Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids.
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ABSTRACT:
SUBMITTER: Schluter PM
PROVIDER: S-EPMC3078338 | biostudies-literature | 2011 Apr
REPOSITORIES: biostudies-literature
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Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids.
Schlüter Philipp M PM Xu Shuqing S Gagliardini Valeria V Whittle Edward E Shanklin John J Grossniklaus Ueli U Schiestl Florian P FP
Proceedings of the National Academy of Sciences of the United States of America 20110321 14
The orchids Ophrys sphegodes and O. exaltata are reproductively isolated from each other by the attraction of two different, highly specific pollinator species. For pollinator attraction, flowers chemically mimic the pollinators' sex pheromones, the key components of which are alkenes with different double-bond positions. This study identifies genes likely involved in alkene biosynthesis, encoding stearoyl-acyl carrier protein (ACP) desaturase (SAD) homologs. The expression of two isoforms, SAD1 ...[more]
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Project description:Background and aimsThe events leading to speciation are best investigated in systems where speciation is ongoing or incomplete, such as incipient species. By examining reproductive barriers among incipient sister taxa and their congeners we can gain valuable insights into the relative timing and importance of the various barriers involved in the speciation process. The aim of this study was to identify the reproductive barriers among sexually deceptive orchid taxa in the genus Chiloglottis.MethodsThe study targeted four closely related taxa with varying degrees of geographic overlap. Chemical, morphological and genetic evidence was combined to explore the basis of reproductive isolation. Of primary interest was the degree of genetic differentiation among taxa at both nuclear and chloroplast DNA markers. To objectively test whether or not species boundaries are defined by the chemistry that controls pollinator specificity, genetic analysis was restricted to samples of known odour chemistry.Key resultsFloral odour chemical analysis was performed for 600+ flowers. The three sympatric taxa were defined by their specific chiloglottones, the semiochemicals responsible for pollinator attraction, and were found to be fully cross-compatible. Multivariate morphometric analysis could not reliably distinguish among the four taxa. Although varying from very low to moderate, significant levels of genetic differentiation were detected among all pairwise combinations of taxa at both nuclear and chloroplast loci. However, the levels of genetic differentiation were lower than expected for mature species. Critically, a lack of chloroplast DNA haplotype sharing among the morphologically indistinguishable and most closely related taxon pair confirmed that chemistry alone can define taxon boundaries.ConclusionsThe results confirmed that pollinator isolation, mediated by specific pollinator attraction, underpins strong reproductive isolation in these taxa. A combination of large effective population sizes, initial neutral mutations in the genes controlling floral scent, and a pool of available pollinators likely drives diversity in this system.
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Project description:BACKGROUND:Sexually deceptive orchids of the genus Ophrys attract their pollinators, male insects, on a highly specific basis through the emission of odour blends that mimic the female sex pheromone of the targeted species. In this study, we have investigated a contact site between Ophrys arachnitiformis and O. lupercalis, two sympatric orchid species that are usually reproductively isolated via the exploitation of different pollinator "niches", but occasionally hybridise despite their apparent combination of ethological and mechanical isolation barriers. In particular, we have investigated the extent to which these Ophrys hybrids generate "emergent" combinations (i.e. novel and unpredictable from the parents' phenotypes) of floral traits, and how these phenotypic novelties, particularly the odour blends emitted by the flower, could facilitate the invasion of a novel pollinator "niche" and induce the rapid formation of reproductive isolation, a prerequisite for adaptive evolutionary divergence. RESULTS:Our chemical analyses of floral scents show that the Ophrys F1 hybrids investigated here produce more compounds, significantly different ratios (% of odour compounds in the total blend), as well as new compounds in their floral odour compared to their progenitors. When tested for their attractiveness to the pollinator of each parent orchid species, we found that floral scent extracts of the hybrids triggered less inspecting flights and contacts by the male bees with the scented dummy than those of the parental orchid species. However, a series of additional behavioural bioassays revealed that the novel floral scent of the hybrids was significantly more attractive than either of the two parents to a pollinator species not initially involved in the pollination of any of the parent Ophrys species. CONCLUSIONS:Collectively, our results illustrate that the process of hybridisation can lead to the generation of evolutionary novelties, and that novel combinations of floral traits can drive pollinator shifts and rapid reproductive isolation in highly specific plant-pollinator interactions.
