Permanent Translocation Heterozygosity Research Articles

Outcrossing rates in the permanent translocation heterozygote Oenothera biennis L. (Onagraceae)

In species that primarily reproduce asexually, occasional sex can have important evolutionary consequences. Many plant species in the genus Oenothera have a genetic system called permanent translocation heterozygosity (PTH), which renders plants functionally asexual when they self-fertilize. PTH results from reciprocal translocations of chromosomes that suppress recombination and a balanced lethal mortality of homozygous gametes that prevents independent assortment of alleles. When PTH plants self-fertilize, the offspring are genetically identical to the parents, but when they outcross they can create new genotypes. Here, we sought to determine the outcrossing rate of natural populations of PTH Oenothera biennis L. (Onagraceae). We genotyped 46 parents from 14 populations in Tompkins County, NY, USA, and 754 of their offspring at highly polymorphic microsatellite loci. 99.5% of offspring were genetically identical to their seed parents, whereas 4 offspring out of 754 exhibited allelic mismatches with their seed parent. The estimated outcrossing rate ranged from 0.1% to 0.4%. Our study design also permitted us to estimate mutation rate of microsatellite loci, which ranged from 1.33 × 10−3 to 3.98 × 10−3. These results show that O. biennis typically exhibits a functionally asexual genetic system, but rare outcrossing events can generate novel genotypes that may have important evolutionary consequences.

Migration of repetitive DNAs during evolution of the permanent translocation heterozygosity in the oyster plant (Tradescantia section Rhoeo)

Due to translocation heterozygosity for all chromosomes in the cell complement, the oyster plant (Tradescantia spathacea) forms a complete meiotic ring. It also shows Rabl-arrangement at interphase, featured by polar centromere clustering. We demonstrate that the pericentromeric regions of the oyster plant are homogenized in concert by three subtelomeric sequences: 45S rDNA, (TTTAGGG)n motif, and TSrepI repeat. The Rabl-based clustering of pericentromeric regions may have been an excellent device to combine the subtelomere-pericentromere sequence migration (via inversions) with the pericentromere-pericentromere DNA movement (via whole arm translocations) that altogether led to the concerted homogenization of all the pericentromeric domains by the subtelomeric sequences. We also show that the repetitive sequence landscape of interstitial chromosome regions contains many loci consisting of Arabidopsis-type telomeric sequence or of TSrepI repeat, and it is extensively heterozygous. However, the sequence arrangement on some chromosomal arms suggest segmental inversions that are fully or partially homozygous, a fact that could be explained if the inversions started to create linkages already in a bivalent-forming ancestor. Remarkably, the subterminal TSrepI loci reside exclusively on the longer arms that could be due to sharing sequences between similarly-sized chromosomal arms in the interphase nucleus. Altogether, our study spotlights the supergene system of the oyster plant as an excellent model to link complex chromosome rearrangements, evolution of repetitive sequences, and nuclear architecture.

Target Enrichment and Extensive Population Sampling Help Untangle the Recent, Rapid Radiation of Oenothera Sect. Calylophus.

Oenothera sect. Calylophus is a North American group of 13 recognized taxa in the evening primrose family (Onagraceae) with an evolutionary history that may include independent origins of bee pollination, edaphic endemism, and permanent translocation heterozygosity. Like other groups that radiated relatively recently and rapidly, taxon boundaries within Oenothera sect. Calylophus have remained challenging to circumscribe. In this study, we used target enrichment, flanking noncoding regions, gene tree/species tree methods, tests for gene flow modified for target-enrichment data, and morphometric analysis to reconstruct phylogenetic hypotheses, evaluate current taxon circumscriptions, and examine character evolution in Oenothera sect. Calylophus. Because sect. Calylophus comprises a clade with a relatively restricted geographic range, we were able to extensively sample across the range of geographic, edaphic, and morphological diversity in the group. We found that the combination of exons and flanking noncoding regions led to improved support for species relationships. We reconstructed potential hybrid origins of some accessions and note that if processes such as hybridization are not taken into account, the number of inferred evolutionary transitions may be artificially inflated. We recovered strong evidence for multiple evolutionary origins of bee pollination from ancestral hawkmoth pollination, edaphic specialization on gypsum, and permanent translocation heterozygosity. This study applies newly emerging techniques alongside dense infraspecific sampling and morphological analyses to effectively reconstruct the recalcitrant history of a rapid radiation. [Gypsum endemism; Oenothera sect. Calylophus; Onagraceae; phylogenomics; pollinator shift; recent radiation; target enrichment.].

