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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...

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Autores principales: Jąkalski, Marcin, Minasiewicz, Julita, Caius, José, May, Michał, Selosse, Marc-André, Delannoy, Etienne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8220222/
https://www.ncbi.nlm.nih.gov/pubmed/34177974
http://dx.doi.org/10.3389/fpls.2021.632033
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author Jąkalski, Marcin
Minasiewicz, Julita
Caius, José
May, Michał
Selosse, Marc-André
Delannoy, Etienne
author_facet Jąkalski, Marcin
Minasiewicz, Julita
Caius, José
May, Michał
Selosse, Marc-André
Delannoy, Etienne
author_sort Jąkalski, Marcin
collection PubMed
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.
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spelling pubmed-82202222021-06-24 The Genomic Impact of Mycoheterotrophy in Orchids Jąkalski, Marcin Minasiewicz, Julita Caius, José May, Michał Selosse, Marc-André Delannoy, Etienne Front Plant Sci Plant Science 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. Frontiers Media S.A. 2021-06-09 /pmc/articles/PMC8220222/ /pubmed/34177974 http://dx.doi.org/10.3389/fpls.2021.632033 Text en Copyright © 2021 Jąkalski, Minasiewicz, Caius, May, Selosse and Delannoy. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Jąkalski, Marcin
Minasiewicz, Julita
Caius, José
May, Michał
Selosse, Marc-André
Delannoy, Etienne
The Genomic Impact of Mycoheterotrophy in Orchids
title 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_short The Genomic Impact of Mycoheterotrophy in Orchids
title_sort genomic impact of mycoheterotrophy in orchids
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8220222/
https://www.ncbi.nlm.nih.gov/pubmed/34177974
http://dx.doi.org/10.3389/fpls.2021.632033
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