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...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-11-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.876779/full |
| _version_ | 1828122155511971840 |
|---|---|
| author | Prakash Raj Timilsena Eric K. Wafula Craig F. Barrett Saravanaraj Ayyampalayam Saravanaraj Ayyampalayam Joel R. McNeal Jeremy D. Rentsch Michael R. McKain Karolina Heyduk Alex Harkess Matthieu Villegente John G. Conran Nicola Illing Bruno Fogliani Cécile Ané Cécile Ané J. Chris Pires Jerrold I. Davis Wendy B. Zomlefer Dennis W. Stevenson Sean W. Graham Thomas J. Givnish James Leebens-Mack Claude W. dePamphilis |
| author_facet | Prakash Raj Timilsena Eric K. Wafula Craig F. Barrett Saravanaraj Ayyampalayam Saravanaraj Ayyampalayam Joel R. McNeal Jeremy D. Rentsch Michael R. McKain Karolina Heyduk Alex Harkess Matthieu Villegente John G. Conran Nicola Illing Bruno Fogliani Cécile Ané Cécile Ané J. Chris Pires Jerrold I. Davis Wendy B. Zomlefer Dennis W. Stevenson Sean W. Graham Thomas J. Givnish James Leebens-Mack Claude W. dePamphilis |
| author_sort | Prakash Raj Timilsena |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T14:30:39Z |
| format | Article |
| id | doaj.art-251682fdada7476dab1f51d9b098173d |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-11T14:30:39Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-251682fdada7476dab1f51d9b098173d2022-12-22T04:18:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.876779876779Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genesPrakash Raj Timilsena0Eric K. Wafula1Craig F. Barrett2Saravanaraj Ayyampalayam3Saravanaraj Ayyampalayam4Joel R. McNeal5Jeremy D. Rentsch6Michael R. McKain7Karolina Heyduk8Alex Harkess9Matthieu Villegente10John G. Conran11Nicola Illing12Bruno Fogliani13Cécile Ané14Cécile Ané15J. Chris Pires16Jerrold I. Davis17Wendy B. Zomlefer18Dennis W. Stevenson19Sean W. Graham20Thomas J. Givnish21James Leebens-Mack22Claude W. dePamphilis23Department of Biology and Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, United StatesDepartment of Biology and Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, United StatesDepartment of Biology, West Virginia University, Morgantown, WV, United StatesGeorgia Advanced Computing Resource Center, University of Georgia, Athens, GA, United StatesDepartment of Plant Biology, University of Georgia, Athens, GA, United StatesDepartment of Ecology, Evolution, and Organismal Biology, Biology Kennesaw State University, Kennesaw, GA, United StatesDepartment of Biology, Francis Marion University, Florence, SC, United StatesDepartment of Biological Sciences, University of Alabama, Tuscaloosa, AL, United StatesSchool of Life Sciences, University of Hawai’i at Mānoa, Honolulu, HI, United StatesHudsonAlpha Institute for Biotechnology, Huntsville, AL, United States0Institut des Sciences Exactes et Appliquees (ISEA), University of New Caledonia, Noumea, New Caledonia1Australian Centre for Evolutionary Biology and Biodiversity & Sprigg Geobiology Centre, School of Biological Sciences, University of Adelaide, Adelaide, SA, Australia2Department of Molecular and Cell Biology, University of Cape Town, Cape Town, South Africa0Institut des Sciences Exactes et Appliquees (ISEA), University of New Caledonia, Noumea, New Caledonia3Department of Botany, University of Wisconsin-Madison, Madison, WI, United States4Department of Statistics, University of Wisconsin–Madison, Madison, WI, United States5Division of Biological Sciences and Bond Life Sciences Center, University of Missouri, Columbia, MO, United States6School of Integrative Plant Sciences and L.H. Bailey Hortorium, Cornell University, Ithaca, NY, United StatesDepartment of Plant Biology, University of Georgia, Athens, GA, United States7Department of Botany, University of British Columbia, Vancouver, BC, Canada8New York Botanical Garden, New York, NY, United States3Department of Botany, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Plant Biology, University of Georgia, Athens, GA, United StatesDepartment of Biology and Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA, United StatesWe 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.876779/fullphylogenomicsphylotranscriptomicsmonocotsconserved single-copy genesBUSCOconcordance analysis |
| spellingShingle | Prakash Raj Timilsena Eric K. Wafula Craig F. Barrett Saravanaraj Ayyampalayam Saravanaraj Ayyampalayam Joel R. McNeal Jeremy D. Rentsch Michael R. McKain Karolina Heyduk Alex Harkess Matthieu Villegente John G. Conran Nicola Illing Bruno Fogliani Cécile Ané Cécile Ané J. Chris Pires Jerrold I. Davis Wendy B. Zomlefer Dennis W. Stevenson Sean W. Graham Thomas J. Givnish James Leebens-Mack Claude W. dePamphilis Phylogenomic resolution of order- and family-level monocot relationships using 602 single-copy nuclear genes and 1375 BUSCO genes Frontiers in Plant Science phylogenomics phylotranscriptomics monocots conserved single-copy genes BUSCO concordance analysis |
| 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 | phylogenomics phylotranscriptomics monocots conserved single-copy genes BUSCO concordance analysis |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.876779/full |
| work_keys_str_mv | AT prakashrajtimilsena phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT erickwafula phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT craigfbarrett phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT saravanarajayyampalayam phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT saravanarajayyampalayam phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT joelrmcneal phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT jeremydrentsch phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT michaelrmckain phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT karolinaheyduk phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT alexharkess phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT matthieuvillegente phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT johngconran phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT nicolailling phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT brunofogliani phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT cecileane phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT cecileane phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT jchrispires phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT jerroldidavis phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT wendybzomlefer phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT denniswstevenson phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT seanwgraham phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT thomasjgivnish phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT jamesleebensmack phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes AT claudewdepamphilis phylogenomicresolutionoforderandfamilylevelmonocotrelationshipsusing602singlecopynucleargenesand1375buscogenes |