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Project description:Speciation is typically accompanied by the formation of isolation barriers between lineages. Commonly, reproductive barriers are separated into pre- and post-zygotic mechanisms that can evolve with different speed. In this study, we measured the strength of different reproductive barriers in two closely related, sympatric orchids of the Ophrys insectifera group, namely Ophrys insectifera and Ophrys aymoninii to infer possible mechanisms of speciation. We quantified pre- and post-pollination barriers through observation of pollen flow, by performing artificial inter- and intraspecific crosses and analyzing scent bouquets. Additionally, we investigated differences in mycorrhizal fungi as a potential extrinsic factor of post-zygotic isolation. Our results show that floral isolation mediated by the attraction of different pollinators acts apparently as the sole reproductive barrier between the two orchid species, with later-acting intrinsic barriers seemingly absent. Also, the two orchids share most of their fungal mycorrhizal partners in sympatry, suggesting little or no importance of mycorrhizal symbiosis in reproductive isolation. Key traits underlying floral isolation were two alkenes and wax ester, present predominantly in the floral scent of O. aymoninii. These compounds, when applied to flowers of O. insectifera, triggered attraction and a copulation attempt of the bee pollinator of O. aymoninii and thus led to the (partial) breakdown of floral isolation. Based on our results, we suggest that adaptation to different pollinators, mediated by floral scent, underlies species isolation in this plant group. Pollinator switches may be promoted by low pollination success of individuals in dense patches of plants, an assumption that we also confirmed in our study.
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Project description:The orchids (Orchidaceae) constitute one of the largest and most diverse families of flowering plants. They have evolved a great variety of adaptations to achieve pollination by a diverse group of pollinators. Many orchids reward their pollinators, typically with nectar, but the family is also well-known for employing deceptive pollination strategies in which there is no reward for the pollinator, in the most extreme case by mimicking sexual signals of pollinators. In the European flora, two examples of these different pollination strategies are the sexually deceptive genus Ophrys and the rewarding genus Gymnadenia, which differ in their level of pollinator specialization; Ophrys is typically pollinated by pseudo-copulation of males of a single insect species, whilst Gymnadenia attracts a broad range of floral visitors. Here, we present and describe the annotated floral transcriptome of Ophrys iricolor, an Andrena-pollinated representative of the genus Ophrys that is widespread throughout the Aegean. Furthermore, we present additional floral transcriptomes of both sexually deceptive and rewarding orchids, specifically the deceptive Ophrys insectifera, Ophrys aymoninii, and an updated floral transcriptome of Ophrys sphegodes, as well as the floral transcriptomes of the rewarding orchids Gymnadenia conopsea, Gymnadenia densiflora, Gymnadenia odoratissima, and Gymnadenia rhellicani (syn. Nigritella rhellicani). Comparisons of these novel floral transcriptomes reveal few annotation differences between deceptive and rewarding orchids. Since together, these transcriptomes provide a representative sample of the genus-wide taxonomic diversity within Ophrys and Gymnadenia (Orchidoideae: Orchidinae), we employ a phylogenomic approach to address open questions of phylogenetic relationships within the genera. Specifically, this includes the controversial placement of O. insectifera within the Ophrys phylogeny and the placement of "Nigritella"-type morphologies within the phylogeny of Gymnadenia. Whereas in Gymnadenia, several conflicting topologies are supported by a similar number of gene trees, a majority of Ophrys gene topologies clearly supports a placement of O. insectifera as sister to a clade containing O. sphegodes.
