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1.  Characterization of a New Burrowing Nematode Population, Radopholus citrophilus, from Hawaii 
Journal of Nematology  1986;18(1):50-53.
Karyotype, host preference, isozyzme patterns, morphometrics, and mating behavior of two burrowing nematode populations from Hawaii, one infecting Anthurium sp. and the second infecting Musa sp., were compared with Radopholus similis and R. citrophilus populations from Florida. The population from Anthurium sp. had five chromosomes (n = 5), and that from Musa sp. had four (n = 4). Neither of the Hawaiian nematode populations persisted in roots of Citrus limon or C. aurantium. Anthurium clarinerivum and A. hookeri were hosts of the burrowing nematode population from anthurium in Hawaii and of R. citrophilus from Florida, whereas the two anthurium species were poor hosts of the population from Musa sp. in Hawaii and R. similis from Florida. The isozyme pattern of the population isolated from anthurium was identical to that of R. citrophigus, whereas the pattern of the population from banana in Hawaii was identical to that of R. similis. Mating behavior between the burrowing nematode population isolated from Anthurium sp. and a Florida population of R. citrophilus supports their close taxonomic relationship. Mating was observed between the population from Anthurium sp. and the Florida population of R. citrophilus but not between the Hawaiian burrowing nematode population isolated from Musa sp. and a Florida population of R. citrophilus. These findings indicate that a previously unidentified population of R. citrophilus which does not parasitize citrus occurs in Hawaii.
PMCID: PMC2618493  PMID: 19294139
anthurium; banana; biotype; citrus; ornamental; race; Radopholus similis; Radopholus citrophilus
2.  De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress 
BMC Genomics  2013;14(1):827.
Anthurium andraeanum is one of the most popular tropical flowers. In temperate and cold zones, a much greater risk of cold stress occurs in the supply of Anthurium plants. Unlike the freeze-tolerant model plants, Anthurium plants are particularly sensitive to low temperatures. Improvement of chilling tolerance in Anthurium may significantly increase its production and extend its shelf-life. To date, no previous genomic information has been reported in Anthurium plants.
Using Illumina sequencing technology, we generated over two billion base of high-quality sequence in Anthurium, and demonstrated de novo assembly and annotation of genes without prior genome information. These reads were assembled into 44,382 unigenes (mean length = 560 bp). Based on similarity search with known protein in the non-redundant (nr) protein database, 27396 unigenes (62%) were functionally annotated with a cut-off E-value of 10-5. Further, DGE tags were mapped to the assembled transcriptome for gene expression analysis under cold stress. In total, 4363 differentially expressed genes were identified. Among these genes, 292, 805 and 708 genes were up-regulated after 1-h, 5-h and 24-h cold treatment, respectively. Then we mapped these cold-induced genes to the KEGG database. Specific enrichment was observed in photosynthesis pathway, metabolic pathways and oxidative phosphorylation pathway in 1-h cold-treated plants. After a 5-h cold treatment, the metabolic pathways and oxidative phosphorylation pathway were significantly identified as the top two pathways. After 24-h cold treatment, mRNA surveillance pathway, RNA transport pathway and plant-pathogen interaction pathway were significantly enriched. Together, a total of 39 cold-inducible transcription factors were identified, including subsets of AP2/ERF, Zinc figure, NAC, MYB and bZIP family members.
Our study is the first to provide the transcriptome sequence resource for Anthurium plants, and demonstrate its digital gene expression profiling under cold conditions using the assembled transcriptome data for reference. These data provides a valuable resource for genetic and genomic studies under abiotic conditions for Anthurium plants.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2164-14-827) contains supplementary material, which is available to authorized users.
PMCID: PMC4046746  PMID: 24267953
Anthurium; Cold; Transcriptome; Digital gene expression
3.  Relationship between Symptom Development and Actual Sites of Infection in Leaves of Anthurium Inoculated with a Bioluminescent Strain of Xanthomonas campestris pv. dieffenbachiae 
The infection process of bacterial blight of anthurium was monitored with a bioluminescent strain of Xanthomonas campestris pv. dieffenbachiae. The relationship between symptom expression on infected leaves (assessed visually) and the extent of bacterial movement within tissues (evaluated by bioluminescence emission) varied among anthurium cultivars. In several cultivars previously considered susceptible on the basis of symptom development alone, bacterial invasion of leaves extended far beyond the visually affected areas. In other cultivars previously considered resistant, bacterial invasion was restricted to areas with visible symptoms. In three cultivars previously considered resistant, leaves were extensively invaded by the bacterium, and yet few or no symptoms were seen on infected leaves. The pathogen was consistently recovered from leaf sections emitting bioluminescence but not from sections emitting no light. At an early stage of infection, no significant differences in the percentages of infected areas as determined by visual assessment were observed in any of the cultivars. However, differences among cultivars were detected by bioluminescence as the disease progressed, because bacterial invasion was not always accompanied by symptom expression. In susceptible cultivars, the advancing border of infection was 5 to 10 cm inward from the margins of the visible symptoms and often reached to the leaf petiole even when symptoms were visible in <10% of the total leaf area. Comparisons of anthurium cultivars in which a nondestructive method was used to quantify the severity of leaf infection by a bioluminescent pathogen have enabled us to evaluate susceptibility and resistance to bacterial blight accurately. Such evaluations will be of importance in breeding resistant cultivars for disease control.