Fitness consequences of occasional outcrossing in a functionally asexual plant (Oenothera biennis).

Many clonal organisms occasionally outcross, but the long-term consequences of such infrequent events are often unknown. During fiveyears, representing three to five plant generations, we followed 16 experimental field populations of the forb, Oenothera biennis, originally planted with the same 18 original genotypes. Oenothera biennis usually self fertilizes, which, due to its genetic system (permanent translocation heterozygosity), results in seeds that are clones of the maternal plant. However, rare outcrossing produces genetically novel offspring (but without recombination or increased heterozygosity). We sought to understand whether novel genotypes produced through natural outcrossing had greater fecundity or different multigenerational dynamics compared to our original genotypes. We further assessed whether any differences in fitness or abundances through time between original and novel genotypes were exaggerated in the presence vs. absence of insect herbivores. Over the course of the experiment, we genotyped >12,500 plants using microsatellite DNA markers to identify and track the frequency of specific genotypes and estimated fecundity on a subset (>3,000) of plants. The effective outcrossing rate was 7.3% in the first year and ultimately 50% of the plants were of outcrossed origin by the final year of the experiment. Lifetime fruit production per plant was on average 32% higher across all novel genotypes produced via outcrossing compared to the original genotypes, and this fecundity advantage was significantly enhanced in populations lacking herbivores. Among 43 novel genotypes that were abundant enough to phenotype with replication, plants produced nearly 30% more fruits than the average of their specific two parental genotypes, and marginally more fruits (8%) than their most fecund parent. Mean per capita fecundity of novel genotypes predicted their relative frequencies at the end of the experiment. Novel genotypes increased more dramatically in herbivore-present compared to suppressed populations (45% vs. 27% of all plants), countering the increased competition from dandelions (Taraxacum officinale) that resulted from herbivore suppression. Increased interspecific competition likely also lead to the lower realized fitness of novel vs. original genotypes in herbivore-suppressed populations. These results demonstrate that rare outcrossing and the generation of novel genotypes can create high-fecundity progeny, with the biotic environment influencing the dynamical outcome of such advantages.

Recurrent Loss of Sex Is Associated with Accumulation of Deleterious Mutations in Oenothera

Sexual reproduction is nearly universal among eukaryotes. Theory predicts that the rarity of asexual eukaryotic species is in part caused by accumulation of deleterious mutations and heightened extinction risk associated with suppressed recombination and segregation in asexual species. We tested this prediction with a large data set of 62 transcriptomes from 29 species in the plant genus Oenothera, spanning ten independent transitions between sexual and a functionally asexual genetic system called permanent translocation heterozygosity. Illumina short-read sequencing and de novo transcript assembly yielded an average of 16.4 Mb of sequence per individual. Here, we show that functionally asexual species accumulate more deleterious mutations than sexual species using both population genomic and phylogenetic analysis. At an individual level, asexual species exhibited 1.8 × higher heterozygosity than sexual species. Within species, we detected a higher proportion of nonsynonymous polymorphism relative to synonymous variation within asexual compared with sexual species, indicating reduced efficacy of purifying selection. Asexual species also exhibited a greater proportion of transcripts with premature stop codons. The increased proportion of nonsynonymous mutations was also positively correlated with divergence time between sexual and asexual species, consistent with Muller's ratchet. Between species, we detected repeated increases in the ratio of nonsynonymous to synonymous divergence in asexual species compared with sexually reproducing sister taxa, indicating increased accumulation of deleterious mutations. These results confirm that an important advantage of sex is that it facilitates selection against deleterious alleles, which might help to explain the dearth of extant asexual species.