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Project description:Background and aimsSexually deceptive orchids of the genus Ophrys use mimicry of pollinator females to attract specific pollinators. Pollinator shifts may drive speciation in Ophrys, since novel pollinators may in principle act as isolating factors immediately. It is thus possible that evolution of novel species occurs rapidly and with a progenitor-derivative pattern. The aims of this study are to compare genetic structure and diversity among widespread and geographically restricted Ophrys taxa, to test whether genetic structure is associated with specific pollinators, and to investigate whether any widespread species may have acted as a progenitor for the evolution of more restricted taxa.MethodsGenetic differentiation and diversity were investigated in O. leucadica and O. cinereophila, the two taxa of the Ophrys fusca sensu lato complex widespread in the Aegean, and three geographically restricted taxa from Rhodes, O. attaviria, O. parvula and O. persephonae, all differing in their specific pollinators. This was done using amplified fragment length polymorphism (AFLP) DNA fingerprinting, and sequencing of the low-copy nuclear gene LEAFY (LFY).Key resultsAll taxa were found to be separate genetic entities, with O. leucadica forming two geographic groups from the west and east of the Aegean. Genetic structure was significantly shaped by pollinators and geography, and comparison of sequence and AFLP data revealed ancestral polymorphisms shared among several taxa. Among the sampled taxa, O. leucadica harbours the greatest genetic differentiation and geographic structure, and the highest genetic diversity. Part of the genome of O. parvula, endemic to Rhodes, may be derived from O. leucadica.ConclusionsPollinators probably influence the genetic structure of the investigated Ophrys species. The genetic pattern identified is consistent with O. leucadica being the oldest of the sampled taxa, making O. leucadica a candidate progenitor species from which more restricted taxa such as O. parvula may have evolved.
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Project description:Background and aimsThe deception strategies of orchids remain poorly understood, especially in regard to the chemical compounds emitted from their flowers and their interaction with various taxonomic groups of pollinators. We investigated the phylogenetic relationships and compared the variation of floral chemical compounds between food-deceptive Dactylorhiza taxa (D. incarnata var. incarnata and D. incarnata var. ochroleuca, D. fuchsii and D. majalis) from populations in north-eastern Poland. We propose a model of the evolution of deception based on floral chemical signals in this genus.MethodsA Bayesian approach based on polymorphic plastid DNA (trnL, trnF and psbC-trnK), internal transcribed spacer (ITS) sequences and flow cytometry data was applied to confirm the taxonomic status of the studied orchids. We also identified and classified the pollinators and flower visitors in each Dactylorhiza population to the taxonomic level and compared our results with literature data. The chemical composition of pentane and diethyl ether extracts from the flowers was analysed by gas chromatography-mass spectrometry. Variation of the floral chemical components was visualized by non-metric multidimensional scaling based on Bray-Curtis dissimilarity.Key resultsThe genetic distinctiveness of D. incarnata, D. fuchsii and D. majalis was confirmed. No hybrids between them were found, but the chloroplast DNA (cpDNA), ITS haplotypes and flow cytometry showed genetic similarity between D. incarnata var. incarnata and D. incarnata var. ochroleuca. We determined that Apis mellifera (Hymenoptera) was the only shared pollinator of these taxa. Strangalia attenuata and Alosterna tabacicolor (Coleoptera) and Volucella pellucens and V. bombylans (Hymenoptera) were observed pollinating D. fuchsii. Visualization of the emission rates of the 61 floral chemical compounds detected from pentane extracts (mainly hydrocarbons and aldehydes) and the 51 from diethyl extracts (with abundant groups of benzenoids and non-aromatic acids) strongly differentiated D. incarnata, D. fuchsii and D. majalis, while those of the two varieties of D. incarnata (var. incarnata and var. ochroleuca) were almost identical.ConclusionsWhile the genetic data clearly supported the distinct lineages of D. incarnata, D. fuchsii and D. majalis, the patterns of emission of their flower chemical compounds were more complex within the series of shared compounds (alkanes and aldehydes) and taxon-specific compounds (benzenoids and esters). Their floral bouquet can influence the sexual, social and feeding behaviour of pollinators in different ways. We observed that the floral chemical compounds attracted both shared and species-specific pollinators to Dactylorhiza, confirming the multidirectional character of floral chemical signals in these food-deceptive taxa. Reduction of species-specific pollination levels in Dactylorhiza orchid taxa may promote hybridization between them.
