A transcriptome-based study on the phylogeny and evolution of the taxonomically controversial subfamily Apioideae (Apiaceae).

Apioideae coalescent-based method evolutionary history fruit phylogeny single copy genes species tree transcriptome

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
13 05 2020
Historique:
received: 06 06 2019
accepted: 28 01 2020
pubmed: 6 2 2020
medline: 14 7 2020
entrez: 5 2 2020
Statut: ppublish

Résumé

A long-standing controversy in the subfamily Apioideae concerns relationships among the major lineages, which has prevented a comprehensive study of their fruits and evolutionary history. Here we use single copy genes (SCGs) generated from transcriptome datasets to generate a reliable species tree and explore the evolutionary history of Apioideae. In total, 3351 SCGs were generated from 27 transcriptome datasets and one genome, and further used for phylogenetic analysis using coalescent-based methods. Fruit morphology and anatomy were studied in combination with the species tree. Eleven SCGs were screened out for dating analysis with two fossils selected for calibration. A well-supported species tree was generated with a topology [Chamaesieae, (Bupleureae, (Pleurospermeae, (Physospermopsis Clade, (Group C, (Group A, Group B)))))] that differed from previous trees. Daucinae and Torilidinae were not in the tribe Scandiceae and existed as sister groups to the Acronema Clade. Five branches (I-V) of the species tree showed low quartet support but strong local posterior probabilities. Dating analysis suggested that Apioideae originated around 56.64 Mya (95 % highest posterior density interval, 45.18-73.53 Mya). This study resolves a controversial phylogenetic relationship in Apioideae based on 3351 SCGs and coalescent-based species tree estimation methods. Gene trees that contributed to the species tree may undergoing rapid evolutionary divergence and incomplete lineage sorting. Fruits of Apioideae might have evolved in two directions, anemochorous and hydrochorous, with epizoochorous as a derived mode. Molecular and morphological evidence suggests that Daucinae and Torilidinae should be restored to the tribe level. Our results provide new insights into the morphological evolution of this subfamily, which may contribute to a better understanding of species diversification in Apioideae. Molecular dating analysis suggests that uplift of the Qinghai-Tibetan Plateau (QTP) and climate changes probably drove rapid speciation and diversification of Apioideae in the QTP region.

Sections du résumé

BACKGROUND AND AIMS
A long-standing controversy in the subfamily Apioideae concerns relationships among the major lineages, which has prevented a comprehensive study of their fruits and evolutionary history. Here we use single copy genes (SCGs) generated from transcriptome datasets to generate a reliable species tree and explore the evolutionary history of Apioideae.
METHODS
In total, 3351 SCGs were generated from 27 transcriptome datasets and one genome, and further used for phylogenetic analysis using coalescent-based methods. Fruit morphology and anatomy were studied in combination with the species tree. Eleven SCGs were screened out for dating analysis with two fossils selected for calibration.
KEY RESULTS
A well-supported species tree was generated with a topology [Chamaesieae, (Bupleureae, (Pleurospermeae, (Physospermopsis Clade, (Group C, (Group A, Group B)))))] that differed from previous trees. Daucinae and Torilidinae were not in the tribe Scandiceae and existed as sister groups to the Acronema Clade. Five branches (I-V) of the species tree showed low quartet support but strong local posterior probabilities. Dating analysis suggested that Apioideae originated around 56.64 Mya (95 % highest posterior density interval, 45.18-73.53 Mya).
CONCLUSIONS
This study resolves a controversial phylogenetic relationship in Apioideae based on 3351 SCGs and coalescent-based species tree estimation methods. Gene trees that contributed to the species tree may undergoing rapid evolutionary divergence and incomplete lineage sorting. Fruits of Apioideae might have evolved in two directions, anemochorous and hydrochorous, with epizoochorous as a derived mode. Molecular and morphological evidence suggests that Daucinae and Torilidinae should be restored to the tribe level. Our results provide new insights into the morphological evolution of this subfamily, which may contribute to a better understanding of species diversification in Apioideae. Molecular dating analysis suggests that uplift of the Qinghai-Tibetan Plateau (QTP) and climate changes probably drove rapid speciation and diversification of Apioideae in the QTP region.

Identifiants

pubmed: 32016402
pii: 5722139
doi: 10.1093/aob/mcaa011
pmc: PMC7218814
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

