC), nucleotide sequencing of the chloroplast trnK gene and chloroplast microsatellite polymorphism were analysed in all nine known species of Eleusine. The RFLP of all seven amplified chloroplast genes/intergenic spacers and trnK gene sequences in the diploid (2n = 16, 18, 20) and allotetraploid (2n = 36, 38) species resulted in well-resolved phylogenetic trees with high bootstrap values. Eleusine coracana, E. africana, E. tristachya, E. indica and E. kigeziensis did not show even a single change in restriction site. Eleusine intermedia and E. floccifolia were also shown to have identical cpDNA fragment patterns. The cpDNA diversity in Eleusine multiflora was found to be more extensive than that of the other eight species. The trnK gene sequence data complemented the results obtained by PCR–RFLP. The maternal lineage of all three allotetraploid species (AABB, AADD) was the same, with E. indica being the maternal diploid progenitor species. The markers specific to certain species were also identified.
doi:10.1093/aobpla/plt056
PMCID: PMC3924058  PMID: 24790119
cpSSR; Eleusine; PCR–RFLP; phylogeny; Poaceae; trnK gene sequence.
2.  Infrageneric Phylogeny and Temporal Divergence of Sorghum (Andropogoneae, Poaceae) Based on Low-Copy Nuclear and Plastid Sequences 
PLoS ONE  2014;9(8):e104933.
The infrageneric phylogeny and temporal divergence of Sorghum were explored in the present study. Sequence data of two low-copy nuclear (LCN) genes, phosphoenolpyruvate carboxylase 4 (Pepc4) and granule-bound starch synthase I (GBSSI), from 79 accessions of Sorghum plus Cleistachne sorghoides together with those from outgroups were used for maximum likelihood (ML) and Bayesian inference (BI) analyses. Bayesian dating based on three plastid DNA markers (ndhA intron, rpl32-trnL, and rps16 intron) was used to estimate the ages of major diversification events in Sorghum. The monophyly of Sorghum plus Cleistachne sorghoides (with the latter nested within Sorghum) was strongly supported by the Pepc4 data using BI analysis, and the monophyly of Sorghum was strongly supported by GBSSI data using both ML and BI analyses. Sorghum was divided into three clades in the Pepc4, GBSSI, and plastid phylograms: the subg. Sorghum lineage; the subg. Parasorghum and Stiposorghum lineage; and the subg. Chaetosorghum and Heterosorghum lineage. Two LCN homoeologous loci of Cleistachne sorghoides were first discovered in the same accession. Sorghum arundinaceum, S. bicolor, S. x drummondii, S. propinquum, and S. virgatum were closely related to S. x almum in the Pepc4, GBSSI, and plastid phylograms, suggesting that they may be potential genome donors to S. almum. Multiple LCN and plastid allelic variants have been identified in S. halepense of subg. Sorghum. The crown ages of Sorghum plus Cleistachne sorghoides and subg. Sorghum are estimated to be 12.7 million years ago (Mya) and 8.6 Mya, respectively. Molecular results support the recognition of three distinct subgenera in Sorghum: subg. Chaetosorghum with two sections, each with a single species, subg. Parasorghum with 17 species, and subg. Sorghum with nine species and we also provide a new nomenclatural combination, Sorghum sorghoides.
doi:10.1371/journal.pone.0104933
PMCID: PMC4133246  PMID: 25122516
3.  Analysis of Complete Nucleotide Sequences of 12 Gossypium Chloroplast Genomes: Origin and Evolution of Allotetraploids 
PLoS ONE  2012;7(8):e37128.
Background
Cotton (Gossypium spp.) is a model system for the analysis of polyploidization. Although ascertaining the donor species of allotetraploid cotton has been intensively studied, sequence comparison of Gossypium chloroplast genomes is still of interest to understand the mechanisms underlining the evolution of Gossypium allotetraploids, while it is generally accepted that the parents were A- and D-genome containing species. Here we performed a comparative analysis of 13 Gossypium chloroplast genomes, twelve of which are presented here for the first time.
Methodology/Principal Findings
The size of 12 chloroplast genomes under study varied from 159,959 bp to 160,433 bp. The chromosomes were highly similar having >98% sequence identity. They encoded the same set of 112 unique genes which occurred in a uniform order with only slightly different boundary junctions. Divergence due to indels as well as substitutions was examined separately for genome, coding and noncoding sequences. The genome divergence was estimated as 0.374% to 0.583% between allotetraploid species and A-genome, and 0.159% to 0.454% within allotetraploids. Forty protein-coding genes were completely identical at the protein level, and 20 intergenic sequences were completely conserved. The 9 allotetraploids shared 5 insertions and 9 deletions in whole genome, and 7-bp substitutions in protein-coding genes. The phylogenetic tree confirmed a close relationship between allotetraploids and the ancestor of A-genome, and the allotetraploids were divided into four separate groups. Progenitor allotetraploid cotton originated 0.43–0.68 million years ago (MYA).
Conclusion
Despite high degree of conservation between the Gossypium chloroplast genomes, sequence variations among species could still be detected. Gossypium chloroplast genomes preferred for 5-bp indels and 1–3-bp indels are mainly attributed to the SSR polymorphisms. This study supports that the common ancestor of diploid A-genome species in Gossypium is the maternal source of extant allotetraploid species and allotetraploids have a monophyletic origin. G. hirsutum AD1 lineages have experienced more sequence variations than other allotetraploids in intergenic regions. The available complete nucleotide sequences of 12 Gossypium chloroplast genomes should facilitate studies to uncover the molecular mechanisms of compartmental co-evolution and speciation of Gossypium allotetraploids.
doi:10.1371/journal.pone.0037128
PMCID: PMC3411646  PMID: 22876273
4.  Genetic diversity in tef [Eragrostis tef (Zucc.) Trotter] 
Tef [Eragrostis tef (Zucc.) Trotter] is a cereal crop resilient to adverse climatic and soil conditions, and possessing desirable storage properties. Although tef provides high quality food and grows under marginal conditions unsuitable for other cereals, it is considered to be an orphan crop because it has benefited little from genetic improvement. Hence, unlike other cereals such as maize and wheat, the productivity of tef is extremely low. In spite of the low productivity, tef is widely cultivated by over six million small-scale farmers in Ethiopia where it is annually grown on more than three million hectares of land, accounting for over 30% of the total cereal acreage. Tef, a tetraploid with 40 chromosomes (2n = 4x = 40), belongs to the family Poaceae and, together with finger millet (Eleusine coracana Gaerth.), to the subfamily Chloridoideae. It was originated and domesticated in Ethiopia. There are about 350 Eragrostis species of which E. tef is the only species cultivated for human consumption. At the present time, the gene bank in Ethiopia holds over five thousand tef accessions collected from geographical regions diverse in terms of climate and elevation. These germplasm accessions appear to have huge variability with regard to key agronomic and nutritional traits. In order to properly utilize the variability in developing new tef cultivars, various techniques have been implemented to catalog the extent and unravel the patterns of genetic diversity. In this review, we show some recent initiatives investigating the diversity of tef using genomics, transcriptomics and proteomics and discuss the prospect of these efforts in providing molecular resources that can aid modern tef breeding.
