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Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages

Mycoheterotrophy is an alternative nutritional strategy whereby plants obtain sugars and other nutrients from soil fungi. Mycoheterotrophy and associated loss of photosynthesis have evolved repeatedly in plants, particularly in monocots. Although reductive evolution of plastomes in mycoheterotrophs...

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Autores principales: Timilsena, Prakash Raj, Barrett, Craig F, Piñeyro-Nelson, Alma, Wafula, Eric K, Ayyampalayam, Saravanaraj, McNeal, Joel R, Yukawa, Tomohisa, Givnish, Thomas J, Graham, Sean W, Pires, J Chris, Davis, Jerrold I, Ané, Cécile, Stevenson, Dennis W, Leebens-Mack, Jim, Martínez-Salas, Esteban, Álvarez-Buylla, Elena R, dePamphilis, Claude W
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9887272/
https://www.ncbi.nlm.nih.gov/pubmed/36582124
http://dx.doi.org/10.1093/gbe/evac183
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author Timilsena, Prakash Raj
Barrett, Craig F
Piñeyro-Nelson, Alma
Wafula, Eric K
Ayyampalayam, Saravanaraj
McNeal, Joel R
Yukawa, Tomohisa
Givnish, Thomas J
Graham, Sean W
Pires, J Chris
Davis, Jerrold I
Ané, Cécile
Stevenson, Dennis W
Leebens-Mack, Jim
Martínez-Salas, Esteban
Álvarez-Buylla, Elena R
dePamphilis, Claude W
author_facet Timilsena, Prakash Raj
Barrett, Craig F
Piñeyro-Nelson, Alma
Wafula, Eric K
Ayyampalayam, Saravanaraj
McNeal, Joel R
Yukawa, Tomohisa
Givnish, Thomas J
Graham, Sean W
Pires, J Chris
Davis, Jerrold I
Ané, Cécile
Stevenson, Dennis W
Leebens-Mack, Jim
Martínez-Salas, Esteban
Álvarez-Buylla, Elena R
dePamphilis, Claude W
author_sort Timilsena, Prakash Raj
collection PubMed
description Mycoheterotrophy is an alternative nutritional strategy whereby plants obtain sugars and other nutrients from soil fungi. Mycoheterotrophy and associated loss of photosynthesis have evolved repeatedly in plants, particularly in monocots. Although reductive evolution of plastomes in mycoheterotrophs is well documented, the dynamics of nuclear genome evolution remains largely unknown. Transcriptome datasets were generated from four mycoheterotrophs in three families (Orchidaceae, Burmanniaceae, Triuridaceae) and related green plants and used for phylogenomic analyses to resolve relationships among the mycoheterotrophs, their relatives, and representatives across the monocots. Phylogenetic trees based on 602 genes were mostly congruent with plastome phylogenies, except for an Asparagales + Liliales clade inferred in the nuclear trees. Reduction and loss of chlorophyll synthesis and photosynthetic gene expression and relaxation of purifying selection on retained genes were progressive, with greater loss in older nonphotosynthetic lineages. One hundred seventy-four of 1375 plant benchmark universally conserved orthologous genes were undetected in any mycoheterotroph transcriptome or the genome of the mycoheterotrophic orchid Gastrodia but were expressed in green relatives, providing evidence for massively convergent gene loss in nonphotosynthetic lineages. We designate this set of deleted or undetected genes Missing in Mycoheterotrophs (MIM). MIM genes encode not only mainly photosynthetic or plastid membrane proteins but also a diverse set of plastid processes, genes of unknown function, mitochondrial, and cellular processes. Transcription of a photosystem II gene (psb29) in all lineages implies a nonphotosynthetic function for this and other genes retained in mycoheterotrophs. Nonphotosynthetic plants enable novel insights into gene function as well as gene expression shifts, gene loss, and convergence in nuclear genomes.
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spelling pubmed-98872722023-01-31 Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages Timilsena, Prakash Raj Barrett, Craig F Piñeyro-Nelson, Alma Wafula, Eric K Ayyampalayam, Saravanaraj McNeal, Joel R Yukawa, Tomohisa Givnish, Thomas J Graham, Sean W Pires, J Chris Davis, Jerrold I Ané, Cécile Stevenson, Dennis W Leebens-Mack, Jim Martínez-Salas, Esteban Álvarez-Buylla, Elena R dePamphilis, Claude W Genome Biol Evol Research Article Mycoheterotrophy is an alternative nutritional strategy whereby plants obtain sugars and other nutrients from soil fungi. Mycoheterotrophy and associated loss of photosynthesis have evolved repeatedly in plants, particularly in monocots. Although reductive evolution of plastomes in mycoheterotrophs is well documented, the dynamics of nuclear genome evolution remains largely unknown. Transcriptome datasets were generated from four mycoheterotrophs in three families (Orchidaceae, Burmanniaceae, Triuridaceae) and related green plants and used for phylogenomic analyses to resolve relationships among the mycoheterotrophs, their relatives, and representatives across the monocots. Phylogenetic trees based on 602 genes were mostly congruent with plastome phylogenies, except for an Asparagales + Liliales clade inferred in the nuclear trees. Reduction and loss of chlorophyll synthesis and photosynthetic gene expression and relaxation of purifying selection on retained genes were progressive, with greater loss in older nonphotosynthetic lineages. One hundred seventy-four of 1375 plant benchmark universally conserved orthologous genes were undetected in any mycoheterotroph transcriptome or the genome of the mycoheterotrophic orchid Gastrodia but were expressed in green relatives, providing evidence for massively convergent gene loss in nonphotosynthetic lineages. We designate this set of deleted or undetected genes Missing in Mycoheterotrophs (MIM). MIM genes encode not only mainly photosynthetic or plastid membrane proteins but also a diverse set of plastid processes, genes of unknown function, mitochondrial, and cellular processes. Transcription of a photosystem II gene (psb29) in all lineages implies a nonphotosynthetic function for this and other genes retained in mycoheterotrophs. Nonphotosynthetic plants enable novel insights into gene function as well as gene expression shifts, gene loss, and convergence in nuclear genomes. Oxford University Press 2022-12-30 /pmc/articles/PMC9887272/ /pubmed/36582124 http://dx.doi.org/10.1093/gbe/evac183 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Timilsena, Prakash Raj
Barrett, Craig F
Piñeyro-Nelson, Alma
Wafula, Eric K
Ayyampalayam, Saravanaraj
McNeal, Joel R
Yukawa, Tomohisa
Givnish, Thomas J
Graham, Sean W
Pires, J Chris
Davis, Jerrold I
Ané, Cécile
Stevenson, Dennis W
Leebens-Mack, Jim
Martínez-Salas, Esteban
Álvarez-Buylla, Elena R
dePamphilis, Claude W
Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title_full Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title_fullStr Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title_full_unstemmed Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title_short Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages
title_sort phylotranscriptomic analyses of mycoheterotrophic monocots show a continuum of convergent evolutionary changes in expressed nuclear genes from three independent nonphotosynthetic lineages
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9887272/
https://www.ncbi.nlm.nih.gov/pubmed/36582124
http://dx.doi.org/10.1093/gbe/evac183
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