Thirteen New Plastid Genomes from Mixotrophic and Autotrophic Species Provide Insights into Heterotrophy Evolution in Neottieae Orchids

Mixotrophic species use both organic and mineral carbon sources. Some mixotrophic plants combine photosynthesis and a nutrition called mycoheterotrophy, where carbon is obtained from fungi forming mycorrhizal symbiosis with their roots. These species can lose photosynthetic abilities and evolve full mycoheterotrophy. Besides morphological changes, the latter transition is associated with a deep alteration of the plastid genome. Photosynthesis-related genes are lost first, followed by housekeeping genes, eventually resulting in a highly reduced genome. Whether relaxation of selective constraints already occurs for the plastid genome of mixotrophic species, which remain photosynthetic, is unclear. This is partly due to the difficulty of comparing plastid genomes of autotrophic, mixotrophic, and mycoheterotrophic species in a narrow phylogenetic framework. We address this question in the orchid tribe Neottieae, where this large assortment of nutrition types occurs. We sequenced 13 new plastid genomes, including 9 mixotrophic species and covering all 6 Neottieae genera. We investigated selective pressure on plastid genes in each nutrition type and conducted a phylogenetic inference of the group. Surprisingly, photosynthesis-related genes did not experience selection relaxation in mixotrophic species compared with autotrophic relatives. Conversely, we observed evidence for selection intensification for some plastid genes. Photosynthesis is thus still under purifying selection, maybe because of its role in fruit formation and thus reproductive success. Phylogenetic analysis resolved most relationships, but short branches at the base of the tree suggest an evolutionary radiation at the beginning of Neottieae history, which, we hypothesize, may be linked to mixotrophy emergence. © 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Lallemand F.1 , Logacheva M.2, 3 , Le Clainche I. , Bérard A.4 , Zheleznaia E. 5 , May M.6 , Jakalski M.6 , Delannoy É.7, 8 , Le Paslier M.-C. , Selosse M.-A.1, 6
Oxford University Press
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  • 1 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Paris, France
  • 2 Laboratory of Plant Genomics, Institute for Information Transmission Problems, Moscow, Russian Federation
  • 3 Skolkovo Institute of Science and Technology, Moscow, Russian Federation
  • 4 Etude du Polymorphisme des Génomes Végétaux (EPGV), INRA, Université Paris-Saclay, Evry, France
  • 5 Peoples' Friendship University of Russia, Timiryazev State Biological Museum, Moscow, Russian Federation
  • 6 Faculty of Biology, Department of Plant Taxonomy and Nature Conservation, University of Gdańsk, Poland
  • 7 Institute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRA, Université Paris-Sud, Orsay, France
  • 8 Université Evry, Université Paris-Saclay, Orsay, France
Ключевые слова
mixotrophy; mycoheterotrophy; Mycorrhiza; Neottieae; phylogeny; plastome
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