doi:10.3389/fpls.2015.00177
PMCID: PMC4374454  PMID: 25859251
Eragrostis tef; diversity; genomics; proteomics; tef; transcriptomics; variability
5.  A DNA Barcoding Method to Discriminate between the Model Plant Brachypodium distachyon and Its Close Relatives B. stacei and B. hybridum (Poaceae) 
PLoS ONE  2012;7(12):e51058.
Background
Brachypodium distachyon s. l. has been widely investigated across the world as a model plant for temperate cereals and biofuel grasses. However, this annual plant shows three cytotypes that have been recently recognized as three independent species, the diploids B. distachyon (2n = 10) and B. stacei (2n = 20) and their derived allotetraploid B. hybridum (2n = 30).
Methodology/Principal Findings
We propose a DNA barcoding approach that consists of a rapid, accurate and automatable species identification method using the standard DNA sequences of complementary plastid (trnLF) and nuclear (ITS, GI) loci. The highly homogenous but largely divergent B. distachyon and B. stacei diploids could be easily distinguished (100% identification success) using direct trnLF (2.4%), ITS (5.5%) or GI (3.8%) sequence divergence. By contrast, B. hybridum could only be unambiguously identified through the use of combined trnLF+ITS sequences (90% of identification success) or by cloned GI sequences (96.7%) that showed 5.4% (ITS) and 4% (GI) rate divergence between the two parental sequences found in the allopolyploid.
Conclusion/Significance
Our data provide an unbiased and effective barcode to differentiate these three closely-related species from one another. This procedure overcomes the taxonomic uncertainty generated from methods based on morphology or flow cytometry identifications that have resulted in some misclassifications of the model plant and its allies. Our study also demonstrates that the allotetraploid B. hybridum has resulted from bi-directional crosses of B. distachyon and B. stacei plants acting either as maternal or paternal parents.
doi:10.1371/journal.pone.0051058
PMCID: PMC3519806  PMID: 23240000
6.  Origins and diversity of a cosmopolitan fern genus on an island archipelago 
AoB Plants  2015;7:plv118.
Isolated oceanic islands are characterized by patterns of biological diversity different from those on continents. Nucleotide sequences from chloroplast and nuclear genes were used to examine the origins and diversity of the cosmopolitan fern genus Pteridium on the Galapagos Islands. We found evidence for multiple origins of the widespread allotetraploid P. caudatum. We also show that the Galapagos Islands are home to P. caudatum as well as diploid P. esculentum subsp. arachnoideum and possible hybrids between the two. Haplotype diversity indicates that Pteridium has colonized the islands multiple times and probably from diverse mainland sources.
Isolated oceanic islands are characterized by patterns of biological diversity different from that on nearby continental mainlands. Isolation can provide the opportunity for evolutionary divergence, but also set the stage for hybridization between related taxa arriving from different sources. Ferns disperse by haploid spores, which are produced in large numbers and can travel long distances in air currents, enabling these plants to become established on most oceanic islands. Here, we examine the origins and patterns of diversity of the cosmopolitan fern genus Pteridium (Dennstaedtiaceae; bracken) on the Galapagos Islands. We use nucleotide sequences from two plastid genes, and two nuclear gene markers, to examine phylogeography of Pteridium on the Galapagos Islands. We incorporate data from a previous study to provide a worldwide context. We also sampled new specimens from South and Central America. We used flow cytometry to estimate genome size of some accessions. We found that both plastid and nuclear haplotypes fall into two distinct clades, consistent with a two-diploid-species taxonomy of P. aquilinum and P. esculentum. As predicted, the allotetraploid P. caudatum possesses nuclear haplotypes from both diploid species. Samples from the Galapagos include P. esculentum subsp. arachnoideum, P. caudatum and possible hybrids between them. Multiple Pteridium taxa were also observed growing together at some sites. We find evidence for multiple origins of Pteridium on the Galapagos Islands and multiple origins of tetraploid P. caudatum throughout its range in Central and South America. We also posit that P. caudatum may include recent diploid hybrids, backcrosses to P. esculentum, as well as allotetraploid plants. The Galapagos Islands are positioned close to the equator where they can receive dispersing propagules from both hemispheres. This may partly explain the high levels of diversity found for this cosmopolitan fern on these islands.
doi:10.1093/aobpla/plv118
PMCID: PMC4662730  PMID: 26487677
Biogeography; bracken; ferns; Galapagos; hybridization; islands; nuclear genes; phylogeny; Pteridium
7.  Reticulate evolution in diploid and tetraploid species of Polystachya (Orchidaceae) as shown by plastid DNA sequences and low-copy nuclear genes 
Annals of Botany  2010;106(1):37-56.
Background and Aims
Here evidence for reticulation in the pantropical orchid genus Polystachya is presented, using gene trees from five nuclear and plastid DNA data sets, first among only diploid samples (homoploid hybridization) and then with the inclusion of cloned tetraploid sequences (allopolyploids). Two groups of tetraploids are compared with respect to their origins and phylogenetic relationships.
Methods
Sequences from plastid regions, three low-copy nuclear genes and ITS nuclear ribosomal DNA were analysed for 56 diploid and 17 tetraploid accessions using maximum parsimony and Bayesian inference. Reticulation was inferred from incongruence between gene trees using supernetwork and consensus network analyses and from cloning and sequencing duplicated loci in tetraploids.
Key Results
Diploid trees from individual loci showed considerable incongruity but little reticulation signal when support from more than one gene tree was required to infer reticulation. This was coupled with generally low support in the individual gene trees. Sequencing the duplicated gene copies in tetraploids showed clearer evidence of hybrid evolution, including multiple origins of one group of tetraploids included in the study.