PMCID: PMC1388810  PMID: 16535253
4.  Suppression of Bacterial Blight by a Bacterial Community Isolated from the Guttation Fluids of Anthuriums† 
Growth and survival of Xanthomonas campestris pv. dieffenbachiae in guttation fluids (xylem sap exuded from leaf margins) of anthuriums were suppressed by several bacterial strains indigenous to leaves of various anthurium cultivars. Inhibition of growth was not observed in filter-sterilized guttation fluids and was restored to original levels only by reintroducing specific mixtures of bacteria into filter-sterilized guttation fluids. The inhibitory effect was related to the species in the bacterial community rather than to the total numbers of bacteria in the guttation fluids. One very effective bacterial community consisted of five species isolated from inhibitory guttation fluids of two susceptible anthurium cultivars. The individual strains in this community had no effect on the pathogen, but the mixture was inhibitory to X. campestris pv. dieffenbachiae in guttation fluids. The populations of the individual strains remained near the initial inoculum levels for at least 14 days. The effect of the five inhibitory strains on reducing disease in susceptible anthurium plants was tested by using a bioluminescent strain of X. campestris pv. dieffenbachiae to monitor the progression of disease in leaves nondestructively. Invasion of the pathogen through hydathodes at leaf margins was reduced by applying the strain mixture to the leaves. When the strain mixture was applied directly to wounds created on the leaf margins, the pathogen failed to invade through the wounds. This bacterial community has potential for biological control of anthurium blight.
PMCID: PMC91139  PMID: 10049858
5.  A reassessment of Anthurium species with palmately divided leaves, and a reinterpretation of Anthurium section Dactylophyllium (Araceae) 
PhytoKeys  2013;41-54.
A reappraisal is made of the Anthurium Schott species with palmately divided leaves with 3 or more segments free to the base (i.e. palmatisect leaves), previously recognized as section Dactylophyllium Schott (Engler), as well as those species with 5 or more segments united at the base (i.e. palmatifid leaves), formerly placed in section Schizoplacium Schott (Engler). New molecular data indicates that several species (Anthurium pedatum (Kunth) Schott, Anthurium pedatoradiatum Schott, and possibly, Anthurium podophyllum (Schltdl. & Cham.) Kunth) should be excluded from section Schizoplacium, and other species previously placed in that section cannot be separated from section Dactylophyllium. Thus, Anthurium section Schizoplacium is here synonymized within section Dactylophyllium and type species are designated for both groups. This paper also provides an updated description of section Dactylophyllium as here emended, listing the 24 accepted taxa now included (20 species and 4 varieties or subspecies), along with their geographic distributions.
PMCID: PMC3690980  PMID: 23805054
Anthurium; molecular phylogeny; palmately divided leaves; palmatisect leaves; palmatifid leaves; section Schizoplacium; sectional classification
6.  Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse 
The house mouse (Mus musculus) is universally adopted as the mammalian laboratory model, and it is involved in most studies of large-scale comparative genomics. Paradoxically, this taxon is rarely the index species for evolutionary analyses of genome architecture owing to its highly rearranged karyotype. To unravel the origin and nature of this extensive repatterning genome, we performed a multidirectional chromosome painting study of representative species within the genus Mus. However, the latter includes four extant subgenera (Mus, Coelomys, Nannomys and Pyromys) between which the phylogenetic relationships remain elusive despite the numerous molecular studies. Comparative genomic maps were established using chromosome-specific painting probes of the laboratory mouse and Nannomys minutoides. Hence, by integrating closely related species within Mus, this study allowed us to: (i) unambiguously resolve for the first time the long-standing controversial phylogeny, (ii) trace the evolution of genome organization in the house mouse, (iii) track rearrangements that necessitated new centromere locations, i.e. formation of neocentromere or reactivation of latent centromeres, (iv) reveal an extremely high rate of karyotypic evolution, with a 10- to 30-fold acceleration which was coincidental with subgeneric cladogenesis and (v) highlight genomic areas of interest for high-resolution studies on neocentromere formation and synteny breakpoints.
PMCID: PMC1639516  PMID: 17015352
fluorescence in situ hybridization; phylogenomics; Mus; Nannomys; Coelomys; neocentromere
7.  Ralstonia solanacearum Strains from Martinique (French West Indies) Exhibiting a New Pathogenic Potential▿ †  
Applied and Environmental Microbiology  2007;73(21):6790-6801.
We investigated a destructive pathogenic variant of the plant pathogen Ralstonia solanacearum that was consistently isolated in Martinique (French West Indies). Since the 1960s, bacterial wilt of solanaceous crops in Martinique has been caused primarily by strains of R. solanacearum that belong to either phylotype I or phylotype II. Since 1999, anthurium shade houses have been dramatically affected by uncharacterized phylotype II strains that also affected a wide range of species, such as Heliconia caribea, cucurbitaceous crops, and weeds. From 1989 to 2003, a total of 224 R. solanacearum isolates were collected and compared to 6 strains isolated in Martinique in the 1980s. The genetic diversity and phylogenetic position of selected strains from Martinique were assessed (multiplex PCRs, mutS and egl DNA sequence analysis) and compared to the genetic diversity and phylogenetic position of 32 reference strains covering the known diversity within the R. solanacearum species complex. Twenty-four representative isolates were tested for pathogenicity to Musa species (banana) and tomato, eggplant, and sweet pepper. Based upon both PCR and sequence analysis, 119 Martinique isolates from anthurium, members of the family Cucurbitaceae, Heliconia, and tomato, were determined to belong to a group termed phylotype II/sequevar 4 (II/4). While these strains cluster with the Moko disease-causing strains, they were not pathogenic to banana (NPB). The strains belonging to phylotype II/4NPB were highly pathogenic to tomato, eggplant, and pepper, were able to wilt the resistant tomato variety Hawaii7996, and may latently infect cooking banana. Phylotype II/4NPB constitutes a new pathogenic variant of R. solanacearum that has recently appeared in Martinique and may be latently prevalent throughout Caribbean and Central/South America.
PMCID: PMC2074947  PMID: 17720825
8.  New hosts of Myrothecium SPP. In brazil and a preliminary In Vitro assay of fungicides 
Brazilian Journal of Microbiology  2010;41(1):246-252.