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Project description:BackgroundSexually deceptive orchids of the genus Ophrys mimic the mating signals of their pollinator females to attract males as pollinators. This mode of pollination is highly specific and leads to strong reproductive isolation between species. This study aims to identify candidate genes responsible for pollinator attraction and reproductive isolation between three closely related species, O. exaltata, O. sphegodes and O. garganica. Floral traits such as odour, colour and morphology are necessary for successful pollinator attraction. In particular, different odour hydrocarbon profiles have been linked to differences in specific pollinator attraction among these species. Therefore, the identification of genes involved in these traits is important for understanding the molecular basis of pollinator attraction by sexually deceptive orchids.ResultsWe have created floral reference transcriptomes and proteomes for these three Ophrys species using a combination of next-generation sequencing (454 and Solexa), Sanger sequencing, and shotgun proteomics (tandem mass spectrometry). In total, 121 917 unique transcripts and 3531 proteins were identified. This represents the first orchid proteome and transcriptome from the orchid subfamily Orchidoideae. Proteome data revealed proteins corresponding to 2644 transcripts and 887 proteins not observed in the transcriptome. Candidate genes for hydrocarbon and anthocyanin biosynthesis were represented by 156 and 61 unique transcripts in 20 and 7 genes classes, respectively. Moreover, transcription factors putatively involved in the regulation of flower odour, colour and morphology were annotated, including Myb, MADS and TCP factors.ConclusionOur comprehensive data set generated by combining transcriptome and proteome technologies allowed identification of candidate genes for pollinator attraction and reproductive isolation among sexually deceptive orchids. This includes genes for hydrocarbon and anthocyanin biosynthesis and regulation, and the development of floral morphology. These data will serve as an invaluable resource for research in orchid floral biology, enabling studies into the molecular mechanisms of pollinator attraction and speciation.
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Project description:Analyzing the processes that determine whether species boundaries are maintained on secondary contact may shed light on the early phase of speciation. In Anacamptis morio and Anacamptis longicornu, two Mediterranean orchid sister-species, we used molecular and morphological analyses, together with estimates of pollination success and experimental crosses, to assess whether floral isolation can shelter the species' genomes from genetic admixture on secondary contact. We found substantial genetic and morphological homogenization in sympatric populations in combination with an apparent lack of postmating isolation. We further detected asymmetric introgression in the sympatric populations and an imbalance in cytotype representation, which may be due either to a difference in flowering phenology or else be a consequence of cytonuclear incompatibilities. Estimates of genetic clines for markers across sympatric zones revealed markers that significantly deviated from neutral expectations. We observed a significant correlation between spur length and reproductive success in sympatric populations, which may suggest that directional selection is the main cause of morphological differentiation in this species pair. Our results suggest that allopatric divergence has not led to the evolution of sufficient reproductive isolation to prevent genomic admixture on secondary contact in this orchid species pair.
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Project description:Background and aimsPlants use a diverse range of visual and olfactory cues to advertize to pollinators. Australian Chiloglottis orchids employ one to three related chemical variants, all 2,5-dialkylcyclohexane-1,3-diones or 'chiloglottones' to sexually attract their specific male pollinators. Here an investigation was made of the physiological aspects of chiloglottone synthesis and storage that have not previously been examined.MethodsThe location of chiloglottone production was determined and developmental and diurnal changes by GC-MS analysis of floral tissue extracts was monitored in two distantly related Chiloglottis species. Light treatment experiments were also performed using depleted flowers to evaluate if sunlight is required for chiloglottone production; which specific wavelengths of light are required was also determined.Key resultsChiloglottone production only occurs in specific floral tissues (the labellum calli and sepals) of open flowers. Upon flower opening chiloglottone production is rapid and levels remain more or less stable both day and night, and over the 2- to 3-week lifetime of the flower. Furthermore, it was determined that chiloglottone production requires continuous sunlight, and determined the optimal wavelengths of sunlight in the UV-B range (with peak of 300 nm).ConclusionsUV-B light is required for the synthesis of chiloglottones - the semiochemicals used by Chiloglottis orchids to sexually lure their male pollinators. This discovery appears to be the first case to our knowledge where plant floral odour production depends on UV-B radiation at normal levels of sunlight. In the future, identification of the genes and enzymes involved, will allow us to understand better the role of UV-B light in the biosynthesis of chiloglottones.
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