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1.  Do Flower Color and Floral Scent of Silene Species affect Host Preference of Hadena bicruris, a Seed-Eating Pollinator, under Field Conditions? 
PLoS ONE  2014;9(6):e98755.
Specialization in plant–insect interactions is an important driver of evolutionary divergence; yet, plant traits mediating such interactions are poorly understood. In this study, we investigated how flower color and floral scent are related to seed predation by a seed-eating pollinator. We used field-transplanted recombinant F2 hybrids between Silene latifolia and S. dioica that are the preferred and alternative hosts of the moth Hadena bicruris and crosses within these species for comparison. We scored seed predation and flower color and analyzed floral scent. Pinker S. dioica-like flowers and emission of α-pinene decreased the odds of seed predation while emission of benzyl acetate and 6-methyl-5-hepten-2-one increased the odds of seed predation. Emission of these compounds did not differ significantly between the two Silene species. Our results suggest that flower color plays an important role in the specific interaction of H. bicruris with its preferred host S. latifolia. The compounds α-pinene, benzyl acetate and 6-methyl-5-hepten-2-one could represent non-specific deterrents and attractants to ovipositing moths. Alternatively, emission of these compounds could be related to herbivory or pathogen attack and act as a signal for host quality. This would weaken the predictability of the plant's costs and benefits of the interaction and act to maintain an imperfect degree of specialization.
doi:10.1371/journal.pone.0098755
PMCID: PMC4048206  PMID: 24905986
2.  How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant 
Background
Sexual selection theory predicts that males are limited in their reproductive success by access to mates, whereas females are more limited by resources. In animal-pollinated plants, attraction of pollinators and successful pollination is crucial for reproductive success. In dioecious plant species, males should thus be selected to increase their attractiveness to pollinators by investing more than females in floral traits that enhance pollinator visitation. We tested the prediction of higher attractiveness of male flowers in the dioecious, moth-pollinated herb Silene latifolia, by investigating floral signals (floral display and fragrance) and conducting behavioral experiments with the pollinator-moth, Hadena bicruris.
Results
As found in previous studies, male plants produced more but smaller flowers. Male flowers, however, emitted significantly larger amounts of scent than female flowers, especially of the pollinator-attracting compounds. In behavioral tests we showed that naïve pollinator-moths preferred male over female flowers, but this preference was only significant for male moths.
Conclusion
Our data suggest the evolution of dimorphic floral signals is shaped by sexual selection and pollinator preferences, causing sexual conflict in both plants and pollinators.
doi:10.1186/1471-2148-9-190
PMCID: PMC2738674  PMID: 19660122
3.  A White Campion (Silene latifolia) floral expressed sequence tag (EST) library: annotation, EST-SSR characterization, transferability, and utility for comparative mapping 
BMC Genomics  2009;10:243.
Background
Expressed sequence tag (EST) databases represent a valuable resource for the identification of genes in organisms with uncharacterized genomes and for development of molecular markers. One class of markers derived from EST sequences are simple sequence repeat (SSR) markers, also known as EST-SSRs. These are useful in plant genetic and evolutionary studies because they are located in transcribed genes and a putative function can often be inferred from homology searches. Another important feature of EST-SSR markers is their expected high level of transferability to related species that makes them very promising for comparative mapping. In the present study we constructed a normalized EST library from floral tissue of Silene latifolia with the aim to identify expressed genes and to develop polymorphic molecular markers.
Results
We obtained a total of 3662 high quality sequences from a normalized Silene cDNA library. These represent 3105 unigenes, with 73% of unigenes matching genes in other species. We found 255 sequences containing one or more SSR motifs. More than 60% of these SSRs were trinucleotides. A total of 30 microsatellite loci were identified from 106 ESTs having sufficient flanking sequences for primer design. The inheritance of these loci was tested via segregation analyses and their usefulness for linkage mapping was assessed in an interspecific cross. Tests for crossamplification of the EST-SSR loci in other Silene species established their applicability to related species.
Conclusion
The newly characterized genes and gene-derived markers from our Silene EST library represent a valuable genetic resource for future studies on Silene latifolia and related species. The polymorphism and transferability of EST-SSR markers facilitate comparative linkage mapping and analyses of genetic diversity in the genus Silene.
doi:10.1186/1471-2164-10-243
PMCID: PMC2689282  PMID: 19467153
4.  Asymmetrical conspecific seed-siring advantage between Silene latifolia and S. dioica 
Annals of Botany  2010;105(4):595-605.
Background and Aims
Silene dioica and S. latifolia experience only limited introgression despite overlapping flowering phenologies, geographical distributions, and some pollinator sharing. Conspecific pollen precedence and other reproductive barriers operating between pollination and seed germination may limit hybridization. This study investigates whether barriers at this stage contribute to reproductive isolation between these species and, if so, which mechanisms are responsible.
Methods
Pollen-tube lengths for pollen of both species in styles of both species were compared. Additionally, both species were pollinated with majority S. latifolia and majority S. dioica pollen mixes; then seed set, seed germination rates and hybridity of the resulting seedlings were determined using species-specific molecular markers.
Key Results
The longest pollen tubes were significantly longer for conspecific than heterospecific pollen in both species, indicating conspecific pollen precedence. Seed set but not seed germination was lower for flowers pollinated with pure heterospecific versus pure conspecific pollen. Mixed-species pollinations resulted in disproportionately high representation of nonhybrid offspring for pollinations of S. latifolia but not S. dioica flowers.