Myrothecium roridum and M. verrucaria are two plant pathogenic species causing foliar spots in a large number of cultivated plants. This paper aims to study the causal agents of foliar spots in vegetable crops (sweet pepper, tomato, cucumber), ornamental plants (Spathiphyllum, Solidago canadensis, Anthurium, Dieffenbachia) and a solanaceous weed plant (Nicandra physalodes). Most of the isolates were identified as M. roridum; only the isolate ‘Myr-02’ from S. canadensis was identified as M. verrucaria. All the isolates were pathogenic to their original plant hosts and also to some other plants. Some fungicides were tested in vitro against an isolate of M. roridum and the mycelial growth recorded after seven days. Fungicides with quartenary ammonium, Tebuconzole and copper were highly effective in inhibiting the mycelial growth of M. roridum. This paper confirms the first record of M. roridum causing leaf spots in sweet pepper, tomato, Spathiphyllum, Anthurium, Dieffenbachia and N. physalodes. We also report M. roridum as causal agent of cucumber fruit rot and also M. verrucaria in tango plants.
PMCID: PMC3768628  PMID: 24031487
Myrothecium roridum; M. verrucaria; vegetable crops; quorum sensing; weeds; etiology
9.  Characterization of Myrothecium roridum Isolated from Imported Anthurium Plant Culture Medium 
Mycobiology  2014;42(1):82-85.
During an investigation of microorganisms and pests in plant culture media from imported anthurium pots, a fungal isolate (DUCC4002) was detected. Based on its morphological characters including colony shape on potato dextrose agar, the microstructures of spores observed by light and scanning electron microscopy and the results of phylogenetic analysis using an internal transcribed spacer rDNA sequence, the fungal isolate was identified as Myrothecium roridum. Pathogenicity testing on anthurium leaves revealed that the fungus could colonize and produce sporodochia on the inoculated leaves. This is the first report of M. roridum detected in imported plant culture medium in Korea.
PMCID: PMC4004954  PMID: 24808740
Anthurium; Import; Myrothecium roridum; Plant culture medium
10.  Evolution of genome size in Carex (Cyperaceae) in relation to chromosome number and genomic base composition 
Annals of Botany  2012;111(1):79-94.
Background and Aims
The genus Carex exhibits karyological peculiarities related to holocentrism, specifically extremely broad and almost continual variation in chromosome number. However, the effect of these peculiarities on the evolution of the genome (genome size, base composition) remains unknown. While in monocentrics, determining the arithmetic relationship between the chromosome numbers of related species is usually sufficient for the detection of particular modes of karyotype evolution (i.e. polyploidy and dysploidy), in holocentrics where chromosomal fission and fusion occur such detection requires knowledge of the DNA content.
The genome size and GC content were estimated in 157 taxa using flow cytometry. The exact chromosome numbers were known for 96 measured samples and were taken from the available literature for other taxa. All relationships were tested in a phylogenetic framework using the ITS tree of 105 species.
Key Results
The 1C genome size varied between 0·24 and 1·64 pg in Carex secalina and C. cuspidata, respectively. The genomic GC content varied from 34·8 % to 40·6 % from C. secalina to C. firma. Both genomic parameters were positively correlated. Seven polyploid and two potentially polyploid taxa were detected in the core Carex clade. A strong negative correlation between genome size and chromosome number was documented in non-polyploid taxa. Non-polyploid taxa of the core Carex clade exhibited a higher rate of genome-size evolution compared with the Vignea clade. Three dioecious taxa exhibited larger genomes, larger chromosomes, and a higher GC content than their hermaphrodite relatives.
Genomes of Carex are relatively small and very GC-poor compared with other angiosperms. We conclude that the evolution of genome and karyotype in Carex is promoted by frequent chromosomal fissions/fusions, rare polyploidy and common repetitive DNA proliferation/removal.
PMCID: PMC3523652  PMID: 23175591
Agmatoploidy; AT/GC ratio; chromosomal fusion and fission; chromosome numbers; DNA content; flow cytometry; GC content; karyotype; phylogeny; polyploidy; symploidy
11.  Correlated evolution of LTR retrotransposons and genome size in the genus eleocharis 
BMC Plant Biology  2010;10:265.
Transposable elements (TEs) are considered to be an important source of genome size variation and genetic and phenotypic plasticity in eukaryotes. Most of our knowledge about TEs comes from large genomic projects and studies focused on model organisms. However, TE dynamics among related taxa from natural populations and the role of TEs at the species or supra-species level, where genome size and karyotype evolution are modulated in concert with polyploidy and chromosomal rearrangements, remain poorly understood. We focused on the holokinetic genus Eleocharis (Cyperaceae), which displays large variation in genome size and the occurrence of polyploidy and agmatoploidy/symploidy. We analyzed and quantified the long terminal repeat (LTR) retrotransposons Ty1-copia and Ty3-gypsy in relation to changes in both genome size and karyotype in Eleocharis. We also examined how this relationship is reflected in the phylogeny of Eleocharis.
Using flow cytometry, we measured the genome sizes of members of the genus Eleocharis (Cyperaceae). We found positive correlation between the independent phylogenetic contrasts of genome size and chromosome number in Eleocharis. We analyzed PCR-amplified sequences of various reverse transcriptases of the LTR retrotransposons Ty1-copia and Ty3-gypsy (762 sequences in total). Using real-time PCR and dot blot approaches, we quantified the densities of Ty1-copia and Ty3-gypsy within the genomes of the analyzed species. We detected an increasing density of Ty1-copia elements in evolutionarily younger Eleocharis species and found a positive correlation between Ty1-copia densities and C/n-values (an alternative measure of monoploid genome size) in the genus phylogeny. In addition, our analysis of Ty1-copia sequences identified a novel retrotransposon family named Helos1, which is responsible for the increasing density of Ty1-copia. The transition:transversion ratio of Helos1 sequences suggests that Helos1 recently transposed in later-diverging Eleocharis species.