Effects of functionally asexual reproduction on quantitative genetic variation in the evening primroses (Oenothera, Onagraceae).

It has long been predicted that a loss of sexual reproduction leads to decreased heritable variation within populations and increased differentiation between populations. Despite an abundance of theory, there are few empirical tests of how sex affects genetic variation in phenotypic traits, especially for plants. Here we test whether repeated losses of two critical components of sex (recombination and segregation) in the evening primroses (Oenothera L., Onagraceae) affect quantitative genetic variation within and between populations. We sampled multiple genetic families from 3-5 populations from each of eight Oenothera species, which represented four independent transitions between sexual reproduction and a functionally asexual genetic system called "permanent translocation heterozygosity." We used quantitative genetics methods to partition genetic variation within and between populations for eight plant traits related to growth, leaf physiology, flowering, and resistance to herbivores. Heritability was, on average, 74% higher in sexual Oenothera populations than in functionally asexual populations, with plant growth rate, specific leaf area, and the percentage of leaf water content showing the strongest differences. By contrast, genetic differentiation among populations was 2.8× higher in functionally asexual vs. sexual Oenothera species. This difference was particularly strong for specific leaf area. Sexual populations tended to exhibit higher genetic correlations among traits, but this difference was weakly supported. These results support the prediction that sexual reproduction maintains higher genetic variation within populations, which may facilitate adaptive evolution. We also found partial support for the prediction that a loss of sex leads to greater population differentiation, which may elevate speciation rates.

Translocations of Chromosome End-Segments and Facultative Heterochromatin Promote Meiotic Ring Formation in Evening Primroses

Due to reciprocal chromosomal translocations, many species of Oenothera (evening primrose) form permanent multichromosomal meiotic rings. However, regular bivalent pairing is also observed. Chiasmata are restricted to chromosomal ends, which makes homologous recombination virtually undetectable. Genetic diversity is achieved by changing linkage relations of chromosomes in rings and bivalents via hybridization and reciprocal translocations. Although the structural prerequisite for this system is enigmatic, whole-arm translocations are widely assumed to be the mechanistic driving force. We demonstrate that this prerequisite is genome compartmentation into two epigenetically defined chromatin fractions. The first one facultatively condenses in cycling cells into chromocenters negative both for histone H3 dimethylated at lysine 4 and for C-banding, and forms huge condensed middle chromosome regions on prophase chromosomes. Remarkably, it decondenses in differentiating cells. The second fraction is euchromatin confined to distal chromosome segments, positive for histone H3 lysine 4 dimethylation and for histone H3 lysine 27 trimethylation. The end-segments are deprived of canonical telomeres but capped with constitutive heterochromatin. This genomic organization promotes translocation breakpoints between the two chromatin fractions, thus facilitating exchanges of end-segments. We challenge the whole-arm translocation hypothesis by demonstrating why reciprocal translocations of chromosomal end-segments should strongly promote meiotic rings and evolution toward permanent translocation heterozygosity. Reshuffled end-segments, each possessing a major crossover hot spot, can furthermore explain meiotic compatibility between genomes with different translocation histories.

Tradescantia spathacea (syn. Rhoeo spathacea). A review / Cytogenetyka Tradescantia spathace (syn. Rhoeo spathacea). Artykuł przeglądowy

As a favorable PTH (permanent translocation heterozygosity) model, Tradescantia spathacea (synon. Rhoeo spathacea) offers an unusual opportunity to address crucial cytogenetic problems, among them complex chromosome rearrangements, recognition and segregation of translocated genome parts, the relation of crossing-over to synaptic processes. Here I present the existing knowledge on T. spathacea with the intention to reestablish it for advanced cytogenetic research.