Conclusions
The finding of conspecific pollen precedence for pollen-tube growth but not seed siring in S. dioica flowers may be explained by variation in pollen-tube growth rates, either at different locations in the style or between leading and trailing pollen tubes. Additionally, this study finds a barrier to hybridization operating between pollination and seed germination against S. dioica but not S. latifolia pollen. The results are consistent with the underlying cause of this barrier being attrition of S. dioica pollen tubes or reduced success of heterospecifically fertilized ovules, rather than time-variant mechanisms. Post-pollination, pre-germination barriers to hybridization thus play a partial role in limiting introgression between these species.
doi:10.1093/aob/mcq013
PMCID: PMC2850797  PMID: 20147372
Conspecific pollen precedence; hybridization; pollen tubes; reproductive isolation; Silene dioica; Silene latifolia
5.  Identification of Internal Reference Genes for Gene Expression Normalization between the Two Sexes in Dioecious White Campion 
PLoS ONE  2014;9(3):e92893.
Quantitative real time (qRT)-PCR is a precise and efficient method for studying gene expression changes between two states of interest, and is frequently used for validating interesting gene expression patterns in candidate genes initially identified in genome-wide expression analyses, such as RNA-seq experiments. For an adequate normalisation of qRT-PCR data, it is essential to have reference genes available whose expression intensities are constant among the different states of interest. In this study we present and validate a catalogue of traditional and newly identified reference genes that were selected from RNA-seq data from multiple individuals from the dioecious plant Silene latifolia with the aim of studying gene expression differences between the two sexes in both reproductive and vegetative tissues. The catalogue contains more than 15 reference genes with both stable expression intensities and a range of expression intensities in flower buds and leaf tissues. These reference genes were used to normalize expression differences between reproductive and vegetative tissues in eight candidate genes with sex-biased expression. Our results suggest a trend towards a reduced sex-bias in sex-linked gene expression in vegetative tissues. In this study, we report on the systematic identification and validation of internal reference genes for adequate normalization of qRT-PCR-based analyses of gene expression differences between the two sexes in S. latifolia. We also show how RNA-seq data can be used efficiently to identify suitable reference genes in a wide diversity of species.
doi:10.1371/journal.pone.0092893
PMCID: PMC3968030  PMID: 24675788
6.  Sex Determination in Plants 
Plant Signaling & Behavior  2007;2(3):178-179.
Most dioecious plant species are believed to derive from hermaphrodite ancestors. The regulatory pathways that have been modified during evolution of the hermaphrodite ancestors and led to the emergence of dioecious species (with separate sexes) still remain unknown. Silene latifolia is a dioecious plant species harbouring XY sex chromosomes. To identify the molecular mechanisms involved in female organ suppression in male flowers of S. latifolia, we looked for genes potentially involved in the establishment of floral organ and whorl boundaries. We identified Arabidopsis thaliana homologs of SHOOTMERISTEMLESS (STM) and CUP SHAPED COTYLEDON 1 (CUC1) and CUC2 genes in S. latifolia. Our phylogenetic analyses suggest that we identified true orthologs for both types of genes. Detailed expression analyses showed a conserved expression pattern for these genes between S. latifolia and A. thaliana, suggesting a conserved function of the corresponding proteins. Both orthologs showed clear differences in their expression pattern between males and females or hermaphrodites suggesting their possible involvement in the sex determination pathway in S. latifolia.
PMCID: PMC2634050  PMID: 19704689
floral meristem; sex determination; shoot-meristemless; cup shaped cotyledon
7.  Demethylation of Veratrole by Cytochrome P-450 in Streptomyces setonii 
The actinomycete Streptomyces setonii 75Vi2 demethylates vanillic acid and guaiacol to protocatechuic acid and catechol, respectively, and then metabolizes the products by the β-ketoadipate pathway. UV spectroscopy showed that this strain could also metabolize veratrole (1,2-dimethoxybenzene). When grown in veratrole-containing media supplemented with 2,2′-dipyridyl to inhibit cleavage of the aromatic ring, S. setonii accumulated catechol, which was detected by both liquid chromatography and gas chromatography. Reduced cell extracts from veratrole-grown cultures, but not sodium succinate-grown cultures, produced a carbon monoxide difference spectrum with a peak at 450 nm that indicated the presence of soluble cytochrome P-450. Addition of veratrole or guaiacol to oxidized cell extracts from veratrole-grown cultures produced difference spectra that indicated that these compounds were substrates for cytochrome P-450. My results suggest that S. setonii produces a cytochrome P-450 that is involved in the demethylation of veratrole and guaiacol to catechol, which is then catabolized by the β-ketoadipate pathway.
PMCID: PMC203400  PMID: 16347120
8.  Identifying new sex-linked genes through BAC sequencing in the dioecious plant Silene latifolia 
BMC Genomics  2015;16(1):546.
Background
Silene latifolia represents one of the best-studied plant sex chromosome systems. A new approach using RNA-seq data has recently identified hundreds of new sex-linked genes in this species. However, this approach is expected to miss genes that are either not expressed or are expressed at low levels in the tissue(s) used for RNA-seq. Therefore other independent approaches are needed to discover such sex-linked genes.