Using several different approaches, we were able to distinguish between the roles of LTR retrotransposons, polyploidy and agmatoploidy/symploidy in shaping Eleocharis genomes and karyotypes. Our results confirm the occurrence of both polyploidy and agmatoploidy/symploidy in Eleocharis. Additionally, we introduce a new player in the process of genome evolution in holokinetic plants: LTR retrotransposons.
PMCID: PMC3095338  PMID: 21118487
12.  Chromosome diversity and evolution in Liliaceae 
Annals of Botany  2008;103(3):459-475.
Background and Aims
There is an extensive literature on the diversity of karyotypes found in genera within Liliaceae, but there has been no attempt to analyse these data within a robust phylogenetic framework. In part this has been due to a lack of consensus on which genera comprise Liliaceae and the relationships between them. Recently, however, this changed with the proposal for a relatively broad circumscription of Liliaceae comprising 15 genera and an improved understanding of the evolutionary relationships between them. Thus there is now the opportunity to examine patterns and trends in chromosome evolution across the family as a whole.
Based on an extensive literature survey, karyo-morphometric features for 217 species belonging to all genera in Liliaceae sensu the APG (Angiosperm Phylogeny Group) were obtained. Included in the data set were basic chromosome number, ploidy, chromosome total haploid length (THL) and 13 different measures of karyotype asymmetry. In addition, genome size estimates for all species studied were inferred from THLs using a power regression model constructed from the data set. Trends in karyotype evolution were analysed by superimposing the karyological data onto a phylogenetic framework for Liliaceae.
Key Results and Conclusions
Combining the large amount of data enabled mean karyotypes to be produced, highlighting marked differences in karyotype structure between the 15 genera. Further differences were noted when various parameters for analysing karyotype asymmetry were assessed. By examining the effects of increasing genome size on karyotype asymmetry, it was shown that in many but not all (e.g. Fritillaria and all of Tulipeae) species, the additional DNA was added preferentially to the long arms of the shorter chromosomes rather than being distributed across the whole karyotype. This unequal pattern of DNA addition is novel, contrasting with the equal and proportional patterns of DNA increase previously reported. Overall, the large-scale analyses of karyotype features within a well-supported phylogenetic framework enabled the most likely patterns of chromosome evolution in Liliaceae to be reconstructed, highlighting diverse modes of karyotype evolution, even within this comparatively small monocot family.
PMCID: PMC2707325  PMID: 19033282
C-value; chromosomes; genome size; karyotype asymmetry; karyotype evolution; Liliaceae; Liliales; polyploidy
13.  Phylogenetic Relationships of Palaearctic Formica Species (Hymenoptera, Formicidae) Based on Mitochondrial Cytochrome b Sequences 
PLoS ONE  2012;7(7):e41697.
Ants of genus Formica demonstrate variation in social organization and represent model species for ecological, behavioral, evolutionary studies and testing theoretical implications of the kin selection theory. Subgeneric division of the Formica ants based on morphology has been questioned and remained unclear after an allozyme study on genetic differentiation between 13 species representing all subgenera was conducted. In the present study, the phylogenetic relationships within the genus were examined using mitochondrial DNA sequences of the cytochrome b and a part of the NADH dehydrogenase subunit 6. All 23 Formica species sampled in the Palaearctic clustered according to the subgeneric affiliation except F. uralensis that formed a separate phylogenetic group. Unlike Coptoformica and Formica s. str., the subgenus Serviformica did not form a tight cluster but more likely consisted of a few small clades. The genetic distances between the subgenera were around 10%, implying approximate divergence time of 5 Myr if we used the conventional insect divergence rate of 2% per Myr. Within-subgenus divergence estimates were 6.69% in Serviformica, 3.61% in Coptoformica, 1.18% in Formica s. str., which supported our previous results on relatively rapid speciation in the latter subgenus. The phylogeny inferred from DNA sequences provides a necessary framework against which the evolution of social traits can be compared. We discuss implications of inferred phylogeny for the evolution of social traits.
PMCID: PMC3402446  PMID: 22911845
14.  Chromosomal diversification and karyotype evolution of diploids in the cytologically diverse genus Prospero (Hyacinthaceae) 
Prospero (Hyacinthaceae) provides a unique system to assess the impact of genome rearrangements on plant diversification and evolution. The genus exhibits remarkable chromosomal variation but very little morphological differentiation. Basic numbers of x = 4, 5, 6 and 7, extensive polyploidy, and numerous polymorphic chromosome variants were described, but only three species are commonly recognized: P. obtusifolium, P. hanburyi, and P. autumnale s.l., the latter comprising four diploid cytotypes. The relationship between evolutionary patterns and chromosomal variation in diploids, the basic modules of the extensive cytological diversity, is presented.
Evolutionary inferences were derived from fluorescence in situ hybridization (FISH) with 5S and 35S rDNA, genome size estimations, and phylogenetic analyses of internal transcribed spacer (ITS) of 35S rDNA of 49 diploids in the three species and all cytotypes of P. autumnale s.l. All species and cytotypes possess a single 35S rDNA locus, interstitial except in P. hanburyi where it is sub-terminal, and one or two 5S rDNA loci (occasionally a third in P. obtusifolium) at fixed locations. The localization of the two rDNA types is unique for each species and cytotype. Phylogenetic data in the P. autumnale complex enable tracing of the evolution of rDNA loci, genome size, and direction of chromosomal fusions: mixed descending dysploidy of x = 7 to x = 6 and independently to x = 5, rather than successive descending dysploidy, is proposed.
All diploid cytotypes are recovered as well-defined evolutionary lineages. The cytogenetic and phylogenetic approaches have provided excellent phylogenetic markers to infer the direction of chromosomal change in Prospero. Evolution in Prospero, especially in the P. autumnale complex, has been driven by differentiation of an ancestral karyotype largely unaccompanied by morphological change. These new results provide a framework for detailed analyses of various types of chromosomal rearrangements and karyotypic variation in polyploids.
