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Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes

We assess relationships among 192 species in all 12 monocot orders and 72 of 77 families, using 602 conserved single-copy (CSC) genes and 1375 benchmarking single-copy ortholog (BUSCO) genes extracted from genomic and transcriptomic datasets. Phylogenomic inferences based on these data, using both c...

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Autores principales: Timilsena, Prakash Raj, Wafula, Eric K., Barrett, Craig F., Ayyampalayam, Saravanaraj, McNeal, Joel R., Rentsch, Jeremy D., McKain, Michael R., Heyduk, Karolina, Harkess, Alex, Villegente, Matthieu, Conran, John G., Illing, Nicola, Fogliani, Bruno, Ané, Cécile, Pires, J. Chris, Davis, Jerrold I., Zomlefer, Wendy B., Stevenson, Dennis W., Graham, Sean W., Givnish, Thomas J., Leebens-Mack, James, dePamphilis, Claude W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723157/
https://www.ncbi.nlm.nih.gov/pubmed/36483967
http://dx.doi.org/10.3389/fpls.2022.876779
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author Timilsena, Prakash Raj
Wafula, Eric K.
Barrett, Craig F.
Ayyampalayam, Saravanaraj
McNeal, Joel R.
Rentsch, Jeremy D.
McKain, Michael R.
Heyduk, Karolina
Harkess, Alex
Villegente, Matthieu
Conran, John G.
Illing, Nicola
Fogliani, Bruno
Ané, Cécile
Pires, J. Chris
Davis, Jerrold I.
Zomlefer, Wendy B.
Stevenson, Dennis W.
Graham, Sean W.
Givnish, Thomas J.
Leebens-Mack, James
dePamphilis, Claude W.
author_facet Timilsena, Prakash Raj
Wafula, Eric K.
Barrett, Craig F.
Ayyampalayam, Saravanaraj
McNeal, Joel R.
Rentsch, Jeremy D.
McKain, Michael R.
Heyduk, Karolina
Harkess, Alex
Villegente, Matthieu
Conran, John G.
Illing, Nicola
Fogliani, Bruno
Ané, Cécile
Pires, J. Chris
Davis, Jerrold I.
Zomlefer, Wendy B.
Stevenson, Dennis W.
Graham, Sean W.
Givnish, Thomas J.
Leebens-Mack, James
dePamphilis, Claude W.
author_sort Timilsena, Prakash Raj
collection PubMed
description We assess relationships among 192 species in all 12 monocot orders and 72 of 77 families, using 602 conserved single-copy (CSC) genes and 1375 benchmarking single-copy ortholog (BUSCO) genes extracted from genomic and transcriptomic datasets. Phylogenomic inferences based on these data, using both coalescent-based and supermatrix analyses, are largely congruent with the most comprehensive plastome-based analysis, and nuclear-gene phylogenomic analyses with less comprehensive taxon sampling. The strongest discordance between the plastome and nuclear gene analyses is the monophyly of a clade comprising Asparagales and Liliales in our nuclear gene analyses, versus the placement of Asparagales and Liliales as successive sister clades to the commelinids in the plastome tree. Within orders, around six of 72 families shifted positions relative to the recent plastome analysis, but four of these involve poorly supported inferred relationships in the plastome-based tree. In Poales, the nuclear data place a clade comprising Ecdeiocoleaceae+Joinvilleaceae as sister to the grasses (Poaceae); Typhaceae, (rather than Bromeliaceae) are resolved as sister to all other Poales. In Commelinales, nuclear data place Philydraceae sister to all other families rather than to a clade comprising Haemodoraceae+Pontederiaceae as seen in the plastome tree. In Liliales, nuclear data place Liliaceae sister to Smilacaceae, and Melanthiaceae are placed sister to all other Liliales except Campynemataceae. Finally, in Alismatales, nuclear data strongly place Tofieldiaceae, rather than Araceae, as sister to all the other families, providing an alternative resolution of what has been the most problematic node to resolve using plastid data, outside of those involving achlorophyllous mycoheterotrophs. As seen in numerous prior studies, the placement of orders Acorales and Alismatales as successive sister lineages to all other extant monocots. Only 21.2% of BUSCO genes were demonstrably single-copy, yet phylogenomic inferences based on BUSCO and CSC genes did not differ, and overall functional annotations of the two sets were very similar. Our analyses also reveal significant gene tree-species tree discordance despite high support values, as expected given incomplete lineage sorting (ILS) related to rapid diversification. Our study advances understanding of monocot relationships and the robustness of phylogenetic inferences based on large numbers of nuclear single-copy genes that can be obtained from transcriptomes and genomes.
