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, Craig F Barrett Department of Biology, West Virginia University , Morgantown, WV 26506 , USA For correspondence. E-mail craig.barrett@mail.wvu.edu Search for other works by this author on: Oxford Academic Matthew C Pace New York Botanical Garden , Bronx, New York, NY 10458 , USA Search for other works by this author on: Oxford Academic Cameron W Corbett Department of Biology, West Virginia University , Morgantown, WV 26506 , USA Search for other works by this author on: Oxford Academic Aaron H Kennedy Mycology and Nematology Genetic Diversity and Biology Laboratory, USDA-APHIS , Beltsville, MD 20705 , USA Search for other works by this author on: Oxford Academic Hana L Thixton-Nolan Department of Biology, West Virginia University , Morgantown, WV 26506 , USA Search for other works by this author on: Oxford Academic John V Freudenstein Department of Evolution, Ecology, and Organismal Biology, Ohio State University , Columbus, OH 43212 , USA Search for other works by this author on: Oxford Academic
Annals of Botany, mcae084, https://doi.org/10.1093/aob/mcae084
Published:
28 May 2024
Article history
Received:
06 March 2024
Revision requested:
17 May 2024
Editorial decision:
22 May 2024
Accepted:
27 May 2024
Published:
28 May 2024
Corrected and typeset:
14 June 2024
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Craig F Barrett, Matthew C Pace, Cameron W Corbett, Aaron H Kennedy, Hana L Thixton-Nolan, John V Freudenstein, Organellar phylogenomics at the epidendroid orchid base, with a focus on the mycoheterotrophic Wullschlaegelia, Annals of Botany, 2024;, mcae084, https://doi.org/10.1093/aob/mcae084
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Abstract
Background and Aims
Heterotrophic plants have long been a challenge for systematists, exemplified by the base of the orchid subfamily Epidendroideae, which contains numerous mycoheterotrophic species.
Methods
Here we address the utility of organellar genomes in resolving relationships at the epidendroid base, specifically employing models of heterotachy, or lineage-specific rate variation over time. We further conduct comparative analyses of plastid genome evolution in heterotrophs and structural variation in matK.
Key Results
We present the first complete plastid genomes (plastomes) of Wullschlaegelia, the sole genus of the tribe Wullschlaegelieae, revealing a highly reduced genome of 37kb, which retains a fraction of the genes present in related autotrophs. Plastid phylogenomic analyses recovered a strongly supported clade composed exclusively of mycoheterotrophic species with long branches. We further analysed mitochondrial gene sets, which recovered similar relationships to those in other studies using nuclear data, but the placement of Wullschlaegelia remains uncertain. We conducted comparative plastome analyses among Wullschlaegelia and other heterotrophic orchids, revealing a suite of correlated substitutional and structural changes relative to autotrophic species. Lastly, we investigated evolutionary and structural variation in matK, which is retained in Wullschlaegelia and a few other ‘late stage’ heterotrophs and found evidence for structural conservation despite rapid substitution rates in both Wullschlaegelia and the leafless Gastrodia.
Conclusions
Our analyses reveal the limits of what the plastid genome can tell us on orchid relationships in this part of the tree, even when applying parameter-rich heterotachy models. Our study underscores the need for increased taxon sampling across all three genomes at the epidendroid base, and illustrates the need for further research on addressing heterotachy in phylogenomic analyses.
Orchidaceae, Epidendroideae, herbarium, mycoheterotrophy, comparative genomics, plastid, mitochondrial, heterotachy, Wullschlaegelia calcarata, Triphora trianthophoros, Triphora aff. wagneri, Uleiorchis ulei
© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.
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