Results
Here we used 10 well-characterized S. latifolia sex-linked genes and their homologs in Silene vulgaris, a species without sex chromosomes, to screen BAC libraries of both species. We isolated and sequenced 4 Mb of BAC clones of S. latifolia X and Y and S. vulgaris genomic regions, which yielded 59 new sex-linked genes (with S. vulgaris homologs for some of them). We assembled sequences that we believe represent the tip of the Xq arm. These sequences are clearly not pseudoautosomal, so we infer that the S. latifolia X has a single pseudoautosomal region (PAR) on the Xp arm. The estimated mean gene density in X BACs is 2.2 times lower than that in S. vulgaris BACs, agreeing with the genome size difference between these species. Gene density was estimated to be extremely low in the Y BAC clones. We compared our BAC-located genes with the sex-linked genes identified in previous RNA-seq studies, and found that about half of them (those with low expression in flower buds) were not identified as sex-linked in previous RNA-seq studies. We compiled a set of ~70 validated X/Y genes and X-hemizygous genes (without Y copies) from the literature, and used these genes to show that X-hemizygous genes have a higher probability of being undetected by the RNA-seq approach, compared with X/Y genes; we used this to estimate that about 30 % of our BAC-located genes must be X-hemizygous. The estimate is similar when we use BAC-located genes that have S. vulgaris homologs, which excludes genes that were gained by the X chromosome.
Conclusions
Our BAC sequencing identified 59 new sex-linked genes, and our analysis of these BAC-located genes, in combination with RNA-seq data suggests that gene losses from the S. latifolia Y chromosome could be as high as 30 %, higher than previous estimates of 10-20 %.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1698-7) contains supplementary material, which is available to authorized users.
doi:10.1186/s12864-015-1698-7
PMCID: PMC4520012  PMID: 26223308
Sex chromosomes; Sex-linked genes; Plant; BAC; RNA-seq; Gene loss; Y degeneration; Silene latifolia; Silene vulgaris
9.  Molecular characterisation of four double-flowered mutants of Silene dioica representing four centuries of variation 
Journal of Experimental Botany  2015;66(11):3297-3307.
Highlight
Four double-flowered mutants of dioecious Silene dioica have been characterized; we recount their 400 year history, trace their ancestral genetic relationships, describe their phenotypes, and characterize mutant MADS-box gene alleles.
Records of double-flowered Silene dioica date from the late sixteenth century and four named varieties are grown today, as previously, for their horticultural interest. Although double-flowered mutants have been characterized in several plants, their study in dioecious species is of particular interest due to influences of the homeotic mutation on the different floral whorl configurations in males and females. We have analysed four double-flowered varieties of Silene dioica: Flore Pleno and Rosea Plena date back to the seventeenth and nineteenth centuries, Thelma Kay and Firefly were recognized in the latter part of the twentieth and early twenty-first centuries. We have analysed the floral structure of the four varieties, which have distinct floral architectures. Based on Y chromosome-specific PCR analysis we show that Firefly is male and that the other three varieties are female: Random Amplification of Polymorphic DNA (RAPD) analyses suggested a common origin for the three female varieties. The double-flowered phenotype in all four varieties is caused by mutation of the C-function MADS-box transcription factor gene SDM1. We show that Firefly carries a unique 44bp insertion into SDM1, revealing an independent origin for this variety. Comparative analysis of SDM1 cDNA and genomic sequences in Flore Pleno, Rosea Plena and Thelma Kay shows that all three are caused by the same 7bp insertion within SDM1 and therefore share a common origin. The three alleles also differ by several single nucleotide polymorphisms, which represent somatic mutations accumulated over four centuries of asexual propagation.
doi:10.1093/jxb/erv139
PMCID: PMC4449544  PMID: 25878355
C-function MADS-box; dioecy; double-flowered; floral homeotic mutation; sex determination; Silene dioica.
10.  Floral dimorphism in plant populations with combined versus separate sexes 
Annals of Botany  2011;108(4):765-776.
Background and Aims
Dimorphism among floral traits can evolve through variation in selection intensity between female and male performance, especially when sex functions are separated between flowers on a plant (monoecy), or between individuals (dioecy). In animal-pollinated species, male floral traits are predicted to be larger because competition for pollinators should favour larger displays. Floral dimorphism may be greater in dioecious than monoecious populations because of trade-offs between female and male function and opportunities for selfing in hermaphrodites.
Methods
These predictions were tested by surveying flower size, total flowers per inflorescence and daily display size in the insect-pollinated Sagittaria latifolia (Alismataceae). This species is useful for comparative analysis because populations are mostly either monoecious or dioecious. We examined floral dimorphism in 13 monoecious and 16 dioecious populations in eastern North America.
Key Results
Male flowers were significantly larger than female flowers in monoecious and dioecious populations, but there was no evidence for greater flower size dimorphism in dioecious populations despite their larger flower sizes overall. Although inflorescences in both dioecious and monoecious populations produced more male flowers, daily floral displays were significantly larger for female than male function due to more synchronous female flower opening. Daily floral display dimorphism was significantly greater in dioecious populations, due to greater female daily floral displays. There was a positive relationship between mean flower size and total flowers per inflorescence for both sexes in dioecious populations, but no relationship for either sex function in monoecious populations. Flower size dimorphism was positively correlated with the frequencies of females in dioecious populations.
Conclusions
The increased size and number of male flowers and protracted male floral displays in S. latifolia are probably shaped by sexual selection for more effective pollen dispersal.
doi:10.1093/aob/mcr025
PMCID: PMC3170149  PMID: 21385777
Sexual dimorphism; flower size; daily floral display; sexual selection; sex ratios; monoecy; dioecy; Sagittaria latifolia
11.  Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus 
BMC Genomics  2015;16(1):461.
Background
The genus Microbotryum includes plant pathogenic fungi afflicting a wide variety of hosts with anther smut disease. Microbotryum lychnidis-dioicae infects Silene latifolia and replaces host pollen with fungal spores, exhibiting biotrophy and necrosis associated with altering plant development.