937-953

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Références

Trends Plant Sci. 2013 Sep;18(9):492-5
pubmed: 23707196
Biol Rev Camb Philos Soc. 2015 Feb;90(1):236-53
pubmed: 24784793
Proc Natl Acad Sci U S A. 2012 May 15;109(20):7659-64
pubmed: 22547792
Nucleic Acids Res. 2013 Jul;41(Web Server issue):W238-41
pubmed: 23661681
Mol Biol Evol. 2020 Feb 1;37(2):604-606
pubmed: 31670774
Mol Biol Evol. 2010 Mar;27(3):570-80
pubmed: 19906793
PLoS Genet. 2006 May;2(5):e68
pubmed: 16733550
Am J Bot. 1998 Apr;85(4):563
pubmed: 21684940
Science. 2005 Sep 30;309(5744):2207-9
pubmed: 16195459
Mol Phylogenet Evol. 2017 Mar;108:1-21
pubmed: 28179182
Nature. 2003 Oct 23;425(6960):798-804
pubmed: 14574403
New Phytol. 2009;182(1):272-83
pubmed: 19192190
Ann Bot. 2019 Jan 1;123(1):221
pubmed: 30184163
Nat Genet. 2016 Jun;48(6):657-66
pubmed: 27158781
Nature. 2019 Oct;574(7780):679-685
pubmed: 31645766
Nature. 2008 Apr 10;452(7188):745-9
pubmed: 18322464
Mol Ecol Resour. 2016 Sep;16(5):1107-23
pubmed: 27289081
Evolution. 1994 Dec;48(6):1959-1972
pubmed: 28565156
Bioinformatics. 2014 Sep 1;30(17):i541-8
pubmed: 25161245
Syst Biol. 2016 Jul;65(4):726-36
pubmed: 27235697
Trends Ecol Evol. 1996 Aug;11(8):334
pubmed: 21237865
BMC Genomics. 2014 Jun 21;15:504
pubmed: 24950957
Nature. 2012 Mar 07;483(7388):169-75
pubmed: 22398555
Bioinformatics. 2015 Jun 15;31(12):i44-52
pubmed: 26072508
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Syst Biol. 2017 Sep 1;66(5):823-842
pubmed: 28053140
Syst Biol. 2004 Jun;53(3):496-505
pubmed: 15503676
Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):14942-7
pubmed: 22930817
Syst Biol. 2008 Feb;57(1):38-57
pubmed: 18275001
Mol Biol Evol. 2017 Feb 1;34(2):262-281
pubmed: 27856652
Syst Biol. 2007 Feb;56(1):17-24
pubmed: 17366134
BMC Evol Biol. 2010 Oct 11;10:302
pubmed: 20937096
Theor Popul Biol. 2014 Dec 26;100C:56-62
pubmed: 25545843
Am J Bot. 1999 Jul;86(7):1014-26
pubmed: 10406725
Genetics. 2006 Nov;174(3):1407-20
pubmed: 16951058
Am J Bot. 2006 Dec;93(12):1828-47
pubmed: 21642128
Syst Biol. 2019 Nov 1;68(6):937-955
pubmed: 31135914
Am J Bot. 2010 Aug;97(8):1296-303
pubmed: 21616882
Mol Biol Evol. 2012 Aug;29(8):1969-73
pubmed: 22367748
Trends Ecol Evol. 2009 Jun;24(6):332-40
pubmed: 19307040
Syst Biol. 2009 Oct;58(5):468-77
pubmed: 20525601
Proc Natl Acad Sci U S A. 2007 Apr 3;104(14):5936-41
pubmed: 17392434
Am J Bot. 1997 Apr;84(4):565
pubmed: 21708608
Syst Biol. 2020 Jan 1;69(1):38-60
pubmed: 31062850
Trends Ecol Evol. 2007 Jan;22(1):34-41
pubmed: 17046100
Mol Phylogenet Evol. 2015 Jun;87:14-27
pubmed: 25804934
Am J Bot. 2008 Feb;95(2):196-214
pubmed: 21632345
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
Mol Biol Evol. 2016 Jul;33(7):1654-68
pubmed: 27189547
Curr Protoc Bioinformatics. 2011 Sep;Chapter 6:Unit 6.12.1-19
pubmed: 21901743
Mol Biol Evol. 2014 Dec;31(12):3125-35
pubmed: 25274273
Bioinformatics. 1998;14(9):817-8
pubmed: 9918953
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
Nat Commun. 2014 Sep 24;5:4956
pubmed: 25249442
Mol Biol Evol. 2018 Oct 1;35(10):2585-2593
pubmed: 30053098
Am J Bot. 2000 Feb;87(2):273-92
pubmed: 10675315
Mol Phylogenet Evol. 2009 Oct;53(1):56-68
pubmed: 19501179
Evolution. 1994 Jun;48(3):791-805
pubmed: 28568276
Proc Natl Acad Sci U S A. 2013 Feb 19;110(8):2898-903
pubmed: 23382190
Syst Biol. 2011 Oct;60(5):661-7
pubmed: 21447481
Mol Phylogenet Evol. 1996 Aug;6(1):1-18
pubmed: 8812301
BMC Evol Biol. 2010 Feb 24;10:61
pubmed: 20181251

Auteurs

Jun Wen (J)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.
Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, P.R. China.

Yan Yu (Y)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.

Deng-Feng Xie (DF)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.

Chang Peng (C)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.

Qing Liu (Q)

Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, P.R. China.

Song-Dong Zhou (SD)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.

Xing-Jin He (XJ)

Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu, Sichuan, P.R. China.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family

Classifications MeSH