PMCID: PMC3728210  PMID: 23819574
Chromosomal evolution; FISH; Genome size; Hyacinthaceae; ITS; Phylogeny; Prospero; rDNA
15.  Island species radiation and karyotypic stasis in Pachycladon allopolyploids 
Pachycladon (Brassicaceae, tribe Camelineae) is a monophyletic genus of ten morphologically and ecogeographically differentiated, and presumably allopolyploid species occurring in the South Island of New Zealand and in Tasmania. All Pachycladon species possess ten chromosome pairs (2n = 20). The feasibility of comparative chromosome painting (CCP) in crucifer species allows the origin and genome evolution in this genus to be elucidated. We focus on the origin and genome evolution of Pachycladon as well as on its genomic relationship to other crucifer species, particularly to the allopolyploid Australian Camelineae taxa. As species radiation on islands is usually characterized by chromosomal stasis, i.e. uniformity of chromosome numbers/ploidy levels, the role of major karyotypic reshuffling during the island adaptive and species radiation in Pachycladon is investigated through whole-genome CCP analysis.
The four analyzed Pachycladon species possess an identical karyotype structure. The consensual ancestral karyotype is most likely common to all Pachycladon species and corroborates the monophyletic origin of the genus evidenced by previous phylogenetic analyses. The ancestral Pachycladon karyotype (n = 10) originated through an allopolyploidization event between two genomes structurally resembling the Ancestral Crucifer Karyotype (ACK, n = 8). The primary allopolyploid (apparently with n = 16) has undergone genome reshuffling by descending dysploidy toward n = 10. Chromosome "fusions" were mediated by inversions, translocations and centromere inactivation/loss. Pachycladon chromosome 3 (PC3) resulted from insertional fusion, described in grasses. The allopolyploid ancestor originated in Australia, from the same or closely related ACK-like parental species as the Australian Camelineae allopolyploids. However, the two whole-genome duplication (WGD) events were independent, with the Pachycladon WGD being significantly younger. The long-distance dispersal of the diploidized Pachycladon ancestor to New Zealand was followed by the Pleistocene species radiation in alpine habitats and characterized by karyotypic stasis.
Karyotypic stasis in Pachycladon suggests that the insular species radiation in this genus proceeded through homoploid divergence rather than through species-specific gross chromosomal repatterning. The ancestral Pachycladon genome originated in Australia through an allopolyploidization event involving two closely related parental genomes, and spread to New Zealand by a long-distance dispersal. We argue that the chromosome number decrease mediated by inter-genomic reshuffling (diploidization) could provide the Pachycladon allopolyploid founder with an adaptive advantage to colonize montane/alpine habitats. The ancestral Pachycladon karyotype remained stable during the Pleistocene adaptive radiation into ten different species.
PMCID: PMC3014931  PMID: 21114825
16.  Chromosomal Locations of 5S and 45S rDNA in Gossypium Genus and Its Phylogenetic Implications Revealed by FISH 
PLoS ONE  2013;8(6):e68207.
We investigated the locations of 5S and 45S rDNA in Gossypium diploid A, B, D, E, F, G genomes and tetraploid genome (AD) using multi-probe fluorescent in situ hybridization (FISH) for evolution analysis in Gossypium genus. The rDNA numbers and sizes, and synteny relationships between 5S and 45S were revealed using 5S and 45S as double-probe for all species, and the rDNA-bearing chromosomes were identified for A, D and AD genomes with one more probe that is single-chromosome-specific BAC clone from G. hirsutum (A1D1). Two to four 45S and one 5S loci were found in diploid-species except two 5S loci in G. incanum (E4), the same as that in tetraploid species. The 45S on the 7th and 9th chromosomes and the 5S on the 9th chromosomes seemed to be conserved in A, D and AD genomes. In the species of B, E, F and G genomes, the rDNA numbers, sizes, and synteny relationships were first reported in this paper. The rDNA pattern agrees with previously reported phylogenetic history with some disagreements. Combined with the whole-genome sequencing data from G. raimondii (D5) and the conserved cotton karyotype, it is suggested that the expansion, decrease and transposition of rDNA other than chromosome rearrangements might occur during the Gossypium evolution.
PMCID: PMC3695094  PMID: 23826377
17.  Do Stacked Species Distribution Models Reflect Altitudinal Diversity Patterns? 
PLoS ONE  2012;7(3):e32586.
The objective of this study was to evaluate the performance of stacked species distribution models in predicting the alpha and gamma species diversity patterns of two important plant clades along elevation in the Andes. We modelled the distribution of the species in the Anthurium genus (53 species) and the Bromeliaceae family (89 species) using six modelling techniques. We combined all of the predictions for the same species in ensemble models based on two different criteria: the average of the rescaled predictions by all techniques and the average of the best techniques. The rescaled predictions were then reclassified into binary predictions (presence/absence). By stacking either the original predictions or binary predictions for both ensemble procedures, we obtained four different species richness models per taxa. The gamma and alpha diversity per elevation band (500 m) was also computed. To evaluate the prediction abilities for the four predictions of species richness and gamma diversity, the models were compared with the real data along an elevation gradient that was independently compiled by specialists. Finally, we also tested whether our richness models performed better than a null model of altitudinal changes of diversity based on the literature. Stacking of the ensemble prediction of the individual species models generated richness models that proved to be well correlated with the observed alpha diversity richness patterns along elevation and with the gamma diversity derived from the literature. Overall, these models tend to overpredict species richness. The use of the ensemble predictions from the species models built with different techniques seems very promising for modelling of species assemblages. Stacking of the binary models reduced the over-prediction, although more research is needed. The randomisation test proved to be a promising method for testing the performance of the stacked models, but other implementations may still be developed.