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spelling pubmed-97231572022-12-07 Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes Timilsena, Prakash Raj Wafula, Eric K. Barrett, Craig F. Ayyampalayam, Saravanaraj McNeal, Joel R. Rentsch, Jeremy D. McKain, Michael R. Heyduk, Karolina Harkess, Alex Villegente, Matthieu Conran, John G. Illing, Nicola Fogliani, Bruno Ané, Cécile Pires, J. Chris Davis, Jerrold I. Zomlefer, Wendy B. Stevenson, Dennis W. Graham, Sean W. Givnish, Thomas J. Leebens-Mack, James dePamphilis, Claude W. Front Plant Sci Plant Science We assess relationships among 192 species in all 12 monocot orders and 72 of 77 families, using 602 conserved single-copy (CSC) genes and 1375 benchmarking single-copy ortholog (BUSCO) genes extracted from genomic and transcriptomic datasets. Phylogenomic inferences based on these data, using both coalescent-based and supermatrix analyses, are largely congruent with the most comprehensive plastome-based analysis, and nuclear-gene phylogenomic analyses with less comprehensive taxon sampling. The strongest discordance between the plastome and nuclear gene analyses is the monophyly of a clade comprising Asparagales and Liliales in our nuclear gene analyses, versus the placement of Asparagales and Liliales as successive sister clades to the commelinids in the plastome tree. Within orders, around six of 72 families shifted positions relative to the recent plastome analysis, but four of these involve poorly supported inferred relationships in the plastome-based tree. In Poales, the nuclear data place a clade comprising Ecdeiocoleaceae+Joinvilleaceae as sister to the grasses (Poaceae); Typhaceae, (rather than Bromeliaceae) are resolved as sister to all other Poales. In Commelinales, nuclear data place Philydraceae sister to all other families rather than to a clade comprising Haemodoraceae+Pontederiaceae as seen in the plastome tree. In Liliales, nuclear data place Liliaceae sister to Smilacaceae, and Melanthiaceae are placed sister to all other Liliales except Campynemataceae. Finally, in Alismatales, nuclear data strongly place Tofieldiaceae, rather than Araceae, as sister to all the other families, providing an alternative resolution of what has been the most problematic node to resolve using plastid data, outside of those involving achlorophyllous mycoheterotrophs. As seen in numerous prior studies, the placement of orders Acorales and Alismatales as successive sister lineages to all other extant monocots. Only 21.2% of BUSCO genes were demonstrably single-copy, yet phylogenomic inferences based on BUSCO and CSC genes did not differ, and overall functional annotations of the two sets were very similar. Our analyses also reveal significant gene tree-species tree discordance despite high support values, as expected given incomplete lineage sorting (ILS) related to rapid diversification. Our study advances understanding of monocot relationships and the robustness of phylogenetic inferences based on large numbers of nuclear single-copy genes that can be obtained from transcriptomes and genomes. Frontiers Media S.A. 2022-11-22 /pmc/articles/PMC9723157/ /pubmed/36483967 http://dx.doi.org/10.3389/fpls.2022.876779 Text en Copyright © 2022 Timilsena, Wafula, Barrett, Ayyampalayam, McNeal, Rentsch, McKain, Heyduk, Harkess, Villegente, Conran, Illing, Fogliani, Ané, Pires, Davis, Zomlefer, Stevenson, Graham, Givnish, Leebens-Mack and dePamphilis 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
Timilsena, Prakash Raj
Wafula, Eric K.
Barrett, Craig F.
Ayyampalayam, Saravanaraj
McNeal, Joel R.
Rentsch, Jeremy D.
McKain, Michael R.
Heyduk, Karolina
Harkess, Alex
Villegente, Matthieu
Conran, John G.
Illing, Nicola
Fogliani, Bruno
Ané, Cécile
Pires, J. Chris
Davis, Jerrold I.
Zomlefer, Wendy B.
Stevenson, Dennis W.
Graham, Sean W.
Givnish, Thomas J.
Leebens-Mack, James
dePamphilis, Claude W.
Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title_full Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title_fullStr Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title_full_unstemmed Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title_short Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes
title_sort phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 busco genes
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9723157/
https://www.ncbi.nlm.nih.gov/pubmed/36483967
http://dx.doi.org/10.3389/fpls.2022.876779
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