Results
We determined the haploid genome sequence for M. lychnidis-dioicae and analyzed whole transcriptome data from plant infections and other stages of the fungal lifecycle, revealing the inventory and expression level of genes that facilitate pathogenic growth. Compared to related fungi, an expanded number of major facilitator superfamily transporters and secretory lipases were detected; lipase gene expression was found to be altered by exposure to lipid compounds, which signaled a switch to dikaryotic, pathogenic growth. In addition, while enzymes to digest cellulose, xylan, xyloglucan, and highly substituted forms of pectin were absent, along with depletion of peroxidases and superoxide dismutases that protect the fungus from oxidative stress, the repertoire of glycosyltransferases and of enzymes that could manipulate host development has expanded. A total of 14 % of the genome was categorized as repetitive sequences. Transposable elements have accumulated in mating-type chromosomal regions and were also associated across the genome with gene clusters of small secreted proteins, which may mediate host interactions.
Conclusions
The unique absence of enzyme classes for plant cell wall degradation and maintenance of enzymes that break down components of pollen tubes and flowers provides a striking example of biotrophic host adaptation.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1660-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s12864-015-1660-8
PMCID: PMC4469406  PMID: 26076695
Microbotryum violaceum; Anther smuts; CAZymes; Transposable elements; Mating-type chromosomes; Pathogen alteration of host development
12.  Size Does Matter: Staging of Silene latifolia Floral Buds for Transcriptome Studies 
Dioecious plants in the Caryophyllaceae family are susceptible to infection by members of the anthericolous smut fungi. In our studies of the Silene latifolia/Microbotryum lychnidis-dioicae pathosystem, we were interested in characterizing the plant-pathogen interaction at the molecular level before and during teliosporogenesis. This takes place during floral bud development, and we hoped to capture the interaction by Illumina Next-Gen RNA-Sequencing. Using previous literature that documented the stages of the floral buds for S. latifolia, we examined the floral buds from plants grown and infected under growth chamber conditions, using the disserting microscope to determine the stage of floral buds based on the morphology. We compiled the information and determined the size of floral buds that correspond to the desired stages of development for tissue collection, for the purpose of RNA-sequencing. This offers a practical approach for researchers who require a large number of floral buds/tissue categorized by stages of development, ascertaining whether infected/uninfected buds are at comparable stages of development and whether this also holds true for male vs. female buds. We also document our experience in infecting the plants and some of the unusual morphologies we observed after infection.
doi:10.3390/ijms160922027
PMCID: PMC4613295  PMID: 26378529
Silene latifolia; Microbotryum; anther smut; RNA-Seq; floral bud stage; host-pathogen interactions
13.  A new plant sex-linked gene with high sequence diversity and possible introgression of the X copy 
Heredity  2010;106(2):339-347.
We describe patterns of DNA sequence diversity in a newly identified sex linked gene, SlX9/SlY9, in Silene latifolia (Caryophyllaceae). The copies on both sex chromosomes appear to be functional, and each maps close to the respective X- and Y-linked copy of another sex-linked gene pair, SlCypX/SlCypY. The Y-linked copy has low diversity, similar to what has been found for several other Y-linked genes in S. latifolia, and consistent with the theoretical expectations of hitch-hiking processes occurring on a non-recombining chromosome. However, SlX9 has higher diversity than other genes on the S. latifolia X chromosome. We evaluate the hypothesis of introgression from the closely related species S. dioica as an explanation for the high sequence diversity observed.
doi:10.1038/hdy.2010.76
PMCID: PMC3044453  PMID: 20551975
Silene latifolia; sex chromosomes; introgression; SlX9
14.  A new plant sex-linked gene with high sequence diversity and possible introgression of the X copy 
Heredity  2010;106(2):339-347.
We describe patterns of DNA sequence diversity in a newly identified sex-linked gene, SlX9/SlY9, in Silene latifolia (Caryophyllaceae). The copies on both sex chromosomes seem to be functional, and each maps close to the respective X- and Y-linked copy of another sex-linked gene pair, SlCypX/SlCypY. The Y-linked copy has low diversity, similar to what has been found for several other Y-linked genes in S. latifolia, and consistent with the theoretical expectations of hitch-hiking processes occurring on a non-recombining chromosome. However, SlX9 has higher diversity than other genes on the S. latifolia X chromosome. We evaluate the hypothesis of introgression from the closely related species S. dioica as an explanation for the high sequence diversity observed.