Conclusions
A combination of cloning duplicate gene copies in allotetraploids and consensus network comparison of gene trees allowed a phylogenetic framework for reticulation in Polystachya to be built. There was little evidence for homoploid hybridization, but our knowledge of the origins and relationships of three groups of allotetraploids are greatly improved by this study. One group showed evidence of multiple long-distance dispersals to achieve a pantropical distribution; another showed no evidence of multiple origins or long-distance dispersal but had greater morphological variation, consistent with hybridization between more distantly related parents.
doi:10.1093/aob/mcq092
PMCID: PMC2889800  PMID: 20525745
Allopolyploidy; consensus network; filtered supernetwork; low-copy nuclear genes; Orchidaceae; phylogenetic analysis; Polystachya; reticulate evolution
8.  Evolution and taxonomic split of the model grass Brachypodium distachyon 
Annals of Botany  2012;109(2):385-405.
Background and Aims
Brachypodium distachyon is being widely investigated across the world as a model plant for temperate cereals. This annual plant has three cytotypes (2n =  10, 20, 30) that are still regarded as part of a single species. Here, a multidisciplinary study has been conducted on a representative sampling of the three cytotypes to investigate their evolutionary relationships and origins, and to elucidate if they represent separate species.
Methods
Statistical analyses of 15 selected phenotypic traits were conducted in individuals from 36 lines or populations. Cytogenetic analyses were performed through flow cytometry, fluorescence in situ hybridization (FISH) with genomic (GISH) and multiple DNA sequences as probes, and comparative chromosome painting (CCP). Phylogenetic analyses were based on two plastid (ndhF, trnLF) and five nuclear (ITS, ETS, CAL, DGAT, GI) genes from different Brachypodium lineages, whose divergence times and evolutionary rates were estimated.
Key Results
The phenotypic analyses detected significant differences between the three cytotypes and demonstrated stability of characters in natural populations. Genome size estimations, GISH, FISH and CCP confirmed that the 2n = 10 and 2n = 20 cytotypes represent two different diploid taxa, whereas the 2n = 30 cytotype represents the allotetraploid derived from them. Phylogenetic analysis demonstrated that the 2n = 20 and 2n = 10 cytotypes emerged from two independent lineages that were, respectively, the maternal and paternal genome donors of the 2n = 30 cytotype. The 2n = 20 lineage was older and mutated significantly faster than the 2n = 10 lineage and all the core perennial Brachypodium species.
Conclusions
The substantial phenotypic, cytogenetic and molecular differences detected among the three B. distachyon sensu lato cytotypes are indicative of major speciation processes within this complex that allow their taxonomic separation into three distinct species. We have kept the name B. distachyon for the 2n = 10 cytotype and have described two novel species as B. stacei and B. hybridum for, respectively, the 2n = 20 and 2n = 30 cytotypes.
doi:10.1093/aob/mcr294
PMCID: PMC3268539  PMID: 22213013
Brachypodium distachyon; Brachypodium stacei; Brachypodium hybridum; cytogenetics; evolutionary systematics; nomenclature; speciation
9.  Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae) 
Background
The thirteen species of Dryopteris in North America have long been suspected of having undergone a complicated history of reticulate evolution via allopolyploid hybridization. Various explanations for the origins of the allopolyploid taxa have been suggested, and though most lines of evidence have supported the so-called “semicristata” hypothesis, contention over the group’s history has continued in several recent, conflicting studies.
Results
Sequence data from nine plastid and two nuclear markers were collected from 73 accessions representing 35 species of Dryopteris. Sequences from each of the allopolyploids are most closely related to their progenitor species as predicted by the “semicristata” hypothesis. Allotetraploid D. campyloptera appears to be derived from a hybrid between diploid D. expansa and D. intermedia; D. celsa, from diploid D. ludoviciana x D. goldiana; and D. carthusiana and D. cristata, from diploid “D. semicristata” x D. intermedia and D. ludoviciana, respectively. Allohexaploid D. clintoniana appears to be derived from D. cristata x D.goldiana. The earliest estimated dates of formation of the allopolyploids, based on divergence time analyses, were within the last 6 Ma. We found no evidence for recurrent formation of any of the allopolyploids. The sexual allopolyploid taxa are derived from crosses between parents that show intermediate levels of genetic divergence relative to all pairs of potential progenitors. In addition, the four allotetraploids are transgressive with respect to geographic range relative to one or both of their parents (their ranges extend beyond those of the parents), suggesting that ecological advantages in novel habitats or regions may promote long-term regional coexistence of the hybrid taxa with their progenitors.
Conclusions
This study provides the first thorough evaluation of the North American complex of woodferns using extensive sampling of taxa and genetic markers. Phylogenies produced from each of three datasets (one plastid and two nuclear) support the “semicristata” hypothesis, including the existence of a missing diploid progenitor, and allow us to reject all competing hypotheses. This study demonstrates the value of using multiple, biparentally inherited markers to evaluate reticulate complexes, assess the frequency of recurrent polyploidization, and determine the relative importance of introgression vs. hybridization in shaping the histories of such groups.
doi:10.1186/1471-2148-12-104
PMCID: PMC3509404  PMID: 22748145
Ferns; Divergence time estimates; Genetic distances; Hybridization; Introgression; Phylogeny; Polyploidy
10.  Patterns of diversification amongst tropical regions compared: a case study in Sapotaceae 
Frontiers in Genetics  2014;5:362.
Species diversity is unequally distributed across the globe, with the greatest concentration occurring in the tropics. Even within the tropics, there are significant differences in the numbers of taxa found in each continental region. Manilkara is a pantropical genus of trees in the Sapotaceae comprising c. 78 species. Its distribution allows for biogeographic investigation and testing of whether rates of diversification differ amongst tropical regions. The age and geographical origin of Manilkara are inferred to determine whether Gondwanan break-up, boreotropical migration or long distance dispersal have shaped its current disjunct distribution. Diversification rates through time are also analyzed to determine whether the timing and tempo of speciation on each continent coincides with geoclimatic events. Bayesian analyses of nuclear (ITS) and plastid (rpl32-trnL, rps16-trnK, and trnS-trnFM) sequences were used to reconstruct a species level phylogeny of Manilkara and related genera in the tribe Mimusopeae. Analyses of the nuclear data using a fossil-calibrated relaxed molecular clock indicate that Manilkara evolved 32–29 million years ago (Mya) in Africa. Lineages within the genus dispersed to the Neotropics 26–18 Mya and to Asia 28–15 Mya. Higher speciation rates are found in the Neotropical Manilkara clade than in either African or Asian clades. Dating of regional diversification correlates with known palaeoclimatic events. In South America, the divergence between Atlantic coastal forest and Amazonian clades coincides with the formation of drier Cerrado and Caatinga habitats between them. In Africa diversification coincides with Tertiary cycles of aridification and uplift of the east African plateaux. In Southeast Asia dispersal may have been limited by the relatively recent emergence of land in New Guinea and islands further east c. 10 Mya.
doi:10.3389/fgene.2014.00362
PMCID: PMC4253964  PMID: 25520736
Sapotaceae; Manilkara; pantropical; biogeography; diversification rates
11.  Plastid phylogenomics of the cool-season grass subfamily: clarification of relationships among early-diverging tribes 
AoB Plants  2015;7:plv046.
