Genetic adaptations in the population history of Arabidopsis thaliana.

Arabidopsis thaliana coadaptation gene expression adaptation phenotypic adaptation population history

Journal

G3 (Bethesda, Md.)
ISSN: 2160-1836
Titre abrégé: G3 (Bethesda)
Pays: England
ID NLM: 101566598

Informations de publication

Date de publication:
06 Dec 2023
Historique:
received: 26 05 2023
accepted: 14 09 2023
medline: 11 12 2023
pubmed: 25 9 2023
entrez: 25 9 2023
Statut: ppublish

Résumé

A population encounters a variety of environmental stresses, so the full source of its resilience can only be captured by collecting all the signatures of adaptation to the selection of the local environment in its population history. Based on the multiomic data of Arabidopsis thaliana, we constructed a database of phenotypic adaptations (p-adaptations) and gene expression (e-adaptations) adaptations in the population. Through the enrichment analysis of the identified adaptations, we inferred a likely scenario of adaptation that is consistent with the biological evidence from experimental work. We analyzed the dynamics of the allele frequencies at the 23,880 QTLs of 174 traits and 8,618 eQTLs of 1,829 genes with respect to the total SNPs in the genomes and identified 650 p-adaptations and 3,925 e-adaptations [false discovery rate (FDR) = 0.05]. The population underwent large-scale p-adaptations and e-adaptations along 4 lineages. Extremely cold winters and short summers prolonged seed dormancy and expanded the root system architecture. Low temperatures prolonged the growing season, and low light intensity required the increased chloroplast activity. The subtropical and humid environment enhanced phytohormone signaling pathways in response to the biotic and abiotic stresses. Exposure to heavy metals selected alleles for lower heavy metal uptake from soil, lower growth rate, lower resistance to bacteria, and higher expression of photosynthetic genes were selected. The p-adaptations are directly interpretable, while the coadapted gene expressions reflect the physiological requirements for the adaptation. The integration of this information characterizes when and where the population has experienced environmental stress and how the population responded at the molecular level.

Identifiants

pubmed: 37748020
pii: 7281879
doi: 10.1093/g3journal/jkad218
pmc: PMC10700115
pii:
doi:

Substances chimiques

Arabidopsis Proteins 0
Soil 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research
ID : 22K11950

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare no conflict of interest.

Références

Plant J. 2018 Oct;96(2):468-481
pubmed: 30030851
Am J Bot. 2020 Nov;107(11):1518-1526
pubmed: 33058187
Mol Ecol. 2005 Jul;14(8):2611-20
pubmed: 15969739
Nat Ecol Evol. 2019 Feb;3(2):274-285
pubmed: 30643246
Genetics. 2018 Apr;208(4):1565-1584
pubmed: 29348143
Biol Methods Protoc. 2021 Sep 16;6(1):bpab017
pubmed: 34595352
Proc Natl Acad Sci U S A. 2004 Sep 7;101(36):13386-90
pubmed: 15326309
Mol Biol Evol. 1999 Feb;16(2):266-74
pubmed: 10028292
Evolution. 2017 Mar;71(3):550-564
pubmed: 27859214
Curr Biol. 2018 May 21;28(10):R619-R634
pubmed: 29787730
Cell. 2016 Jul 14;166(2):481-491
pubmed: 27293186
Ann Bot. 2014 May;113(6):921-9
pubmed: 24573642
New Phytol. 2021 Oct;232(1):208-220
pubmed: 34153129
Trends Plant Sci. 2008 Mar;13(3):145-50
pubmed: 18289920
PLoS Biol. 2015 Apr 10;13(4):e1002112
pubmed: 25859758
Nucleic Acids Res. 2020 Jan 8;48(D1):D1063-D1068
pubmed: 31642487
Science. 2002 Sep 27;297(5590):2253-6
pubmed: 12351787
Nat Ecol Evol. 2018 Feb;2(2):352-358
pubmed: 29255303
Bioinformatics. 2022 May 13;38(10):2952-2953
pubmed: 35561170
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21199-204
pubmed: 21078970
Plant J. 2014 Aug;79(3):466-76
pubmed: 24889055
Plant J. 2013 Jun;74(6):1003-15
pubmed: 23590427
Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):13106-11
pubmed: 19620714
Proc Natl Acad Sci U S A. 2020 Feb 4;117(5):2526-2534
pubmed: 31964817
Plant Cell. 1997 Jul;9(7):1055-1066
pubmed: 12237375
Annu Rev Phytopathol. 2017 Aug 4;55:401-425
pubmed: 28645231
PLoS Genet. 2014 Aug 07;10(8):e1004412
pubmed: 25102153
Nucleic Acids Res. 2011 Jan;39(Database issue):D52-7
pubmed: 21115458
Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5602-7
pubmed: 16565218
Mol Biol Evol. 2019 Jan 1;36(1):141-154
pubmed: 30388255
Trends Plant Sci. 2009 Jul;14(7):373-82
pubmed: 19559643
Planta. 2015 Dec;242(6):1277-90
pubmed: 26189001
Mol Biol Evol. 2021 Dec 9;38(12):5328-5344
pubmed: 34499163
Mol Ecol. 2022 Apr;31(7):2089-2105
pubmed: 35075727
PLoS Genet. 2008 May 16;4(5):e1000075
pubmed: 18483550
FEMS Microbiol Ecol. 2005 Mar 1;52(1):49-58
pubmed: 16329892
Genetics. 2003 Jun;164(2):711-29
pubmed: 12807791
Plant Physiol. 2002 Dec;130(4):2129-41
pubmed: 12481097
Nat Commun. 2017 Feb 09;8:14458
pubmed: 28181519
Nucleic Acids Res. 2023 Jan 6;51(D1):D638-D646
pubmed: 36370105
Nucleic Acids Res. 2021 Jan 8;49(D1):D325-D334
pubmed: 33290552
Genetics. 2002 Dec;162(4):2025-35
pubmed: 12524368
J Exp Bot. 2007;58(12):3091-7
pubmed: 17693414
Trends Ecol Evol. 1995 Jun;10(6):248-52
pubmed: 21237029
PLoS Genet. 2012;8(11):e1002967
pubmed: 23166502
Proc Biol Sci. 2004 Apr 7;271(1540):705-14
pubmed: 15209104
Nucleic Acids Res. 2021 Jan 8;49(D1):D1445-D1451
pubmed: 33219693
Genesis. 2015 Aug;53(8):474-85
pubmed: 26201819
Mol Ecol. 2018 Oct;27(20):4052-4065
pubmed: 30118161
PLoS Biol. 2005 Jul;3(7):e196
pubmed: 15907155
Int J Mol Sci. 2022 Feb 15;23(4):
pubmed: 35216246
Front Microbiol. 2022 Aug 11;13:961794
pubmed: 36033855
Proc Natl Acad Sci U S A. 2020 May 5;117(18):9665-9667
pubmed: 32086393
New Phytol. 2012 Jun;194(4):1112-1122
pubmed: 22432639
Genetics. 2000 Jun;155(2):945-59
pubmed: 10835412
Genome Res. 2009 Sep;19(9):1655-64
pubmed: 19648217

Auteurs

Hirohisa Kishino (H)

Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan.
Research and Development Initiative, Chuo University, 1-13-27 Kasuga, Bunkyo-ku, Tokyo 112-8551, Japan.

Reiichiro Nakamichi (R)

Fisheries Resources Institute, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa-ku, Yokohama, Kanagawa 236-8648, Japan.

Shuichi Kitada (S)

Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Animals Natural Killer T-Cells Mice Adipose Tissue Lipid Metabolism
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis

Classifications MeSH