PMCID: PMC3292561  PMID: 22396782
18.  Rapid Evolution of Enormous, Multichromosomal Genomes in Flowering Plant Mitochondria with Exceptionally High Mutation Rates 
PLoS Biology  2012;10(1):e1001241.
A pair of species within the genus Silene have evolved the largest known mitochondrial genomes, coinciding with extreme changes in mutation rate, recombination activity, and genome structure.
Genome size and complexity vary tremendously among eukaryotic species and their organelles. Comparisons across deeply divergent eukaryotic lineages have suggested that variation in mutation rates may explain this diversity, with increased mutational burdens favoring reduced genome size and complexity. The discovery that mitochondrial mutation rates can differ by orders of magnitude among closely related angiosperm species presents a unique opportunity to test this hypothesis. We sequenced the mitochondrial genomes from two species in the angiosperm genus Silene with recent and dramatic accelerations in their mitochondrial mutation rates. Contrary to theoretical predictions, these genomes have experienced a massive proliferation of noncoding content. At 6.7 and 11.3 Mb, they are by far the largest known mitochondrial genomes, larger than most bacterial genomes and even some nuclear genomes. In contrast, two slowly evolving Silene mitochondrial genomes are smaller than average for angiosperms. Consequently, this genus captures approximately 98% of known variation in organelle genome size. The expanded genomes reveal several architectural changes, including the evolution of complex multichromosomal structures (with 59 and 128 circular-mapping chromosomes, ranging in size from 44 to 192 kb). They also exhibit a substantial reduction in recombination and gene conversion activity as measured by the relative frequency of alternative genome conformations and the level of sequence divergence between repeat copies. The evolution of mutation rate, genome size, and chromosome structure can therefore be extremely rapid and interrelated in ways not predicted by current evolutionary theories. Our results raise the hypothesis that changes in recombinational processes, including gene conversion, may be a central force driving the evolution of both mutation rate and genome structure.
Author Summary
A fundamental challenge in evolutionary biology is to explain why organisms exhibit dramatic variation in genome size and complexity. One hypothesis predicts that high rates of mutation in DNA sequence create selection against large and complex genomes, which are more susceptible to mutational disruption. Species of flowering plants in the genus Silene vary by approximately 100-fold in the rates of mutation in their mitochondrial DNA, providing an excellent opportunity to test the predicted effects of high mutation rates on genome evolution. Contrary to expectation, Silene species with elevated mutation rates have experienced dramatic expansions in mitochondrial genome size compared to their slowly evolving relatives, resulting in the largest known mitochondrial genomes. In addition to the increases in size and mutation rate, these genomes also reveal a history of rapid change in genome structure. They have been fragmented into dozens of chromosomes and appear to have experienced major reductions in recombination activity. All of these changes have occurred in just the past few million years. This mitochondrial genome diversity within the genus Silene provides a striking example of rapid genomic change and raises new hypotheses regarding the relationship between mutation rate and genome evolution.
PMCID: PMC3260318  PMID: 22272183
19.  The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae) 
Annals of Botany  2008;101(6):805-814.
In studies looking at individual polyploid species, the most common patterns of genomic change are that either genome size in the polyploid is additive (i.e. the sum of parental genome donors) or there is evidence of genome downsizing. Reports showing an increase in genome size are rare. In a large-scale analysis of 3008 species, genome downsizing was shown to be a widespread biological response to polyploidy. Polyploidy in the genus Nicotiana (Solanaceae) is common with approx. 40 % of the approx. 75 species being allotetraploid. Recent advances in understanding phylogenetic relationships of Nicotiana species and dating polyploid formation enable a temporal dimension to be added to the analysis of genome size evolution in these polyploids.
Genome sizes were measured in 18 species of Nicotiana (nine diploids and nine polyploids) ranging in age from <200 000 years to approx. 4·5 Myr old, to determine the direction and extent of genome size change following polyploidy. These data were combined with data from genomic in situ hybridization and increasing amounts of information on sequence composition in Nicotiana to provide insights into the molecular basis of genome size changes.
Key Results and Conclusions
By comparing the expected genome size of the polyploid (based on summing the genome size of species identified as either a parent or most closely related to the diploid progenitors) with the observed genome size, four polyploids showed genome downsizing and five showed increases. There was no discernable pattern in the direction of genome size change with age of polyploids, although with increasing age the amount of genome size change increased. In older polyploids (approx. 4·5 million years old) the increase in genome size was associated with loss of detectable genomic in situ hybridization signal, whereas some hybridization signal was still detected in species exhibiting genome downsizing. The possible significance of these results is discussed.
PMCID: PMC2710205  PMID: 18222910
Genome downsizing; genome size; Nicotiana; polyploidy; sequence elimination; Solanaceae
20.  Testing Phylogenetic Hypotheses of the Subgenera of the Freshwater Crayfish Genus Cambarus (Decapoda: Cambaridae) 
PLoS ONE  2012;7(9):e46105.
The genus Cambarus is one of three most species rich crayfish genera in the Northern Hemisphere. The genus has its center of diversity in the Southern Appalachians of the United States and has been divided into 12 subgenera. Using Cambarus we test the correspondence of subgeneric designations based on morphology used in traditional crayfish taxonomy to the underlying evolutionary history for these crayfish. We further test for significant correlation and explanatory power of geographic distance, taxonomic model, and a habitat model to estimated phylogenetic distance with multiple variable regression.
Methodology/Principal Findings
We use three mitochondrial and one nuclear gene regions to estimate the phylogenetic relationships for species within the genus Cambarus and test evolutionary hypotheses of relationships and associated morphological and biogeographical hypotheses. Our resulting phylogeny indicates that the genus Cambarus is polyphyletic, however we fail to reject the monophyly of Cambarus with a topology test. The majority of the Cambarus subgenera are rejected as monophyletic, suggesting the morphological characters used to define those taxa are subject to convergent evolution. While we found incongruence between taxonomy and estimated phylogenetic relationships, a multiple model regression analysis indicates that taxonomy had more explanatory power of genetic relationships than either habitat or geographic distance.