Whole plastid genomes (plastomes) are being sequenced rapidly from across the green plant tree of life, and phylogenetic analyses of these are increasing resolution and support for relationships that were unresolved in earlier studies. The cool-season grass subfamily, Pooideae, includes important temperate cereals, turf grasses and forage species, yet some aspects of deep phylogeny in the lineage are unresolved. We newly sequenced 25 Pooideae plastomes, and conducted phylogenomic analyses of these and 20 existing plastomes from the subfamily. Most aspects of deep relationship in Pooideae are maximally supported in our analyses, including those among early-diverging tribes.
Whole plastid genomes are being sequenced rapidly from across the green plant tree of life, and phylogenetic analyses of these are increasing resolution and support for relationships that have varied among or been unresolved in earlier single- and multi-gene studies. Pooideae, the cool-season grass lineage, is the largest of the 12 grass subfamilies and includes important temperate cereals, turf grasses and forage species. Although numerous studies of the phylogeny of the subfamily have been undertaken, relationships among some ‘early-diverging’ tribes conflict among studies, and some relationships among subtribes of Poeae have not yet been resolved. To address these issues, we newly sequenced 25 whole plastomes, which showed rearrangements typical of Poaceae. These plastomes represent 9 tribes and 11 subtribes of Pooideae, and were analysed with 20 existing plastomes for the subfamily. Maximum likelihood (ML), maximum parsimony (MP) and Bayesian inference (BI) robustly resolve most deep relationships in the subfamily. Complete plastome data provide increased nodal support compared with protein-coding data alone at nodes that are not maximally supported. Following the divergence of Brachyelytrum, Phaenospermateae, Brylkinieae–Meliceae and Ampelodesmeae–Stipeae are the successive sister groups of the rest of the subfamily. Ampelodesmeae are nested within Stipeae in the plastome trees, consistent with its hybrid origin between a phaenospermatoid and a stipoid grass (the maternal parent). The core Pooideae are strongly supported and include Brachypodieae, a Bromeae–Triticeae clade and Poeae. Within Poeae, a novel sister group relationship between Phalaridinae and Torreyochloinae is found, and the relative branching order of this clade and Aveninae, with respect to an Agrostidinae–Brizinae clade, are discordant between MP and ML/BI trees. Maximum likelihood and Bayesian analyses strongly support Airinae and Holcinae as the successive sister groups of a Dactylidinae–Loliinae clade.
doi:10.1093/aobpla/plv046
PMCID: PMC4480051  PMID: 25940204
Chloroplast genome; core Pooideae; phylogenetics; phylogenomics; plastome; Poeae; Schedonorus arundinaceus
12.  Reticulate evolution in Panicum (Poaceae): the origin of tetraploid broomcorn millet, P. miliaceum  
Journal of Experimental Botany  2014;65(12):3165-3175.
Summary
Sequence data and genomic in situ hybridization identify the New World diploid Panicum capillare as an ancestral genome of the Old World tetraploid cereal broomcorn millet, P. miliaceum.
Panicum miliaceum (broomcorn millet) is a tetraploid cereal, which was among the first domesticated crops, but is now a minor crop despite its high water use efficiency. The ancestors of this species have not been determined; we aimed to identify likely candidates within the genus, where phylogenies are poorly resolved. Nuclear and chloroplast DNA sequences from P. miliaceum and a range of diploid and tetraploid relatives were used to develop phylogenies of the diploid and tetraploid species. Chromosomal in situ hybridization with genomic DNA as a probe was used to characterize the genomes in the tetraploid P. miliaceum and a tetraploid accession of P. repens. In situ hybridization showed that half the chromosomes of P. miliaceum hybridized more strongly with labelled genomic DNA from P. capillare, and half with labelled DNA from P. repens. Genomic DNA probes differentiated two sets of 18 chromosomes in the tetraploid P. repens. Our phylogenetic data support the allotetraploid origin of P. miliaceum, with the maternal ancestor being P. capillare (or a close relative) and the other genome being shared with P. repens. Our P. repens accession was also an allotetraploid with two dissimilar but closely related genomes, the maternal genome being similar to P. sumatrense. Further collection of Panicum species, particularly from the Old World, is required. It is important to identify why the water-efficient P. miliaceum is now of minimal importance in agriculture, and it may be valuable to exploit the diversity in this species and its ancestors.
doi:10.1093/jxb/eru161
PMCID: PMC4071833  PMID: 24723408
Crop ancestors; domestication; Panicum; hybridization; polyploidy; genomic in situ hybridization
13.  Experimental evidence for the ancestry of allotetraploid Trifolium repens and creation of synthetic forms with value for plant breeding 
BMC Plant Biology  2012;12:55.
Background
White clover (Trifolium repens) is a ubiquitous weed of the temperate world that through use of improved cultivars has also become the most important legume of grazed pastures world-wide. It has long been suspected to be allotetraploid, but the diploid ancestral species have remained elusive. Putative diploid ancestors were indicated by DNA sequence phylogeny to be T. pallescens and T. occidentale. Here, we use further DNA evidence as well as a combination of molecular cytogenetics (FISH and GISH) and experimental hybridization to test the hypothesis that white clover originated as a hybrid between T. pallescens and T. occidentale.
Results
T. pallescens plants were identified with chloroplast trnL intron DNA sequences identical to those of white clover. Similarly, T. occidentale plants with nuclear ITS sequences identical to white clover were also identified. Reciprocal GISH experiments, alternately using labeled genomic DNA probes from each of the putative ancestral species on the same white clover cells, showed that half of the chromosomes hybridized with each probe. F1 hybrids were generated by embryo rescue and these showed strong interspecific chromosome pairing and produced a significant frequency of unreduced gametes, indicating the likely mode of polyploidization. The F1 hybrids are inter-fertile with white clover and function as synthetic white clovers, a valuable new resource for the re-incorporation of ancestral genomes into modern white clover for future plant breeding.