Microevolution and invasiveness of Oenothera L. species (subsect. Oenothera, Onagraceae) in Europe

A comparative analysis of Oenothera’s hybrid species was carried out. The genus Oenothera L. (subsect. Oenothera, Onagraceae) is one of the most widespread American genera in Europe. These species possess a special breeding system (permanent translocation heterozygosity) which promotes the hybridization (also introgressive one) among any species resulting in formation of a hybrid with a constant complex of morphological characteristics.

Uncoupling of sexual reproduction from homologous recombination in homozygous Oenothera species

Salient features of the first meiotic division are independent segregation of chromosomes and homologous recombination (HR). In non-sexually reproducing, homozygous species studied to date HR is absent. In this study, we constructed the first linkage maps of homozygous, bivalent-forming Oenothera species and provide evidence that HR was exclusively confined to the chromosome ends of all linkage groups in our population. Co-segregation of complementary DNA-based markers with the major group of AFLP markers indicates that HR has only a minor role in generating genetic diversity of this taxon despite its efficient adaptation capability. Uneven chromosome condensation during meiosis in Oenothera may account for restriction of HR. The use of plants with ancient chromosomal arm arrangement demonstrates that limitation of HR occurred before and independent from species hybridizations and reciprocal translocations of chromosome arms—a phenomenon, which is widespread in the genus. We propose that consecutive loss of HR favored the evolution of reciprocal translocations, beneficial superlinkage groups and ultimately permanent translocation heterozygosity.

The arrangement of pericentromeres during meiotic prophase I in the permanent translocation heterozygoteRhoeo spathacea

Abstract A study on the organization of prophase I chromatin in a PTH (permanent translocation heterozygosity) plant -Rhoeo spathacea was carried out. The sequential DAPI/AMD-FISH technique showed that nuclear polarization and centromere clustering during preleptotene-pachytene is a striking feature of all the studied heterozygotic clones. It was revealed that during pachytene pericentromeric heterochromatins assemble into a strikingly regular continuous ring with empty space inside. The topological constraints exerted by the heterochromatic pachytene “ring” exclude both random and multiple centromere interactions, and together with peripheral disposition of GC-rich pericentromeric regions and their reduced number, conform to a condition where one pericentromere interacts side-by-side with its two neighbors. The relation of the meiotic centromere associations in Rhoeo to the processes regulating chromosome arm juxtaposition (e.g. synapsis) and/or segregation was discussed.

Meiotic events inOenothera — a non-standard pattern of chromosome behaviour

The genus Oenothera shows an intriguing extent of permanent translocation heterozygosity. Reciprocal translocations of chromosome arms in species or populations result in various kinds of chromosome multivalents in diakinesis. Early meiotic events conditioning such chromosome behaviour are poorly understood. We found a surprising uniformity of the leptotene-diplotene period, regardless of the chromosome configuration at diakinesis (ring of 14, 7 bivalents, mixture of bivalents and multivalents). It appears that the earliest chromosome interactions at Oenothera meiosis are untypical, since they involve pericentromeric regions. During early leptotene, proximal chromosome parts cluster and form a highly polarized Rabl configuration. Telomeres associated in pairs were seen at zygotene. The high degree of polarization of meiotic nuclei continues for an exceptionally long period, i.e., during zygotene-pachytene into the diplotene contraction stage. The Rabl-polarized meiotic architecture and clustering of pericentromeres suggest a high complexity of karyotypes, not only in structural heterozygotes but also in bivalent-forming homozygous species.

The complete nucleotide sequences of the five genetically distinct plastid genomes of Oenothera, subsection Oenothera: I. sequence evaluation and plastome evolution.