We find convergent evolution has impacted the morphological features used to delimit Cambarus subgenera. Studies of the crayfish genus Orconectes have shown gonopod morphology used to delimit subgenera is also affected by convergent evolution. This suggests that morphological diagnoses based on traditional crayfish taxonomy might be confounded by convergent evolution across the cambarids and has little utility in diagnosing relationships or defining natural groups. We further suggest that convergent morphological evolution appears to be a common occurrence in invertebrates suggesting the need for careful phylogenetically based interpretations of morphological evolution in invertebrate systematics.
PMCID: PMC3458831  PMID: 23049950
21.  Chromosome pairing affinities in interspecific hybrids reflect phylogenetic distances among lady's slipper orchids (Paphiopedilum) 
Annals of Botany  2011;108(1):113-121.
Background and Aims
Lady's slipper orchids (Paphiopedilum) are of high value in floriculture, and interspecific hybridization has long been used for breeding improved cultivars; however, information regarding the genome affinities of species and chromosome pairing behaviour of the hybrids remains almost unknown. The present work analyses the meiotic behaviour of interspecific hybrids by genomic in situ hybridization and cytologically evaluates the genomic relationships among parental species.
Eight interspecific F1 hybrids of Paphiopedilum species in various subgenera or sections were investigated in this study. The chromosome behaviour in meiosis of these interspecific hybrids was analysed and subjected to genomic in situ hybridization and fluorescent in situ hybridization.
Key Results
Genomic in situ hybridization was demonstrated as an efficient method to differentiate between Paphiopedilum genomes and to visualize the chromosome pairing affinities in interspecific F1 hybrids, clarifying the phylogenetic distances among these species. Comparatively regular chromosome pairing observed in the hybrids of P. delenatii × P. bellatulum, P. delenatii × P. rothschildianum and P. rothschildianum × P. bellatulum suggested high genomic affinities and close relationships between parents of each hybrid. In contrast, irregular chromosome associations, such as univalents, trivalents and quadrivalents occurred frequently in the hybrids derived from distant parents with divergent karyotypes, such as P. delenatii × P. callosum, P. delenatii × P. glaucophyllum, P. rothschildianum × P. micranthum and P. rothschildianum × P. moquetteanum. The existence of multivalents and autosyndesis demonstrated by genomic in situ hybridization in this study indicates that some micro-rearrangements and other structural alterations may also play a part in differentiating Paphiopedilum species at chromosomal level, demonstrated as different chromosome pairing affinities in interspecific hybrids.
The results indicate that genome homology and the interaction of genetic factors, but not chromosome number nor karyotype similarity, determine the chromosome pairing behaviour in Paphiopedilum hybrids.
PMCID: PMC3119621  PMID: 21576078
Paphiopedilum; homeologous pairing; autosyndesis; genomic in situ hybridization; pollen formation
22.  Genome Size Variation and Species Relationships in Hieracium Sub-genus Pilosella (Asteraceae) as Inferred by Flow Cytometry 
Annals of Botany  2007;100(6):1323-1335.
Background and Aims
Hieracium sub-genus Pilosella (hawkweeds) is a taxonomically complicated group of vascular plants, the structure of which is substantially influenced by frequent interspecific hybridization and polyploidization. Two kinds of species, ‘basic’ and ‘intermediate’ (i.e. hybridogenous), are usually recognized. In this study, genome size variation was investigated in a representative set of Central European hawkweeds in order to assess the value of such a data set for species delineation and inference of evolutionary relationships.
Holoploid and monoploid genome sizes (C- and Cx-values) were determined using propidium iodide flow cytometry for 376 homogeneously cultivated individuals of Hieracium sub-genus Pilosella, including 24 species (271 individuals), five recent natural hybrids (seven individuals) and experimental F1 hybrids from four parental combinations (98 individuals). Chromosome counts were available for more than half of the plant accessions. Base composition (proportion of AT/GC bases) was cytometrically estimated in 73 individuals.
Key Results
Seven different ploidy levels (2x–8x) were detected, with intraspecific ploidy polymorphism (up to four different cytotypes) occurring in 11 wild species. Mean 2C-values varied approx. 4·3-fold from 3·53 pg in diploid H. hoppeanum to 15·30 pg in octoploid H. brachiatum. 1Cx-values ranged from 1·72 pg in H. pilosella to 2·16 pg in H. echioides (1·26-fold). The DNA content of (high) polyploids was usually proportional to the DNA values of their diploid/low polyploid counterparts, indicating lack of processes altering genome size (i.e. genome down-sizing). Most species showed constant nuclear DNA amounts, exceptions being three hybridogenous taxa, in which introgressive hybridization was suggested as a presumable trigger for genome size variation. Monoploid genome sizes of hybridogenous species were always between the corresponding values of their putative parents. In addition, there was a good congruency between actual DNA estimates and theoretical values inferred from putative parental combinations and between DNA values of experimental F1 hybrids and corresponding established hybridogenous taxa.
Significant differences in genome size between hawkweed species from hybridogenous lineages involving the small-genome H. pilosella document the usefulness of nuclear DNA content as a supportive marker for reliable delineation of several of the most problematic taxa in Hieracium sub-genus Pilosella (including classification of borderline morphotypes). In addition, genome size data were shown to have a good predictive value for inferring evolutionary relationships and genome constitution (i.e. putative parental combinations) in hybridogenous species.
PMCID: PMC2759259  PMID: 17921526
Agamic complex; AT/GC base ratio; DNA C-value; flow cytometry; genome composition; genome size; hawkweeds; Hieracium sub-genus Pilosella; hybridization; nuclear DNA content; polyploidy; taxonomy
23.  Environmental adaptation in stomatal size independent of the effects of genome size 
The New Phytologist  2014;205(2):608-617.