Conclusions
Evidence from DNA sequence analyses, molecular cytogenetics, interspecific hybridization and breeding experiments supports the hypothesis that a diploid alpine species (T. pallescens) hybridized with a diploid coastal species (T. occidentale) to generate tetraploid T. repens. The coming together of these two narrowly adapted species (one alpine and the other maritime), along with allotetraploidy, has led to a transgressive hybrid with a broad adaptive range.
doi:10.1186/1471-2229-12-55
PMCID: PMC3443075  PMID: 22530692
Trifolium repens; White clover; Allopolyploid; Interspecific hybridization
14.  Similar patterns of rDNA evolution in synthetic and recently formed natural populations of Tragopogon (Asteraceae) allotetraploids 
Background
Tragopogon mirus and T. miscellus are allotetraploids (2n = 24) that formed repeatedly during the past 80 years in eastern Washington and adjacent Idaho (USA) following the introduction of the diploids T. dubius, T. porrifolius, and T. pratensis (2n = 12) from Europe. In most natural populations of T. mirus and T. miscellus, there are far fewer 35S rRNA genes (rDNA) of T. dubius than there are of the other diploid parent (T. porrifolius or T. pratensis). We studied the inheritance of parental rDNA loci in allotetraploids resynthesized from diploid accessions. We investigate the dynamics and directionality of these rDNA losses, as well as the contribution of gene copy number variation in the parental diploids to rDNA variation in the derived tetraploids.
Results
Using Southern blot hybridization and fluorescent in situ hybridization (FISH), we analyzed copy numbers and distribution of these highly reiterated genes in seven lines of synthetic T. mirus (110 individuals) and four lines of synthetic T. miscellus (71 individuals). Variation among diploid parents accounted for most of the observed gene imbalances detected in F1 hybrids but cannot explain frequent deviations from repeat additivity seen in the allotetraploid lines. Polyploid lineages involving the same diploid parents differed in rDNA genotype, indicating that conditions immediately following genome doubling are crucial for rDNA changes. About 19% of the resynthesized allotetraploid individuals had equal rDNA contributions from the diploid parents, 74% were skewed towards either T. porrifolius or T. pratensis-type units, and only 7% had more rDNA copies of T. dubius-origin compared to the other two parents. Similar genotype frequencies were observed among natural populations. Despite directional reduction of units, the additivity of 35S rDNA locus number is maintained in 82% of the synthetic lines and in all natural allotetraploids.
Conclusions
Uniparental reductions of homeologous rRNA gene copies occurred in both synthetic and natural populations of Tragopogon allopolyploids. The extent of these rDNA changes was generally higher in natural populations than in the synthetic lines. We hypothesize that locus-specific and chromosomal changes in early generations of allopolyploids may influence patterns of rDNA evolution in later generations.
doi:10.1186/1471-2148-10-291
PMCID: PMC2955031  PMID: 20858289
15.  Evolution of the polyploid north-west Iberian Leucanthemum pluriflorum clan (Compositae, Anthemideae) based on plastid DNA sequence variation and AFLP fingerprinting 
Annals of Botany  2013;111(6):1109-1123.
Background and Aims
The genus Leucanthemum is a species-rich polyploid complex from southern and central Europe, comprising 41 species with ploidy ranging from 2x to 22x. The present contribution aims at reconstructing the evolutionary history of a geographically isolated species group (the L. pluriflorum clan) from the north-west Iberian Peninsula comprising the diploid L. pluriflorum, the tetraploids L. ircutianum subsp. pseudosylvaticum and L. × corunnense (a putative hybrid taxon based on crossing between L. pluriflorum and L. merinoi), and the hexaploids L. sylvaticum and L. merinoi.
Methods
Chromosome number variation (determined flow cytometrically) and sequence variation were analysed for two intergenic spacer regions on the plastid genome (psbA-trnH and trnC-petN) for individuals from 54 populations in combination with amplified fragment length polymorphism (AFLP) fingerprinting of 246 representative individuals from these populations.
Key Results
Plastid sequence data revealed that all surveyed members of the L. pluriflorum clan possess plastid haplotypes that are closely related to each other and distinctly separated from other Leucanthemum species. AFLP fingerprinting resulted in allopolyploid fragment patterns for most of the polyploid populations, except for the tetraploid L. × corunnense and a further tetraploid population in northern Galicia, which cluster with the diploids rather than with the other polyploids. In silico modelling of (auto)tetraploid AFLP genotypes further corroborates the allopolyploid nature of L. ircutianum subsp. pseudosylvaticum, L. sylvaticum and L. merinoi.
Conclusions
The present study provides evidence for recognizing one diploid (L. pluriflorum), one autotetraploid (L. corunnense), one allotetraploid (L. pseudosylvaticum) and one allohexaploid (L. sylvaticum with the two geographically and ecologically differentiated subspecies subsp. sylvaticum and subsp. merinoi) in the L. pluriflorum clan. It also has implications for the understanding of biogeographical patterns in the Iberian Peninsula.
doi:10.1093/aob/mct075
PMCID: PMC3662516  PMID: 23579573
AFLP fingerprinting; Asteraceae; cpDNA sequencing; flow cytometry; hybridization; polyploidy; speciation
16.  A molecular phylogeny and classification of Leptochloa (Poaceae: Chloridoideae: Chlorideae) sensu lato and related genera 
Annals of Botany  2012;109(7):1317-1330.
Background and Aims
Leptochloa (including Diplachne) sensu lato (s.l.) comprises a diverse assemblage of C4 (NAD-ME and PCK) grasses with approx. 32 annual or perennial species. Evolutionary relationships and a modern classification of Leptochloa spp. based on the study of molecular characters have only been superficially investigated in four species. The goals of this study were to reconstruct the evolutionary history of Leptochloa s.l. with molecular data and broad taxon sampling.
Methods
A phylogenetic analysis was conducted of 130 species (mostly Chloridoideae), of which 22 are placed in Leptochloa, using five plastid (rpL32-trn-L, ndhA intron, rps16 intron, rps16-trnK and ccsA) and the nuclear ITS 1 and 2 (ribosomal internal transcribed spacer regions) to infer evolutionary relationships and revise the classification.
Key results
Leptochloa s.l. is polyphyletic and strong support was found for five lineages. Embedded within the Leptochloa sensu stricto (s.s.) clade are two Trichloris spp. and embedded in Dinebra are Drake-brockmania and 19 Leptochloa spp.
