Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae)
The bamboos (Bambusoideae, Poaceae) comprise a major grass lineage with a complex evolutionary history involving ancient hybridization and allopolyploidy. About 1700 described species are classified into three tribes, Olyreae (herbaceous bamboos), Bambuseae (tropical woody bamboos), and Arundinariea...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-09-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.725728/full |
| _version_ | 1818729993380823040 |
|---|---|
| author | Domitille Chalopin Lynn G. Clark William P. Wysocki Minkyu Park Melvin R. Duvall Jeffrey L. Bennetzen |
| author_facet | Domitille Chalopin Lynn G. Clark William P. Wysocki Minkyu Park Melvin R. Duvall Jeffrey L. Bennetzen |
| author_sort | Domitille Chalopin |
| collection | DOAJ |
| description | The bamboos (Bambusoideae, Poaceae) comprise a major grass lineage with a complex evolutionary history involving ancient hybridization and allopolyploidy. About 1700 described species are classified into three tribes, Olyreae (herbaceous bamboos), Bambuseae (tropical woody bamboos), and Arundinarieae (temperate woody bamboos). Nuclear analyses strongly support monophyly of the woody tribes, whereas plastome analyses strongly support paraphyly, with Bambuseae sister to Olyreae. Our objectives were to clarify the origin(s) of the woody bamboo tribes and resolve the nuclear vs. plastid conflict using genomic tools. For the first time, plastid and nuclear genomic information from the same bamboo species were combined in a single study. We sampled 51 species of bamboos representing the three tribes, estimated their genome sizes and generated low-depth sample sequence data, from which plastomes were assembled and nuclear repeats were analyzed. The distribution of repeat families was found to agree with nuclear gene phylogenies, but also provides novel insights into nuclear evolutionary history. We infer two early, independent hybridization events, one between an Olyreae ancestor and a woody ancestor giving rise to the two Bambuseae lineages, and another between two woody ancestors giving rise to the Arundinarieae. Retention of the Olyreae plastome associated with differential dominance of nuclear genomes and subsequent diploidization in some lineages explains the paraphyly observed in plastome phylogenetic estimations. We confirm ancient hybridization and allopolyploidy in the origins of the extant woody bamboo lineages and propose biased fractionation and diploidization as important factors in their evolution. |
| first_indexed | 2024-12-17T22:54:43Z |
| format | Article |
| id | doaj.art-3b43b91fa7d74e95a8450c737aba6228 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-17T22:54:43Z |
| publishDate | 2021-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-3b43b91fa7d74e95a8450c737aba62282022-12-21T21:29:34ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.725728725728Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae)Domitille Chalopin0Lynn G. Clark1William P. Wysocki2Minkyu Park3Melvin R. Duvall4Jeffrey L. Bennetzen5Department of Genetics, University of Georgia, Athens, GA, United StatesDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, United StatesCenter for Translational Data Science, University of Chicago, Chicago, IL, United StatesDepartment of Genetics, University of Georgia, Athens, GA, United StatesDepartment of Biology and Institute for the Study of the Environment, Sustainability, and Energy, Northern Illinois University, DeKalb, IL, United StatesDepartment of Genetics, University of Georgia, Athens, GA, United StatesThe bamboos (Bambusoideae, Poaceae) comprise a major grass lineage with a complex evolutionary history involving ancient hybridization and allopolyploidy. About 1700 described species are classified into three tribes, Olyreae (herbaceous bamboos), Bambuseae (tropical woody bamboos), and Arundinarieae (temperate woody bamboos). Nuclear analyses strongly support monophyly of the woody tribes, whereas plastome analyses strongly support paraphyly, with Bambuseae sister to Olyreae. Our objectives were to clarify the origin(s) of the woody bamboo tribes and resolve the nuclear vs. plastid conflict using genomic tools. For the first time, plastid and nuclear genomic information from the same bamboo species were combined in a single study. We sampled 51 species of bamboos representing the three tribes, estimated their genome sizes and generated low-depth sample sequence data, from which plastomes were assembled and nuclear repeats were analyzed. The distribution of repeat families was found to agree with nuclear gene phylogenies, but also provides novel insights into nuclear evolutionary history. We infer two early, independent hybridization events, one between an Olyreae ancestor and a woody ancestor giving rise to the two Bambuseae lineages, and another between two woody ancestors giving rise to the Arundinarieae. Retention of the Olyreae plastome associated with differential dominance of nuclear genomes and subsequent diploidization in some lineages explains the paraphyly observed in plastome phylogenetic estimations. We confirm ancient hybridization and allopolyploidy in the origins of the extant woody bamboo lineages and propose biased fractionation and diploidization as important factors in their evolution.https://www.frontiersin.org/articles/10.3389/fpls.2021.725728/fullArundinarieaeBambuseaebiased fractionationdiploidizationgenome dominancemobilome |
| spellingShingle | Domitille Chalopin Lynn G. Clark William P. Wysocki Minkyu Park Melvin R. Duvall Jeffrey L. Bennetzen Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) Frontiers in Plant Science Arundinarieae Bambuseae biased fractionation diploidization genome dominance mobilome |
| title | Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) |
| title_full | Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) |
| title_fullStr | Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) |
| title_full_unstemmed | Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) |
| title_short | Integrated Genomic Analyses From Low-Depth Sequencing Help Resolve Phylogenetic Incongruence in the Bamboos (Poaceae: Bambusoideae) |
| title_sort | integrated genomic analyses from low depth sequencing help resolve phylogenetic incongruence in the bamboos poaceae bambusoideae |
| topic | Arundinarieae Bambuseae biased fractionation diploidization genome dominance mobilome |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.725728/full |
| work_keys_str_mv | AT domitillechalopin integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae AT lynngclark integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae AT williampwysocki integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae AT minkyupark integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae AT melvinrduvall integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae AT jeffreylbennetzen integratedgenomicanalysesfromlowdepthsequencinghelpresolvephylogeneticincongruenceinthebamboospoaceaebambusoideae |