A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia

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-...

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Main Authors: Laura Piñeiro Fernández, Kelsey J. R .P. Byers, Jing Cai, Khalid E. M. Sedeek, Roman T. Kellenberger, Alessia Russo, Weihong Qi, Catharine Aquino Fournier, Philipp M. Schlüter
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01553/full
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author Laura Piñeiro Fernández
Laura Piñeiro Fernández
Kelsey J. R .P. Byers
Kelsey J. R .P. Byers
Jing Cai
Jing Cai
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Roman T. Kellenberger
Roman T. Kellenberger
Alessia Russo
Alessia Russo
Alessia Russo
Weihong Qi
Catharine Aquino Fournier
Philipp M. Schlüter
author_facet Laura Piñeiro Fernández
Laura Piñeiro Fernández
Kelsey J. R .P. Byers
Kelsey J. R .P. Byers
Jing Cai
Jing Cai
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Roman T. Kellenberger
Roman T. Kellenberger
Alessia Russo
Alessia Russo
Alessia Russo
Weihong Qi
Catharine Aquino Fournier
Philipp M. Schlüter
author_sort Laura Piñeiro Fernández
collection DOAJ
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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spelling doaj.art-ffccbbfd9443471eb203e535006104de2022-12-21T18:47:11ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-11-011010.3389/fpls.2019.01553486233A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and GymnadeniaLaura Piñeiro Fernández0Laura Piñeiro Fernández1Kelsey J. R .P. Byers2Kelsey J. R .P. Byers3Jing Cai4Jing Cai5Khalid E. M. Sedeek6Khalid E. M. Sedeek7Khalid E. M. Sedeek8Roman T. Kellenberger9Roman T. Kellenberger10Alessia Russo11Alessia Russo12Alessia Russo13Weihong Qi14Catharine Aquino Fournier15Philipp M. Schlüter16Institute of Botany, University of Hohenheim, Stuttgart, GermanyDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandDepartment of Zoology, University of Cambridge, Cambridge, United KingdomDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandCenter for Ecological and Environmental Sciences, Northwestern Polytechnical University, Xi’an, ChinaDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandLaboratory for Genome Engineering and Synthetic Biology, Division of Biological Sciences, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaAgricultural Genetic Engineering Research Institute (AGERI), Agriculture Research Centre, Giza, EgyptDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandDepartment of Plant Sciences, University of Cambridge, Cambridge, United KingdomInstitute of Botany, University of Hohenheim, Stuttgart, GermanyDepartment of Systematic and Evolutionary Botany, University of Zurich, Zurich, SwitzerlandDepartment of Plant and Microbial Biology, University of Zurich, Zurich, SwitzerlandFunctional Genomics Centre Zurich, Zurich, SwitzerlandFunctional Genomics Centre Zurich, Zurich, SwitzerlandInstitute of Botany, University of Hohenheim, Stuttgart, GermanyThe 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.https://www.frontiersin.org/article/10.3389/fpls.2019.01553/fullphylogenomicsorchidsOphrysGymnadeniatranscriptomepollination strategy
spellingShingle Laura Piñeiro Fernández
Laura Piñeiro Fernández
Kelsey J. R .P. Byers
Kelsey J. R .P. Byers
Jing Cai
Jing Cai
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Khalid E. M. Sedeek
Roman T. Kellenberger
Roman T. Kellenberger
Alessia Russo
Alessia Russo
Alessia Russo
Weihong Qi
Catharine Aquino Fournier
Philipp M. Schlüter
A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
Frontiers in Plant Science
phylogenomics
orchids
Ophrys
Gymnadenia
transcriptome
pollination strategy
title A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
title_full A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
title_fullStr A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
title_full_unstemmed A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
title_short A Phylogenomic Analysis of the Floral Transcriptomes of Sexually Deceptive and Rewarding European Orchids, Ophrys and Gymnadenia
title_sort phylogenomic analysis of the floral transcriptomes of sexually deceptive and rewarding european orchids ophrys and gymnadenia
topic phylogenomics
orchids
Ophrys
Gymnadenia
transcriptome
pollination strategy
url https://www.frontiersin.org/article/10.3389/fpls.2019.01553/full
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