Conclusions
The molecular results support the dissolution of Leptochloa s.l. into the following five genera: Dinebra with 23 species, Diplachne with two species, Disakisperma with three species, Leptochloa s.s. with five species and a new genus, Trigonochloa, with two species.
doi:10.1093/aob/mcs077
PMCID: PMC3359928  PMID: 22628365
Classification; Dinebra; Diplachne; Disakisperma; Drake-brockmania; ITS; Leptochloa; phylogeny; plastid DNA sequences; Poaceae; Trichloris; Trigonochloa
17.  A Multilocus Molecular Phylogeny of the Parrots (Psittaciformes): Support for a Gondwanan Origin during the Cretaceous 
Molecular Biology and Evolution  2008;25(10):2141-2156.
The question of when modern birds (Neornithes) first diversified has generated much debate among avian systematists. Fossil evidence generally supports a Tertiary diversification, whereas estimates based on molecular dating favor an earlier diversification in the Cretaceous period. In this study, we used an alternate approach, the inference of historical biogeographic patterns, to test the hypothesis that the initial radiation of the Order Psittaciformes (the parrots and cockatoos) originated on the Gondwana supercontinent during the Cretaceous. We utilized broad taxonomic sampling (representatives of 69 of the 82 extant genera and 8 outgroup taxa) and multilocus molecular character sampling (3,941 bp from mitochondrial DNA (mtDNA) genes cytochrome oxidase I and NADH dehydrogenase 2 and nuclear introns of rhodopsin intron 1, tropomyosin alpha-subunit intron 5, and transforming growth factor ß-2) to generate phylogenetic hypotheses for the Psittaciformes. Analyses of the combined character partitions using maximum parsimony, maximum likelihood, and Bayesian criteria produced well-resolved and topologically similar trees in which the New Zealand taxa Strigops and Nestor (Psittacidae) were sister to all other psittaciforms and the cockatoo clade (Cacatuidae) was sister to a clade containing all remaining parrots (Psittacidae). Within this large clade of Psittacidae, some traditionally recognized tribes and subfamilies were monophyletic (e.g., Arini, Psittacini, and Loriinae), whereas several others were polyphyletic (e.g., Cyclopsittacini, Platycercini, Psittaculini, and Psittacinae). Ancestral area reconstructions using our Bayesian phylogenetic hypothesis and current distributions of genera supported the hypothesis of an Australasian origin for the Psittaciformes. Separate analyses of the timing of parrot diversification constructed with both Bayesian relaxed-clock and penalized likelihood approaches showed better agreement between geologic and diversification events in the chronograms based on a Cretaceous dating of the basal split within parrots than the chronograms based on a Tertiary dating of this split, although these data are more equivocal. Taken together, our results support a Cretaceous origin of Psittaciformes in Gondwana after the separation of Africa and the India/Madagascar block with subsequent diversification through both vicariance and dispersal. These well-resolved molecular phylogenies will be of value for comparative studies of behavior, ecology, and life history in parrots.
doi:10.1093/molbev/msn160
PMCID: PMC2727385  PMID: 18653733
Cretaceous origin; divergence times; Gondwanan distribution; K/T boundary; molecular phylogeny; parrot; Psittaciformes; Tertiary origin
18.  A New Synthetic Allotetraploid (A1A1G2G2) between Gossypium herbaceum and G. australe: Bridging for Simultaneously Transferring Favorable Genes from These Two Diploid Species into Upland Cotton 
PLoS ONE  2015;10(4):e0123209.
Gossypium herbaceum, a cultivated diploid cotton species (2n = 2x = 26, A1A1), has favorable traits such as excellent drought tolerance and resistance to sucking insects and leaf curl virus. G. australe, a wild diploid cotton species (2n = 2x = 26, G2G2), possesses numerous economically valuable characteristics such as delayed pigment gland morphogenesis (which is conducive to the production of seeds with very low levels of gossypol as a potential food source for humans and animals) and resistance to insects, wilt diseases and abiotic stress. Creating synthetic allotetraploid cotton from these two species would lay the foundation for simultaneously transferring favorable genes into cultivated tetraploid cotton. Here, we crossed G. herbaceum (as the maternal parent) with G. australe to produce an F1 interspecific hybrid and doubled its chromosome complement with colchicine, successfully generating a synthetic tetraploid. The obtained tetraploid was confirmed by morphology, cytology and molecular markers and then self-pollinated. The S1 seedlings derived from this tetraploid gradually became flavescent after emergence of the fifth true leaf, but they were rescued by grafting and produced S2 seeds. The rescued S1 plants were partially fertile due to the existence of univalents at Metaphase I of meiosis, leading to the formation of unbalanced, nonviable gametes lacking complete sets of chromosomes. The S2 plants grew well and no flavescence was observed, implying that interspecific incompatibility, to some extent, had been alleviated in the S2 generation. The synthetic allotetraploid will be quite useful for polyploidy evolutionary studies and as a bridge for transferring favorable genes from these two diploid species into Upland cotton through hybridization.
doi:10.1371/journal.pone.0123209
PMCID: PMC4400159  PMID: 25879660
19.  Does the Arcto-Tertiary Biogeographic Hypothesis Explain the Disjunct Distribution of Northern Hemisphere Herbaceous Plants? The Case of Meehania (Lamiaceae) 
PLoS ONE  2015;10(2):e0117171.
Despite considerable progress, many details regarding the evolution of the Arcto-Tertiary flora, including the timing, direction, and relative importance of migration routes in the evolution of woody and herbaceous taxa of the Northern Hemisphere, remain poorly understood. Meehania (Lamiaceae) comprises seven species and five subspecies of annual or perennial herbs, and is one of the few Lamiaceae genera known to have an exclusively disjunct distribution between eastern Asia and eastern North America. We analyzed the phylogeny and biogeographical history of Meehania to explore how the Arcto-Tertiary biogeographic hypothesis and two possible migration routes explain the disjunct distribution of Northern Hemisphere herbaceous plants. Parsimony and Bayesian inference were used for phylogenetic analyses based on five plastid sequences (rbcL, rps16, rpl32-trnH, psbA-trnH, and trnL-F) and two nuclear (ITS and ETS) gene regions. Divergence times and biogeographic inferences were performed using Bayesian methods as implemented in BEAST and S-DIVA, respectively. Analyses including 11 of the 12 known Meehania taxa revealed incongruence between the chloroplast and nuclear trees, particularly in the positions of Glechoma and Meehania cordata, possibly indicating allopolyploidy with chloroplast capture in the late Miocene. Based on nrDNA, Meehania is monophyletic, and the North American species M. cordata is sister to a clade containing the eastern Asian species. The divergence time between the North American M. cordata and the eastern Asian species occurred about 9.81 Mya according to the Bayesian relaxed clock methods applied to the combined nuclear data. Biogeographic analyses suggest a primary role of the Arcto-Tertiary flora in the study taxa distribution, with a northeast Asian origin of Meehania. Our results suggest an Arcto-Tertiary origin of Meehania, with its present distribution most probably being a result of vicariance and southward migrations of populations during climatic oscillations in the middle Miocene with subsequent migration into eastern North America via the Bering land bridge in the late Miocene.