doi:10.1038/hdy.2010.76
PMCID: PMC3044453  PMID: 20551975
Silene latifolia; sex chromosomes; introgression; SlX9
15.  On flavonoid accumulation in different plant parts: variation patterns among individuals and populations in the shore campion (Silene littorea) 
The presence of anthocyanins in flowers and fruits is frequently attributed to attracting pollinators and dispersers. In vegetative organs, anthocyanins and other non-pigmented flavonoids such as flavones and flavonols may serve protective functions against UV radiation, cold, heat, drought, salinity, pathogens, and herbivores; thus, these compounds are usually produced as a plastic response to such stressors. Although, the independent accumulation of anthocyanins in reproductive and vegetative tissues is commonly postulated due to differential regulation, the accumulation of flavonoids within and among populations has never been thoroughly compared. Here, we investigated the shore campion (Silene littorea, Caryophyllaceae) which exhibits variation in anthocyanin accumulation in its floral and vegetative tissues. We examined the in-situ accumulation of flavonoids in floral (petals and calyxes) and vegetative organs (leaves) from 18 populations representing the species' geographic distribution. Each organ exhibited considerable variability in the content of anthocyanins and other flavonoids both within and among populations. In all organs, anthocyanin and other flavonoids were correlated. At the plant level, the flavonoid content in petals, calyxes, and leaves was not correlated in most of the populations. However, at the population level, the mean amount of anthocyanins in all organs was positively correlated, which suggests that the variable environmental conditions of populations may play a role in anthocyanin accumulation. These results are unexpected because the anthocyanins are usually constitutive in petals, yet contingent to environmental conditions in calyxes and leaves. Anthocyanin variation in petals may influence pollinator attraction and subsequent plant reproduction, yet the amount of anthocyanins may be a direct response to environmental factors. In populations on the west coast, a general pattern of increasing accumulation of flavonoids toward southern latitudes was observed in calyxes and leaves. This pattern corresponds to a gradual increase of UV-B radiation and temperature, and a decrease of rainfall toward the south. However, populations along the southern coast exposed to similar climatic stressors showed highly variable flavonoid contents, implying that other factors may play a role in flavonoid accumulation.
doi:10.3389/fpls.2015.00939
PMCID: PMC4625047  PMID: 26579180
anthocyanins; Caryophyllaceae; coastal dune ecosystem; flavones; flavonols; flower color; plasticity; intra- and inter-population variation
16.  Narrowing Down the Mapping of Plant Sex-Determination Regions Using New Y-Chromosome-Specific Markers and Heavy-Ion Beam Irradiation-Induced Y-Deletion Mutants in Silene latifolia 
G3: Genes|Genomes|Genetics  2012;2(2):271-278.
Silene latifolia is a well-studied model system for plant XY sex determination. Three maleness factors are thought to function on the Y chromosome, gynoecium suppression factor (GSF), stamen-promoting factor (SPF), and male fertility factor (MFF), and their deletions result in hermaphrodites, anther defects, and pollen defects, respectively. Although a framework map of the Y chromosome exists, the sex determination genes have not been identified, and no markers close enough to potentially be used for BAC library screening are yet available. The analysis of Y deletion mutants by Y-chromosome-specific STS markers is an efficient way to isolate sex determination regions, but more Y-specific STS markers are needed to accelerate the exploration of sex determination factors. Herein, we report a marker design method that uses simple sequence repeats, which is especially effective on the Y chromosome of S. latifolia because it contains many simple sequence repeats. Six new Y-chromosome-specific STS markers were obtained, SmicSy1–6. These were used to detect relatively small Y deletion sites in heavy-ion beam irradiation-induced mutants. The mapping of male sex determination regions was narrowed down by using more markers and smaller-sized Y deletion mutants. One new marker, SmicSy6, is a proximal marker to SPF and, thus, a second index for SPF. The region including SPF is thought to be located between two SPF proximal markers. The flower phenotype correlates with the deletion size of SPF using SPF proximal markers. These findings represent new progress in isolating the sex determination factor, which has been studied for more than 50 years.
doi:10.1534/g3.111.001420
PMCID: PMC3284334  PMID: 22384405
Silene latifolia; XY; sex chromosomes; STS marker; simple sequence repeat
17.  Comparative analysis of a plant pseudoautosomal region (PAR) in Silene latifolia with the corresponding S. vulgaris autosome 
BMC Genomics  2012;13:226.
Background
The sex chromosomes of Silene latifolia are heteromorphic as in mammals, with females being homogametic (XX) and males heterogametic (XY). While recombination occurs along the entire X chromosome in females, recombination between the X and Y chromosomes in males is restricted to the pseudoautosomal region (PAR). In the few mammals so far studied, PARs are often characterized by elevated recombination and mutation rates and high GC content compared with the rest of the genome. However, PARs have not been studied in plants until now. In this paper we report the construction of a BAC library for S. latifolia and the first analysis of a > 100 kb fragment of a S. latifolia PAR that we compare to the homologous autosomal region in the closely related gynodioecious species S. vulgaris.
Results
Six new sex-linked genes were identified in the S. latifolia PAR, together with numerous transposable elements. The same genes were found on the S. vulgaris autosomal segment, with no enlargement of the predicted coding sequences in S. latifolia. Intergenic regions were on average 1.6 times longer in S. latifolia than in S. vulgaris, mainly as a consequence of the insertion of transposable elements. The GC content did not differ significantly between the PAR region in S. latifolia and the corresponding autosomal region in S. vulgaris.
Conclusions
Our results demonstrate the usefulness of the BAC library developed here for the analysis of plant sex chromosomes and indicate that the PAR in the evolutionarily young S. latifolia sex chromosomes has diverged from the corresponding autosomal region in the gynodioecious S. vulgaris mainly with respect to the insertion of transposable elements. Gene order between the PAR and autosomal region investigated is conserved, and the PAR does not have the high GC content observed in evolutionarily much older mammalian sex chromosomes.
doi:10.1186/1471-2164-13-226
PMCID: PMC3431222  PMID: 22681719
BAC library; Pseudoautosomal region; PAR; Silene latifolia; Sex chromosome; Evolution
18.  Variation in highbush blueberry floral volatile profiles as a function of pollination status, cultivar, time of day and flower part: implications for flower visitation by bees 
Annals of Botany  2011;107(8):1377-1390.
Background and Aims
Studies of the effects of pollination on floral scent and bee visitation remain rare, particularly in agricultural crops. To fill this gap, the hypothesis that bee visitation to flowers decreases after pollination through reduced floral volatile emissions in highbush blueberries, Vaccinium corymbosum, was tested. Other sources of variation in floral emissions and the role of floral volatiles in bee attraction were also examined.