The flowering plant genus Oenothera is uniquely suited for studying molecular mechanisms of speciation. It assembles an intriguing combination of genetic features, including permanent translocation heterozygosity, biparental transmission of plastids, and a general interfertility of well-defined species. This allows an exchange of plastids and nuclei between species often resulting in plastome–genome incompatibility. For evaluation of its molecular determinants we present the complete nucleotide sequences of the five basic, genetically distinguishable plastid chromosomes of subsection Oenothera (=Euoenothera) of the genus, which are associated in distinct combinations with six basic genomes. Sizes of the chromosomes range from 163 365 bp (plastome IV) to 165 728 bp (plastome I), display between 96.3% and 98.6% sequence similarity and encode a total of 113 unique genes. Plastome diversification is caused by an abundance of nucleotide substitutions, small insertions, deletions and repetitions. The five plastomes deviate from the general ancestral design of plastid chromosomes of vascular plants by a subsection-specific 56 kb inversion within the large single-copy segment. This inversion disrupted operon structures and predates the divergence of the subsection presumably 1 My ago. Phylogenetic relationships suggest plastomes I–III in one clade, while plastome IV appears to be closest to the common ancestor.

Invasiveness of Oenothera congeners alien to Europe: Jack of all trades, master of invasion?

Abstract The genus Oenothera includes a number of species alien to central Europe, which differ in their invasion success. The present study was designed to investigate how fecundity, growth rate of seedlings and competitive ability contribute to the invasion potential within this genus. The relative growth rate and response to interspecific competition from neighbouring vegetation were determined for 15 species. Relations between these characteristics and other species traits identified in previous studies (germination, seed production and seed mass) were examined and used to explain the invasion success of particular species in Europe. Ability to germinate in the light was the only significant predictor of invasion success in six European countries. Fecundity is another trait contributing to invasion success. The most successful invaders within the genus are poor at competing with native vegetation, and an ability to escape from competition seems crucial for invasion success. Oenothera biennis , the most successful invader, is not outstanding in any of the characteristics assessed but is well placed in most of them. We suggest that a ‘Jack-of-all-trades’ strategy may be beneficial for an invader. The parental chromosomes of the species studied had no effect on the distribution of traits; hence the conclusions drawn at the species level are not biased by the specific banding pattern within the genus (permanent translocation heterozygosity). The present study indicates that comparative studies of closely related species may indicate the determinants of invasion success if they include many characteristics of the complete life cycle.

Chromosomal variation in plant evolution

Chromosomal variation in plant evolution

Permanent translocation heterozygosity in dioecious Baccharis coridifolia DC. (Asteraceae).

The karyotype of Baccharis coridifolia DC., a dioecious diploid species consists of 16 chromosomes with median (m) and 2 with submedian centromeric positions (sm) (2n = 18). Meiotic analyses of 219 male plants belonging to 12 populations showed across a wide geographical range one quadrivalent and seven bivalents in all of them. The quadrivalent involves the four biggest m chromosomes and probably constitutes a sex multivalent carrying in tight linkage the sex genes and provides a mechanism whereby permanent translocation heterozygosity is maintained. In metaphase I alternate orientation of the quadrivalent was predominant (85.71%). Fourteen megaspore mother cells were analyzed and did not show the quadrivalent. A model for the origin and maintenance of the sexual translocation system is presented. It is assumed that there are two non-allelic factors M and n; M would be a dominant female suppresor and n a recessive male-suppresor. The excess of male plants observed in several populations at different localities might result from heterotic effects of some gene complexes carried by the translocation. This excess probably ensures a good supply of pollen for the vagaries of insect pollination at flowering time.

