The Genomic Impact of Mycoheterotrophy in Orchids

Mycoheterotrophic plants have lost the ability to photosynthesize and obtain essential mineral and organic nutrients from associated soil fungi. Despite involving radical changes in life history traits and ecological requirements, the transition from autotrophy to mycoheterotrophy has occurred indep...

Full description

Bibliographic Details
Main Authors: Marcin Jąkalski, Julita Minasiewicz, José Caius, Michał May, Marc-André Selosse, Etienne Delannoy
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.632033/full
id doaj-632f0a8f74a340b7b9789acc58f86f76
record_format Article
spelling doaj-632f0a8f74a340b7b9789acc58f86f762021-06-09T06:46:33ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-06-011210.3389/fpls.2021.632033632033The Genomic Impact of Mycoheterotrophy in OrchidsMarcin Jąkalski0Julita Minasiewicz1José Caius2José Caius3Michał May4Marc-André Selosse5Marc-André Selosse6Etienne Delannoy7Etienne Delannoy8Department of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, PolandDepartment of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, PolandInstitute of Plant Sciences Paris-Saclay, Université Paris-Saclay, CNRS, INRAE, Univ Evry, Orsay, FranceUniversité de Paris, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay, Orsay, FranceDepartment of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, PolandDepartment of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, PolandSorbonne Université, CNRS, EPHE, Muséum National d’Histoire Naturelle, Institut de Systématique, Evolution, Biodiversité, Paris, FranceInstitute of Plant Sciences Paris-Saclay, Université Paris-Saclay, CNRS, INRAE, Univ Evry, Orsay, FranceUniversité de Paris, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay, Orsay, FranceMycoheterotrophic plants have lost the ability to photosynthesize and obtain essential mineral and organic nutrients from associated soil fungi. Despite involving radical changes in life history traits and ecological requirements, the transition from autotrophy to mycoheterotrophy has occurred independently in many major lineages of land plants, most frequently in Orchidaceae. Yet the molecular mechanisms underlying this shift are still poorly understood. A comparison of the transcriptomes of Epipogium aphyllum and Neottia nidus-avis, two completely mycoheterotrophic orchids, to other autotrophic and mycoheterotrophic orchids showed the unexpected retention of several genes associated with photosynthetic activities. In addition to these selected retentions, the analysis of their expression profiles showed that many orthologs had inverted underground/aboveground expression ratios compared to autotrophic species. Fatty acid and amino acid biosynthesis as well as primary cell wall metabolism were among the pathways most impacted by this expression reprogramming. Our study suggests that the shift in nutritional mode from autotrophy to mycoheterotrophy remodeled the architecture of the plant metabolism but was associated primarily with function losses rather than metabolic innovations.https://www.frontiersin.org/articles/10.3389/fpls.2021.632033/fullmycorrhizaphotosynthesismetabolic evolutionmycoheterotrophyorchidstranscriptome
collection DOAJ
language English
format Article
sources DOAJ
author Marcin Jąkalski
Julita Minasiewicz
José Caius
José Caius
Michał May
Marc-André Selosse
Marc-André Selosse
Etienne Delannoy
Etienne Delannoy
spellingShingle Marcin Jąkalski
Julita Minasiewicz
José Caius
José Caius
Michał May
Marc-André Selosse
Marc-André Selosse
Etienne Delannoy
Etienne Delannoy
The Genomic Impact of Mycoheterotrophy in Orchids
Frontiers in Plant Science
mycorrhiza
photosynthesis
metabolic evolution
mycoheterotrophy
orchids
transcriptome
author_facet Marcin Jąkalski
Julita Minasiewicz
José Caius
José Caius
Michał May
Marc-André Selosse
Marc-André Selosse
Etienne Delannoy
Etienne Delannoy
author_sort Marcin Jąkalski
title The Genomic Impact of Mycoheterotrophy in Orchids
title_short The Genomic Impact of Mycoheterotrophy in Orchids
title_full The Genomic Impact of Mycoheterotrophy in Orchids
title_fullStr The Genomic Impact of Mycoheterotrophy in Orchids
title_full_unstemmed The Genomic Impact of Mycoheterotrophy in Orchids
title_sort genomic impact of mycoheterotrophy in orchids
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-06-01
description Mycoheterotrophic plants have lost the ability to photosynthesize and obtain essential mineral and organic nutrients from associated soil fungi. Despite involving radical changes in life history traits and ecological requirements, the transition from autotrophy to mycoheterotrophy has occurred independently in many major lineages of land plants, most frequently in Orchidaceae. Yet the molecular mechanisms underlying this shift are still poorly understood. A comparison of the transcriptomes of Epipogium aphyllum and Neottia nidus-avis, two completely mycoheterotrophic orchids, to other autotrophic and mycoheterotrophic orchids showed the unexpected retention of several genes associated with photosynthetic activities. In addition to these selected retentions, the analysis of their expression profiles showed that many orthologs had inverted underground/aboveground expression ratios compared to autotrophic species. Fatty acid and amino acid biosynthesis as well as primary cell wall metabolism were among the pathways most impacted by this expression reprogramming. Our study suggests that the shift in nutritional mode from autotrophy to mycoheterotrophy remodeled the architecture of the plant metabolism but was associated primarily with function losses rather than metabolic innovations.
topic mycorrhiza
photosynthesis
metabolic evolution
mycoheterotrophy
orchids
transcriptome
url https://www.frontiersin.org/articles/10.3389/fpls.2021.632033/full
work_keys_str_mv AT marcinjakalski thegenomicimpactofmycoheterotrophyinorchids
AT julitaminasiewicz thegenomicimpactofmycoheterotrophyinorchids
AT josecaius thegenomicimpactofmycoheterotrophyinorchids
AT josecaius thegenomicimpactofmycoheterotrophyinorchids
AT michałmay thegenomicimpactofmycoheterotrophyinorchids
AT marcandreselosse thegenomicimpactofmycoheterotrophyinorchids
AT marcandreselosse thegenomicimpactofmycoheterotrophyinorchids
AT etiennedelannoy thegenomicimpactofmycoheterotrophyinorchids
AT etiennedelannoy thegenomicimpactofmycoheterotrophyinorchids
AT marcinjakalski genomicimpactofmycoheterotrophyinorchids
AT julitaminasiewicz genomicimpactofmycoheterotrophyinorchids
AT josecaius genomicimpactofmycoheterotrophyinorchids
AT josecaius genomicimpactofmycoheterotrophyinorchids
AT michałmay genomicimpactofmycoheterotrophyinorchids
AT marcandreselosse genomicimpactofmycoheterotrophyinorchids
AT marcandreselosse genomicimpactofmycoheterotrophyinorchids
AT etiennedelannoy genomicimpactofmycoheterotrophyinorchids
AT etiennedelannoy genomicimpactofmycoheterotrophyinorchids
_version_ 1721388243797147648