Methods
Pollinator visitation to blueberry flowers was manipulated by bagging all flowers within a bush (pollinator excluded) or leaving them unbagged (open pollinated), and then the effect on floral volatile emissions and future bee visitation were measured. Floral volatiles were also measured from different blueberry cultivars, times of the day and flower parts, and a study was conducted to test the attraction of bees to floral volatiles.
Key Results
Open-pollinated blueberry flowers had 32 % lower volatile emissions than pollinator-excluded flowers. In particular, cinnamyl alcohol, a major component of the floral blend that is emitted exclusively from petals, was emitted in lower quantities from open-pollinated flowers. Although, no differences in cinnamyl alcohol emissions were detected among three blueberry cultivars or at different times of day, some components of the blueberry floral blend were emitted in higher amounts from certain cultivars and at mid-day. Field observations showed that more bees visited bushes with pollinator-excluded flowers. Also, more honey bees were caught in traps baited with a synthetic blueberry floral blend than in unbaited traps.
Conclusions
Greater volatile emissions may help guide bees to unpollinated flowers, and thus increase plant fitness and bee energetic return when foraging in blueberries. Furthermore, the variation in volatile emissions from blueberry flowers depending on pollination status, plant cultivar and time of day suggests an adaptive role of floral signals in increasing pollination of flowers.
doi:10.1093/aob/mcr077
PMCID: PMC3101143  PMID: 21498566
Vaccinium corymbosum; honey bees; bumble bees; volatile organic compounds; diurnal rhythm; nectar production; site of emission
19.  Flower development, pollen fertility and sex expression analyses of three sexual phenotypes of Coccinia grandis 
BMC Plant Biology  2014;14:325.
Background
Coccinia grandis is a dioecious species of Cucurbitaceae having heteromorphic sex chromosomes. The chromosome constitution of male and female plants is 22 + XY and 22 + XX respectively. Y chromosome of male sex is conspicuously large and plays a decisive role in determining maleness. Sex modification has been studied in hypogynous Silene latifolia (Caryophyllaceae) but there is no such report in epigynous Coccinia grandis. Moreover, the role of organ identity genes during sex expression in Coccinia has not been evaluated earlier. Investigations on sexual phenotypes of C. grandis including a rare gynomonoecious (GyM) form and AgNO3 mediated sex modification have added a new dimension to the understanding of sex expression in dioecious flowering plants.
Results
Morphometric analysis showed the presence of staminodes in pistillate flowers and histological study revealed the absence of carpel initials in male flowers. Though GyM plant had XX sex chromosomes, the development of stamens occurred in hermaphrodite flowers but the pollens were not fertile. Silver nitrate (AgNO3) application enhanced stamen growth in wild type female flowers like that of GyM plant but here also the pollens were sterile. Differential expression of CgPI could be involved in the development of different floral phenotypes.
Conclusions
The three principle factors, Gynoecium Suppression (SuF), Stamen Promoting Factor (SPF) and Male Fertility (mF) that control sex expression in dioecious C. grandis assumed to be located on Y chromosome, play a decisive role in determining maleness. However, the characteristic development of stamens in hermaphrodite flowers of GyM plant having XX sex chromosomes indicates that Y-linked SPF regulatory pathway is somehow bypassed. Our experimental findings together with all other previous chromosomal and molecular cytogenetical data strongly support the view that C. grandis could be used as a potential model system to study sex expression in dioecious flowering plant.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0325-0) contains supplementary material, which is available to authorized users.
doi:10.1186/s12870-014-0325-0
PMCID: PMC4255441  PMID: 25430000
Coccinia grandis; Hypogynous; Epigynous; Dioecious; Gynomonoecy; Heteromorphic sex chromosomes; Sex modification; Organ identity genes; Silver nitrate
20.  Dioecious Silene latifolia plants show sexual dimorphism in the vegetative stage 
BMC Plant Biology  2010;10:208.
Background
Prior to this study, no differences in gene expression between male and female dioecious plants in the vegetative state had been detected. Among dioecious plants displaying sexual dimorphism, Silene latifolia is one of the most studied species. Although many sexually dimorphic traits have been described in S. latifolia, all of them are quantitative, and they usually become apparent only after the initiation of flowering.
Results
We present RT-PCR-based evidence that in S. latifolia, sexual dimorphism in gene expression is present long before the initiation of flowering. We describe three ESTs that show sex-specific (two male specific and one female specific) transcription at the rosette stage before the first flowering season.
Conclusions
To our knowledge, this study provides the first molecular evidence of early pre-flowering sexual dimorphism in angiosperms.
doi:10.1186/1471-2229-10-208
PMCID: PMC2956557  PMID: 20854681
21.  How scent and nectar influence floral antagonists and mutualists 
eLife  null;4:e07641.
Many plants attract and reward pollinators with floral scents and nectar, respectively, but these traits can also incur fitness costs as they also attract herbivores. This dilemma, common to most flowering plants, could be solved by not producing nectar and/or scent, thereby cheating pollinators. Both nectar and scent are highly variable in native populations of coyote tobacco, Nicotiana attenuata, with some producing no nectar at all, uncorrelated with the tobacco's main floral attractant, benzylacetone. By silencing benzylacetone biosynthesis and nectar production in all combinations by RNAi, we experimentally uncouple these floral rewards/attractrants and measure their costs/benefits in the plant's native habitat and experimental tents. Both scent and nectar increase outcrossing rates for three, separately tested, pollinators and both traits increase oviposition by a hawkmoth herbivore, with nectar being more influential than scent. These results underscore that it makes little sense to study floral traits as if they only mediated pollination services.
