Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids

Institutes of Systematic Botany, University of Zürich and Zürich-Basel Plant Science Center, CH-8008 Zurich, Switzerland.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 03/2011; 108(14):5696-701. DOI: 10.1073/pnas.1013313108
Source: PubMed


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 and SAD2, is flower-specific and broadly parallels alkene production during flower development. SAD2 shows a significant association with alkene production, and in vitro assays show that O. sphegodes SAD2 has activity both as an 18:0-ACP Δ(9) and a 16:0-ACP Δ(4) desaturase. Downstream metabolism of the SAD2 reaction products would give rise to alkenes with double-bonds at position 9 or position 12, matching double-bond positions observed in alkenes in the odor bouquet of O. sphegodes. SAD1 and SAD2 show evidence of purifying selection before, and positive or relaxed purifying selection after gene duplication. By contributing to the production of species-specific alkene bouquets, SAD2 is suggested to contribute to differential pollinator attraction and reproductive isolation among these species. Taken together, these data are consistent with the hypothesis that SAD2 is a florally expressed barrier gene of large phenotypic effect and, possibly, a genic target of pollinator-mediated selection.

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    • "Specifically, SAD2A synthesizes the precursor of 12-alk- enes from a C 16 FA-ACP substrate (Schl€ uter et al. 2011b), and it is conceivable (but so far untested) that SAD5A might also use an C 16 -ACP precursor for 7-alkene biosynthesis (Xu et al. 2012a). "
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    ABSTRACT: Divergent selection by pollinators can bring about strong reproductive isolation via changes at few genes of large effect. This has recently been demonstrated in sexually deceptive orchids, where studies (1) quantified the strength of reproductive isolation in the field; (2) identified genes that appear to be causal for reproductive isolation; and (3) demonstrated selection by analysis of natural variation in gene sequence and expression. In a group of closely related Ophrys orchids, specific floral scent components, namely n-alkenes, are the key floral traits that control specific pollinator attraction by chemical mimicry of insect sex pheromones. The genetic basis of species-specific differences in alkene production mainly lies in two biosynthetic genes encoding stearoyl–acyl carrier protein desaturases (SAD) that are associated with floral scent variation and reproductive isolation between closely related species, and evolve under pollinator-mediated selection. However, the implications of this genetic architecture of key floral traits on the evolutionary processes of pollinator adaptation and speciation in this plant group remain unclear. Here, we expand on these recent findings to model scenarios of adaptive evolutionary change at SAD2 and SAD5, their effects on plant fitness (i.e., offspring number), and the dynamics of speciation. Our model suggests that the two-locus architecture of reproductive isolation allows for rapid sympatric speciation by pollinator shift; however, the likelihood of such pollinator-mediated speciation is asymmetric between the two orchid species O. sphegodes and O. exaltata due to different fitness effects of their predominant SAD2 and SAD5 alleles. Our study not only provides insight into pollinator adaptation and speciation mechanisms of sexually deceptive orchids but also demonstrates the power of applying a modeling approach to the study of pollinator-driven ecological speciation.
    Ecology and Evolution 12/2014; 5(2). DOI:10.1002/ece3.1378 · 2.32 Impact Factor
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    • "Floral isolation is easier to achieve by shifting between pollinators with similar sexual pheromones (e.g. from one Andrena species to another) than by shifting between pollinators with very different pheromone systems. Indeed, in the former case, only a few slight changes in the genes involved in scent production can be sufficient to attract a different, but related, pollinator species (Schl€ uter et al., 2011b), as was shown in the O. sphegodes group (Xu et al., 2011a, 2012; Sedeek et al., 2014). Thus, a factor further prompting radiation of some Ophrys lineages might be the adoption of one of the most species-rich bee genera, such as Andrena (c. "
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    ABSTRACT: Episodes of rapid speciation provide unique insights into evolutionary processes underlying species radiations and patterns of biodiversity. Here we investigated the radiation of sexually deceptive bee orchids (Ophrys). Based on a time-calibrated phylogeny and by means of ancestral character reconstruction and divergence time estimation, we estimated the tempo and mode of this radiation within a state-dependent evolutionary framework. It appears that, in the Pleistocene, the evolution of Ophrys was marked by episodes of rapid diversification coinciding with shifts to different pollinator types: from wasps to Eucera bees to Andrena and other bees. An abrupt increase in net diversification rate was detected in three clades. Among these, two phylogenetically distant lineages switched from Eucera to Andrena and other bees in a parallel fashion and at about the same time in their evolutionary history. Lack of early radiation associated with the evolution of the key innovation of sexual deception suggests that Ophrys diversification was mainly driven by subsequent ecological opportunities provided by the exploitation of novel pollinator groups, encompassing many bee species slightly differing in their sex pheromone communication systems, and by spatiotemporal fluctuations in the pollinator mosaic.
    New Phytologist 12/2014; 207(2). DOI:10.1111/nph.13219 · 7.67 Impact Factor
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    • "is gene catalyses specific double - bond insertion into precursors of alkenes , and SAD2 alleles with different enzymatic activities are differentially expressed between the two species ; SAD2 thereby contributes to a major difference in hydrocarbon composition between Exa and Sph / Gar that demonstrably affects pollinator attraction and thus RI ( Schlüter et al . 2011b ; Xu et al . 2012a ) . In principle , other genes affecting pseudo - pheromone production ( see Sedeek et al . 2013 ) may also be expected to respond to divergent selection by pollinators . Here , two annotated genes , VPS45 and CER1 , were identified among the GBS tags containing F ST outliers . Arabidopsis VPS45 is an SM protein famil"
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    ABSTRACT: High pollinator specificity and the potential for simple genetic changes to affect pollinator attraction make sexually deceptive orchids an ideal system for the study of ecological speciation, in which change of flower odour is likely important. This study surveys reproductive barriers and differences in floral phenotypes in a group of four closely related, co-flowering sympatric Ophrys species, and uses a genotyping by sequencing (GBS) approach to obtain information on the proportion of the genome that is differentiated between species. Ophrys species were found to effectively lack post-pollination barriers, but are strongly isolated by their different pollinators (floral isolation), and to a smaller extent, by shifts in flowering time (temporal isolation). Although flower morphology and perhaps labellum coloration may contribute to floral isolation, reproductive barriers may largely be due to differences in flower odour chemistry. GBS revealed shared polymorphism throughout the Ophrys genome, with very little population structure between species. Genome scans for FST outliers identified few markers that are highly differentiated between species and repeatable in several populations. These genome scans also revealed highly differentiated polymorphisms in genes with putative involvement in floral odour production, including a previously identified candidate gene thought to be involved in the biosynthesis of pseudo-pheromones by the orchid flowers. Taken together, these data suggest that ecological speciation associated with different pollinators in sexually deceptive orchids has a genic rather than a genomic basis, placing these species at an early phase of genomic divergence within the 'speciation continuum'. This article is protected by copyright. All rights reserved.
    Molecular Ecology 11/2014; 23(24). DOI:10.1111/mec.12992 · 6.49 Impact Factor
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