doi:10.1371/journal.pone.0117171
PMCID: PMC4319762  PMID: 25658699
20.  A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree 
Background
The Solanaceae is a plant family of great economic importance. Despite a wealth of phylogenetic work on individual clades and a deep knowledge of particular cultivated species such as tomato and potato, a robust evolutionary framework with a dated molecular phylogeny for the family is still lacking. Here we investigate molecular divergence times for Solanaceae using a densely-sampled species-level phylogeny. We also review the fossil record of the family to derive robust calibration points, and estimate a chronogram using an uncorrelated relaxed molecular clock.
Results
Our densely-sampled phylogeny shows strong support for all previously identified clades of Solanaceae and strongly supported relationships between the major clades, particularly within Solanum. The Tomato clade is shown to be sister to section Petota, and the Regmandra clade is the first branching member of the Potato clade. The minimum age estimates for major splits within the family provided here correspond well with results from previous studies, indicating splits between tomato & potato around 8 Million years ago (Ma) with a 95% highest posterior density (HPD) 7–10 Ma, Solanum & Capsicum c. 19 Ma (95% HPD 17–21), and Solanum & Nicotiana c. 24 Ma (95% HPD 23–26).
Conclusions
Our large time-calibrated phylogeny provides a significant step towards completing a fully sampled species-level phylogeny for Solanaceae, and provides age estimates for the whole family. The chronogram now includes 40% of known species and all but two monotypic genera, and is one of the best sampled angiosperm family phylogenies both in terms of taxon sampling and resolution published thus far. The increased resolution in the chronogram combined with the large increase in species sampling will provide much needed data for the examination of many biological questions using Solanaceae as a model system.
doi:10.1186/1471-2148-13-214
PMCID: PMC3850475  PMID: 24283922
21.  Spore Fitness Components Do Not Differ Between Diploid and Allotetraploid Species of Dryopteris (Dryopteridaceae) 
Annals of Botany  2006;98(3):609-618.
• Background and Aims Although allopolyploidy is a prevalent speciation mechanism in plants, its adaptive consequences are poorly understood. In addition, the effects of allopolyploidy per se (i.e. hybridization and chromosome doubling) can be confounded with those of subsequent evolutionary divergence between allopolyploids and related diploids. This report assesses whether fern species with the same ploidy level or the same altitudinal distribution have similar germination responses to temperature. The effects of polyploidy on spore abortion and spore size are also investigated, since both traits may have adaptive consequences.
• Methods Three allotetraploid (Dryopteris corleyi, D. filix-mas and D. guanchica) and three related diploid taxa (D. aemula, D. affinis ssp. affinis and D. oreades) were studied. Spores were collected from 24 populations in northern Spain. Four spore traits were determined: abortion percentage, size, germination time and germination percentage. Six incubation temperatures were tested: 8, 15, 20, 25 and 32 °C, and alternating 8/15 °C.
• Key Results Allotetraploids had bigger spores than diploid progenitors, whereas spore abortion percentages were generally similar. Germination times decreased with increasing temperatures in a wide range of temperatures (8–25 °C), although final germination percentages were similar among species irrespective of their ploidy level. Only at low temperature (8 °C) did two allotetraploid species reach higher germination percentages than diploid parents. Allotetraploids showed faster germination rates, which would probably give them a competitive advantage over diploid parents. Germination behaviour was not correlated with altitudinal distribution of species.
• Conclusions The results of this study suggest that (i) relative fitness of allopolyploids at sporogenesis does not differ from that of diploid parents and (ii) neither does allopolyploidization involve a change in the success of spore germination.
doi:10.1093/aob/mcl137
PMCID: PMC2803563  PMID: 16845140
Allopolyploidy; Dryopteris; fitness component; northern Spain; spore abortion; spore germination; temperature
22.  Hybridization and long-distance colonization at different time scales: towards resolution of long-term controversies in the sweet vernal grasses (Anthoxanthum) 
Annals of Botany  2013;112(6):1015-1030.
Background and Aims
Repeated hybridization and/or polyploidization confound classification and phylogenetic inference, and multiple colonizations at different time scales complicate biogeographical reconstructions. This study investigates whether such processes can explain long-term controversies in Anthoxanthum, and in particular its debated relationship to the genus Hierochloë, the evolution of its conspicuously diverse floral morphology, and the origins of its strikingly disjunct occurrences. A hypothesis for recurrent polyploid formation is proposed.
Methods
Three plastid (trnH-psbA, trnT-L and trnL-F) and two nuclear (ITS, ETS) DNA regions were sequenced in 57 accessions of 17 taxa (including 161 ETS clones) and Bayesian phylogenetic analyses were conducted. Divergence times were inferred in *BEAST using a strict molecular clock.
Key Results Anthoxanthum
was inferred as monophyletic and sister to one species of Hierochloë based on the plastid data, whereas the nuclear data suggested that one section (Anthoxanthum section Anthoxanthum) is sister to a clade including the other section (Anthoxanthum section Ataxia) as sister to the genus Hierochloë. This could explain the variation in floral morphology; the aberrant characters in Ataxia seem to result from a Miocene hybridization event between one lineage with one fertile and two sterile florets (the Anthoxanthum lineage) and one which probably had three fertile florets as in extant Hierochloë. The distinct diploid A. gracile lineage originated in the Miocene; all other speciation events, many of them involving polyploidy, were dated to the Late Pliocene to Late Pleistocene. Africa was apparently colonized twice in the Late Pliocene (from the north to afro-alpine eastern Africa, and from south-east Asia to southern Africa), whereas Macaronesia was colonized much later (Late Pleistocene) by a diploid Mediterranean lineage. The widespread European tetraploid A. odoratum originated at least twice.