DOI: http://dx.doi.org/10.7554/eLife.07641.001
eLife digest
Flowering plants have evolved a number of different approaches to reproduction. Some use their own pollen and self-fertilize, while others use pollen from other nearby plants. This fertilization by other plants is called ‘outcrossing’ and introduces new genetic variation into each generation, which is extremely important for the evolutionary process.
Some flowering plants rely on animals to help with pollination, attracting visitors with floral scents and rewarding the visitors with sugar-rich nectar. But scent and nectar also attract herbivores that damage the plants. This causes a dilemma for flowering plants, which has led some to evolve to not produce scent or to offer no nectar while masquerading as a plant that does. Previous studies into the costs and benefits of such strategies have looked at the effects of either floral scent or nectar, but no-one has uncoupled the effects of these two traits on both pollination and herbivore attack.
Kessler et al. have addressed this issue in wild tobacco plants, which can both self-fertilize and outcross, and which produce varying amounts of scent and nectar. The experiments were conducted under mesh tents and in field trials in the plant's natural habitat: the Great Basin Desert in Utah. Kessler et al. used a gene-silencing technique called ‘RNA interference’ to inhibit the production of scent or nectar, either separately or together. When grown in field trials, under conditions that prevent self-fertilization, these tobacco plants are frequently visited by a hummingbird and three species of hawkmoth. All four of these animals pollinate the tobacco plants, but one of the moths also lays eggs that hatch into caterpillars, which damage the plant. Kessler et al. monitored the effects that the loss of scent, nectar or both had on visits by each pollinator and on outcrossing.
These experiments revealed that scent is essential to attract one hawkmoth species but not for another (called Hyles lineata). Furthermore, while, the hummingbird needs nectar, the H. lineata moth does not; but this moth won't visit flowers that lack both scent and nectar. The experiments also show that, for the moth that lays its eggs on the tobacco plants, both scent and nectar increase pollination and egg laying, but nectar has a stronger effect. Thus reducing nectar, as this tobacco plant does in the wild, is one strategy that can be used to reduce herbivore attack by caterpillars. Together, these findings highlight that it is important to study both herbivores and pollinators when attempting to understand the evolution of floral traits.
DOI: http://dx.doi.org/10.7554/eLife.07641.002
doi:10.7554/eLife.07641
PMCID: PMC4530224  PMID: 26132861
Nicotiana attenuata; Manduca sexta; Hyles lineata; Archilochus alexandri; Manduca quinquemaculata; pollination; other
22.  Marcescent corollas as functional structures: effects on the fecundity of two insect-pollinated plants 
Annals of Botany  2010;106(4):659-662.
Background and aims
Persistence of withered corollas after anthesis (‘corolla marcescence’) is widespread in angiosperms, yet its functional significance does not seem to have been explored for any species. This note reports the results of experiments assessing the fecundity effects of marcescent corollas in two southern Spanish insect-pollinated plants, Lavandula latifolia (Lamiaceae) and Viola cazorlensis (Violaceae).
Methods
The effect of marcescent corollas on seed production was evaluated experimentally on wild-growing plants. Newly open flowers were randomly assigned to either control or treatment groups in experimental plants. After anthesis, withered corollas of treatment flowers were removed and those in control flowers were left in place. Fruits produced by treatment and control flowers were collected shortly before dehiscence and the number of seeds counted.
Key Results
In V. cazorlensis, removal of withered corollas had no effect on percentage of fruit set, but mean seeds per fruit increased from 9·5 to 11·4. In L. latifolia, corolla removal had no effect on the number of seeds per fruit, but reduced the proportion of flowers ripening fruit from 60 % to 40 %. The detrimental effect of corolla removal on L. latifolia fecundity resulted from the drastic increase in fruit infestation by seed-predatory cecidomyiid larvae, which occurred in 4 % and 34 % of control and treatment fruits, respectively.
Conclusions
Because of their potential effects on plant fecundity, marcescent corollas should not be dismissed a priori as biologically irrelevant leftovers from past floral functions. The simplicity of the experimental layout required to test for short-term fecundity effects of corolla marcescence should help to achieve a better understanding of the ecological and evolutionary correlates of this widespread but poorly understood trait.
doi:10.1093/aob/mcq160
PMCID: PMC2944983  PMID: 20870656
Corolla marcescence; fecundity; Lavandula latifolia (Lamiaceae); seed predation; Viola cazorlensis (Violaceae)
23.  Rapid De Novo Evolution of X Chromosome Dosage Compensation in Silene latifolia, a Plant with Young Sex Chromosomes 
PLoS Biology  2012;10(4):e1001308.
Evidence for dosage compensation in Silene latifolia, a plant with 10-million-year-old sex chromosomes, reveals that dosage compensation can evolve rapidly in young XY systems and is not an animal-specific phenomenon.