Cell sizes are linked across multiple tissues, including stomata, and this variation is closely correlated with genome size. These associations raise the question of whether generic changes in cell size cause suboptimal changes in stomata, requiring subsequent evolution under selection for stomatal size. We tested the relationships among guard cell length, genome size and vegetation type using phylogenetically independent analyses on 67 species of the ecologically and structurally diverse family, Proteaceae. We also compared how genome and stomatal sizes varied at ancient (among genera) and more recent (within genus) levels. The observed 60-fold range in genome size in Proteaceae largely reflected the mean chromosome size. Compared with variation among genera, genome size varied much less within genera (< 6% of total variance) than stomatal size, implying evolution in stomatal size subsequent to changes in genome size. Open vegetation and closed forest had significantly different relationships between stomatal and genome sizes. Ancient changes in genome size clearly influenced stomatal size in Proteaceae, but adaptation to habitat strongly modified the genome–stomatal size relationship. Direct adaptation to the environment in stomatal size argues that new proxies for past concentrations of atmospheric CO2 that incorporate stomatal size are superior to older models based solely on stomatal frequency.
PMCID: PMC4301182  PMID: 25266914
adaptation; cell size; chromosome size; CO 2; genome size; palaeoproxy; Proteaceae; stomata
24.  Did Genetic Drift Drive Increases in Genome Complexity? 
PLoS Genetics  2010;6(8):e1001080.
Mechanisms underlying the dramatic patterns of genome size variation across the tree of life remain mysterious. Effective population size (Ne) has been proposed as a major driver of genome size: selection is expected to efficiently weed out deleterious mutations increasing genome size in lineages with large (but not small) Ne. Strong support for this model was claimed from a comparative analysis of Neu and genome size for ≈30 phylogenetically diverse species ranging from bacteria to vertebrates, but analyses at that scale have so far failed to account for phylogenetic nonindependence of species. In our reanalysis, accounting for phylogenetic history substantially altered the perceived strength of the relationship between Neu and genomic attributes: there were no statistically significant associations between Neu and gene number, intron size, intron number, the half-life of gene duplicates, transposon number, transposons as a fraction of the genome, or overall genome size. We conclude that current datasets do not support the hypothesis of a mechanistic connection between Ne and these genomic attributes, and we suggest that further progress requires larger datasets, phylogenetic comparative methods, more robust estimators of genetic drift, and a multivariate approach that accounts for correlations between putative explanatory variables.
Author Summary
Genome size (the amount of nuclear DNA) varies tremendously across organisms but is not necessarily correlated with organismal complexity. For example, genome sizes just within the grasses vary nearly 20-fold, but large-genomed grass species are not obviously more complex in terms of morphology or physiology than are the small-genomed species. Recent explanations for genome size variation have instead been dominated by the idea that population size determines genome size: mutations that increase genome size are expected to drift to fixation in species with small populations, but such mutations would be eliminated in species with large populations where natural selection operates at higher efficiency. However, inferences from previous analyses are limited because they fail to recognize that species share evolutionary histories and thus are not necessarily statistically independent. Our analysis takes a phylogenetic perspective and, contrary to previous studies, finds no evidence that genome size or any of its components (e.g., transposon number, intron number) are related to population size. We suggest that genome size evolution is unlikely to be neatly explained by a single factor such as population size.
PMCID: PMC2928810  PMID: 20865118
25.  Genome Evolution in the Genus Sorghum (Poaceae) 
Annals of Botany  2005;95(1):219-227.
• Background and Aims The roles of variation in DNA content in plant evolution and adaptation remain a major biological enigma. Chromosome number and 2C DNA content were determined for 21 of the 25 species of the genus Sorghum and analysed from a phylogenetic perspective.
• Methods DNA content was determined by flow cytometry. A Sorghum phylogeny was constructed based on combined nuclear ITS and chloroplast ndhF DNA sequences.
• Key Results Chromosome counts (2n = 10, 20, 30, 40) were, with few exceptions, concordant with published numbers. New chromosome numbers were obtained for S. amplum (2n = 30) and S. leiocladum (2n = 10). 2C DNA content varies 8·1-fold (1·27–10·30 pg) among the 21 Sorghum species. 2C DNA content varies 3·6-fold from 1·27 pg to 4·60 pg among the 2n = 10 species and 5·8-fold (1·52–8·79 pg) among the 2n = 20 species. The x = 5 genome size varies over an 8·8-fold range from 0·26 pg to 2·30 pg. The mean 2C DNA content of perennial species (6·20 pg) is significantly greater than the mean (2·92 pg) of the annuals. Among the 21 species studied, the mean x = 5 genome size of annuals (1·15 pg) and of perennials (1·29 pg) is not significantly different. Statistical analysis of Australian species showed: (a) mean 2C DNA content of annual (2·89 pg) and perennial (7·73 pg) species is significantly different; (b) mean x = 5 genome size of perennials (1·66 pg) is significantly greater than that of the annuals (1·09 pg); (c) the mean maximum latitude at which perennial species grow (−25·4 degrees) is significantly greater than the mean maximum latitude (−17·6) at which annual species grow.
• Conclusions The DNA sequence phylogeny splits Sorghum into two lineages, one comprising the 2n = 10 species with large genomes and their polyploid relatives, and the other with the 2n = 20, 40 species with relatively small genomes. An apparent phylogenetic reduction in genome size has occurred in the 2n = 10 lineage. Genome size evolution in the genus Sorghum apparently did not involve a ‘one way ticket to genomic obesity’ as has been proposed for the grasses.
PMCID: PMC4246720  PMID: 15596469
Sorghum bicolor; wild sorghum; genome size; DNA content; chromosome numbers; systematics

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