Sex-determining and floating translocation complexes in Viscum cruciatum Sieber ex Boiss. (Viscaceae) in southern Spain. Some evolutionary and ecological comments

Abstract As in other dioecious species of Viscum, males of V. cruciatum always produce large rings of chromosomes during meiosis due to the existence of permanent translocation heterozygosity. Only rings often (and very rarely 12) chromosomes have been found in this species, probably a relative of V. album in the Mediterranean area. Females form bivalents. Another two floating translocations—not sex-associated and affecting different chromosomes—have been observed in both male and female plants in some populations. These produce meiotic configurations previously unrecorded in Viscum . This floating heterozygosity seems to be correlated with the aptitude of V. cruciatum to develop on different hosts, especially Prunus . All studied populations showed an excess of female plants, perhaps partly due to facultative agamospermy.

Sex-determining and floating translocation complexes in Viscum cruciatum Sieber ex Boiss. (Viscaceae) in southern Spain. Some evolutionary and ecological comments

As in other dioecious species of Viscum, males of V. cruciatum always produce large rings of chromosomes during meiosis due to the existence of permanent translocation heterozygosity. Only rings often (and very rarely 12) chromosomes have been found in this species, probably a relative of V. album in the Mediterranean area. Females form bivalents. Another two floating translocations—not sex-associated and affecting different chromosomes—have been observed in both male and female plants in some populations. These produce meiotic configurations previously unrecorded in Viscum . This floating heterozygosity seems to be correlated with the aptitude of V. cruciatum to develop on different hosts, especially Prunus . All studied populations showed an excess of female plants, perhaps partly due to facultative agamospermy.

Cytogenetic and isozyme studies of wild and cultivated Capsicum annuum

The esterase isozymes of 15 wild and cultivated accessions of Capsicum annuum from different geographic areas throughout the United States, Mexico, Central America, and South America showed three patterns. All accessions from central Mexico, including the cultivated type, and some from the United States, had pattern A. Other accessions from the United States, those from Central America, and those from Peru had pattern B; those from Colombia had pattern C. Pattern C had more bands, apparently identical with those in the hybrids between A and B. F1 plants between the Colombian accession used in a hybridization test and accessions with patterns A and B showed associations of four or six chromosomes at metaphase I of meiosis. The hypothesis is discussed that pattern C resulted from a process of gene duplication. The alternative explanation of permanent translocation heterozygosity is excluded because in the Colombian accessions no multivalents were observed at meiosis.Key words: Capsicum, geographic distributions, duplication, translocation, isozymes.

Experimental Hybridization and Chromosomal Diversity within Gaura sect. Gaura (Onagraceae)

The proposed phylogeny of Gaura section Gaura is supported by experimental hy- bridization studies. The generally high average capsule-set of crosses between species of section Gaura (78%), compared with capsule-set averages for intersectional crosses (32%), agrees with a pattern of morphological similarity and geographical congruence in confirming the close relation- ships among these species. Higher average crossing success for G. longiflora and its derivatives, G. biennis and G. demareei, suggests the central importance of G. longiflora within the section. Measures of chromosomal diversity demonstrate the apparent conservation of G. longiflora chromosome end arrangements within both G. angustifolia and G. neomexicana, as well as supporting the hypothesis of a hybrid origin for G. demareei (G. lindheimeri x G. longiflora). Apparent levels of translocation diversity in natural populations depend upon the breeding system. Selfing tends to distribute structurally diverse arrangements among homozygous individuals. The extreme chromosomal di- versity of G. biennis sets it apart as a unique genetic system, as does its permanent translocation heterozygosity. Segregation distortion for chromosomal complexes from a ring of four chromo- somes is present in one individual of G. neomexicana. Speciation in section Gaura has not depended upon post-mating, reproductive isolating mechanisms. Factors that contribute to the maintenance of each species as a distinct natural entity are: geographical isolation due to ecological specialization and/or range expansion (G. angustifolia, G. biennis, G. lindheimeri); self-compatibility (G. angustifolia, G. biennis, G. neomexicana); displacement of seasonal (G. angustifolia, G. lindheimeri) and daily (G. demareei, G. lindheimeri) flowering times; and permanent translocation heterozygosity (G. biennis).