Silene latifolia is a dioecious plant with heteromorphic sex chromosomes that have originated only ∼10 million years ago and is a promising model organism to study sex chromosome evolution in plants. Previous work suggests that S. latifolia XY chromosomes have gradually stopped recombining and the Y chromosome is undergoing degeneration as in animal sex chromosomes. However, this work has been limited by the paucity of sex-linked genes available. Here, we used 35 Gb of RNA-seq data from multiple males (XY) and females (XX) of an S. latifolia inbred line to detect sex-linked SNPs and identified more than 1,700 sex-linked contigs (with X-linked and Y-linked alleles). Analyses using known sex-linked and autosomal genes, together with simulations indicate that these newly identified sex-linked contigs are reliable. Using read numbers, we then estimated expression levels of X-linked and Y-linked alleles in males and found an overall trend of reduced expression of Y-linked alleles, consistent with a widespread ongoing degeneration of the S. latifolia Y chromosome. By comparing expression intensities of X-linked alleles in males and females, we found that X-linked allele expression increases as Y-linked allele expression decreases in males, which makes expression of sex-linked contigs similar in both sexes. This phenomenon is known as dosage compensation and has so far only been observed in evolutionary old animal sex chromosome systems. Our results suggest that dosage compensation has evolved in plants and that it can quickly evolve de novo after the origin of sex chromosomes.
Author Summary
The mammalian sex chromosomes originated from an ancestral pair of autosomes about 150 million years ago and the Y chromosome subsequently degenerated, losing most of its genes. During this process, a phenomenon called dosage compensation evolved to compensate for the gene loss on the Y chromosome and to equalize expression of X-linked genes in the two sexes. In humans, this is achieved by inactivating one of the two X chromosomes in females. Dosage compensation has also been reported in other animal XY systems such as fruit flies and worms, each 100 million years old or more. Here we studied dosage compensation in plants. We used high-throughput RNA sequencing in male and female Silene latifolia (white campion)—a dioecious plant whose XY chromosomes originated only about 10 million years ago—to identify hundreds of sex-linked genes. Analysis of their expression patterns in males and females revealed equal doses of sex-linked transcripts in both sexes, regardless of the degree of reduction of Y expression due to degeneration. Our results thus show that dosage compensation occurs in plants and is thus not an animal-specific phenomenon. They also reveal that proportionate dosage compensation can evolve rapidly de novo after the origin of sex chromosomes.
doi:10.1371/journal.pbio.1001308
PMCID: PMC3328428  PMID: 22529744
24.  Effects of pollination timing on seed paternity and seed mass in Silene latifolia (Caryophyllaceae) 
Annals of Botany  2009;104(4):767-773.
Background and Aims
Competition among genetically different pollen donors within one recipient flower may play an important role in plant populations, increasing offspring genetic diversity and vigour. However, under field conditions stochastic pollen arrival times may result in disproportionate fertilization success of the first-arriving pollen, even to the detriment of the recipient plant's and offspring fitness. It is therefore critical to evaluate the relative importance of arrival times of pollen from different donors in determining siring success.
Methods
Hand pollinations and genetic markers were used to investigate experimentally the effect of pollination timing on seed paternity, seed mass and stigmatic wilting in the the dioecious plant Silene latifolia. In this species, high prevalence of multiply-sired fruits in natural populations suggests that competition among different donors may often take place (at fertilization or during seed development); however, the role of variation due to pollen arrival times is not known.
Key Results
First-arriving pollen sired significantly more seeds than later-arriving pollen. This advantage was expressed already before the first pollen tubes could reach the ovary. Simultaneously with pollen tube growth, the stigmatic papillae wilted visibly. Individual seeds were heavier in fruits where one donor sired most seeds than in fruits where both donors had more even paternity shares.
Conclusions
In field populations of S. latifolia, fruits are often multiply-sired. Because later-arriving pollen had decreased chances of fertilizing the ovules, this implies that open-pollinated flowers often benefit from pollen carry-over or pollinator visits within short time intervals, which may contribute to increase offspring genetic diversity and fitness.
doi:10.1093/aob/mcp154
PMCID: PMC2729624  PMID: 19567418
Reproduction; reproductive success; pollen; siring success; microsatellite DNA; paternity; pollen tube growth; seed mass; Silene alba; stigma wilting
25.  SlWUS1; An X-linked Gene Having No Homologous Y-Linked Copy in Silene latifolia 
G3: Genes|Genomes|Genetics  2012;2(10):1269-1278.
The dioecious plant Silene latifolia has heteromorphic sex chromosomes, and comparison of the positions of sex-linked genes indicates that at least three large inversions have occurred during the evolution of the Y chromosome. In this article, we describe the isolation of a new sex-linked gene from S. latifolia, which provides new information on the evolution of this plant’s young sex chromosomes. By using reverse-transcription polymerase chain reaction degenerate primers based on the Arabidopsis thaliana sequence of WUSCHEL, a flower-development gene, we found two copies in S. latifolia, which we named SlWUS1 and SlWUS2. Southern blot and genetic segregation analysis showed that SlWUS1 is located on the X chromosome and SlWUS2 is autosomal. No Y-linked copy of SlWUS1 was found by either Southern blot analysis under low-stringency conditions or polymerase chain reaction with degenerate primers, so we conclude that SlWUS1 probably has no Y-linked homolog. It is unknown whether the Y chromosome lost the SlWUS1 copy by degeneration of this individual gene or whether deletion of a larger genome region was involved. Several tests lead us to conclude that dosage compensation has not evolved for this sex-linked gene. We mapped the ortholog in the nondioecious relative S. vulgaris (SvWUS1), to compare the location in a species that has no history of having sex chromosomes. SvWUS1 maps to the same linkage group as other fully X-linked genes, indicating that it was not added to the X, but was lost from the Y. Its location differs in the maps from the two species, raising the possibility that the X chromosome, as well as the Y, may have been rearranged.
doi:10.1534/g3.112.003749
PMCID: PMC3464119  PMID: 23050237
dioecious plant; Silene latifolia; X-linkage; genetic degeneration; WUSCHEL

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