Conclusions
Many of the controversies in Anthoxanthum can be explained by recurring hybridization and/or polyploidization on time scales ranging from the Miocene to the Late Pleistocene. All but one of the extant species shared most recent common ancestors in the Late Pliocene to the Late Pleistocene. The disjunct occurrences in Africa originated in the Late Pliocene via independent immigrations, whereas Macaronesia was colonized in the Late Pleistocene.
doi:10.1093/aob/mct170
PMCID: PMC3783235  PMID: 23912698
Africa; Anthoxanthum; Ataxia; biogeography; evolution; C3 grasses; hybridization; long-distance colonization; phylogeny; Poaceae; sweet vernal grasses
23.  Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors 
Heredity  2011;108(4):419-430.
Autopolyploidy and allopolyploidy are common in many plants and some animals. Rapid changes in genomic composition and gene expression have been observed in both autopolyploids and allopolyploids, but the effects of polyploidy on proteomic divergence are poorly understood. Here, we report quantitative analysis of protein changes in leaves of Arabidopsis autopolyploids and allotetraploids and their progenitors using isobaric tags for relative and absolute quantitation (iTRAQ) coupled with mass spectrometry. In more than 1000 proteins analyzed, the levels of protein divergence were relatively high (∼18%) between Arabidopsis thaliana and Arabidopsis arenosa, relatively low (∼6.8%) between an A. thaliana diploid and autotetraploid and intermediate (∼8.3 and 8.2%) in F1- and F8-resynthesized allotetraploids relative to mid-parent values, respectively. This pattern of proteomic divergence was consistent with the previously reported gene expression data. In particular, many non-additively accumulated proteins (61–62%) in the F1 and F8 allotetraploids were also differentially expressed between the parents. The differentially accumulated proteins in functional categories of abiotic and biotic stresses were overrepresented between an A. thaliana autotetraploid and diploid and between two Arabidopsis species, but not significantly different between allotetraploids and their progenitors. Although the trend of changes is similar, the percentage of differentially accumulated proteins that matched previously reported differentially expressed genes was relatively low. Western blot analysis confirmed several selected proteins with isoforms the cumulative levels of which were differentially expressed. These data suggest high protein divergence between species and rapid changes in post-transcriptional regulation and translational modifications of proteins during polyploidization.
doi:10.1038/hdy.2011.92
PMCID: PMC3313054  PMID: 22009271
polyploidy; proteome; iTRAQ; gene expression; hybrids; Arabidopsis
24.  Molecular Phylogeny and Biogeographic Diversification of Linnaeoideae (Caprifoliaceae s. l.) Disjunctly Distributed in Eurasia, North America and Mexico 
PLoS ONE  2015;10(3):e0116485.
Linnaeoideae is a small subfamily of erect or creeping shrubs to small trees in Caprifoliaceae that exhibits a wide disjunct distribution in Eurasia, North America and Mexico. Most taxa of the subfamily occur in eastern Asia and Mexico but the monospecific genus Linnaea has a circumboreal to north temperate distribution. In this study, we conducted phylogenetic and biogeographic analyses for Linnaeoideae and its close relatives based on sequences of the nuclear ribosomal ITS and nine plastid (rbcL, trnS-G, matK, trnL-F, ndhA, trnD-psbM, petB-D, trnL-rpl32 and trnH-psbA) markers. Our results support that Linnaeoideae is monophyletic, consisting of four eastern Asian lineages (Abelia, Diabelia, Dipelta and Kolkwitzia), the Mexican Vesalea, and Linnaea. The Mexican Vesalea was formerly placed in Abelia, but it did not form a clade with the eastern Asian Abelia; instead Vesalea and Linnaea are sisters. The divergence time between the eastern Asian lineages and the Mexican Vesalea plus the Linnaea clade was dated to be 50.86 Ma, with a 95% highest posterior density of 42.8 Ma (middle Eocene) to 60.19 Ma (early Paleocene) using the Bayesian relaxed clock estimation. Reconstructed ancestral areas indicated that the common ancestor of Linnaea plus Vesalea may have been widespread in eastern Asia and Mexico or originated in eastern Asia during the Eocene and likely migrated across continents in the Northern Hemisphere via the North Atlantic Land Bridges or the Bering Land Bridge. The Qinling Mountains of eastern Asia are the modern-day center of diversity of Kolkwitzia-Dipelta-Diabelia clade. The Diabeliaclade became highly diversified in Japan and eastern China. Populations of Diabelia serrata in Japan and eastern China were found to be genetically identical in this study, suggesting a recent disjunction across the East China Sea, following the last glacial event.
doi:10.1371/journal.pone.0116485
PMCID: PMC4355296  PMID: 25756215
25.  Duplication, divergence and persistence in the Phytochrome photoreceptor gene family of cottons (Gossypium spp.) 
BMC Plant Biology  2010;10:119.
Background
Phytochromes are a family of red/far-red photoreceptors that regulate a number of important developmental traits in cotton (Gossypium spp.), including plant architecture, fiber development, and photoperiodic flowering. Little is known about the composition and evolution of the phytochrome gene family in diploid (G. herbaceum, G. raimondii) or allotetraploid (G. hirsutum, G. barbadense) cotton species. The objective of this study was to obtain a preliminary inventory and molecular-evolutionary characterization of the phytochrome gene family in cotton.
Results
We used comparative sequence resources to design low-degeneracy PCR primers that amplify genomic sequence tags (GSTs) for members of the PHYA, PHYB/D, PHYC and PHYE gene sub-families from A- and D-genome diploid and AD-genome allotetraploid Gossypium species. We identified two paralogous PHYA genes (designated PHYA1 and PHYA2) in diploid cottons, the result of a Malvaceae-specific PHYA gene duplication that occurred approximately 14 million years ago (MYA), before the divergence of the A- and D-genome ancestors. We identified a single gene copy of PHYB, PHYC, and PHYE in diploid cottons. The allotetraploid genomes have largely retained the complete gene complements inherited from both of the diploid genome ancestors, with at least four PHYA genes and two genes encoding PHYB, PHYC and PHYE in the AD-genomes. We did not identify a PHYD gene in any cotton genomes examined.
Conclusions
Detailed sequence analysis suggests that phytochrome genes retained after duplication by segmental duplication and allopolyploidy appear to be evolving independently under a birth-and-death-process with strong purifying selection. Our study provides a preliminary phytochrome gene inventory that is necessary and sufficient for further characterization of the biological functions of each of the cotton phytochrome genes, and for the development of 'candidate gene' markers that are potentially useful for cotton improvement via modern marker-assisted selection strategies.
doi:10.1186/1471-2229-10-119
PMCID: PMC3095280  PMID: 20565911

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