Positive selection and heat-response transcriptomes reveal adaptive features of the Brassicaceae desert model, Anastatica hierochuntica.

Anastatica hierochuntica Brassicaceae adaptation desert species extremophyte heat stress positive selection transcriptome

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
11 2022
Historique:
received: 21 04 2022
accepted: 18 07 2022
pubmed: 2 8 2022
medline: 12 10 2022
entrez: 1 8 2022
Statut: ppublish

Résumé

Plant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat-tolerant Brassicaceae species Anastatica hierochuntica is an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts. We generated an A. hierochuntica reference transcriptome and identified extremophyte adaptations by comparing Arabidopsis thaliana and A. hierochuntica transcriptome responses to heat, and detecting positively selected genes in A. hierochuntica. The two species exhibit similar transcriptome adjustment in response to heat and the A. hierochuntica transcriptome does not exist in a constitutive heat 'stress-ready' state. Furthermore, the A. hierochuntica global transcriptome as well as heat-responsive orthologs, display a lower basal and higher heat-induced expression than in A. thaliana. Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV-B induced DNA repair while those unique to A. hierochuntica are consistent with its photoperiod-insensitive, early-flowering phenotype. We suggest that evolution of a flexible transcriptome confers the ability to quickly react to extreme diurnal temperature fluctuations characteristic of a desert environment while positive selection of genes involved in stress tolerance and early flowering could facilitate an opportunistic desert lifestyle.

Identifiants

pubmed: 35909295
doi: 10.1111/nph.18411
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1006-1026

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/R019894/1
Pays : United Kingdom

Informations de copyright

© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

Références

BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Ann Bot. 2013 Nov;112(7):1209-21
pubmed: 24085482
Plant Physiol. 2002 Nov;130(3):1143-51
pubmed: 12427981
Hortic Res. 2015 Nov 11;2:15051
pubmed: 26623076
New Phytol. 2021 Jun;230(5):1985-2000
pubmed: 33629348
Plant Cell Environ. 2017 Oct;40(10):2347-2358
pubmed: 28741704
New Phytol. 2021 Jul;231(2):571-585
pubmed: 33818773
Annu Rev Plant Biol. 2010;61:517-34
pubmed: 20192749
Genome Biol. 2012;13(3):241
pubmed: 22390828
Planta. 2009 Dec;231(1):27-34
pubmed: 19809832
Annu Rev Plant Biol. 2010;61:443-62
pubmed: 20192746
Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13329-34
pubmed: 21788519
Plant J. 2020 Jan;101(2):310-323
pubmed: 31536657
Plant J. 2005 Dec;44(5):826-39
pubmed: 16297073
Plant Physiol. 2018 Apr;176(4):2737-2749
pubmed: 29440562
Autophagy. 2008 Jan;4(1):20-7
pubmed: 17932459
Mol Biol Evol. 2001 Aug;18(8):1585-92
pubmed: 11470850
BMC Plant Biol. 2014 Jan 04;14:2
pubmed: 24387666
Plant J. 2015 Mar;81(5):767-80
pubmed: 25619405
Plant Cell Environ. 2014 Sep;37(9):2128-38
pubmed: 24548003
New Phytol. 2015 Aug;207(3):627-44
pubmed: 25944243
Plant J. 2017 Jul;91(1):3-21
pubmed: 28370611
New Phytol. 2015 Apr;206(2):557-70
pubmed: 25495078
Proc Natl Acad Sci U S A. 1997 Jan 7;94(1):328-32
pubmed: 8990208
New Phytol. 2014 Feb;201(3):862-873
pubmed: 24164092
Plant Cell Environ. 2009 Apr;32(4):336-48
pubmed: 19143989
Plant Cell. 2017 Feb;29(2):277-291
pubmed: 28188267
BMC Bioinformatics. 2013 Nov 19;14:330
pubmed: 24252138
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Plant Physiol. 2007 Apr;143(4):1789-801
pubmed: 17322336
Plant Mol Biol. 2007 Jan;63(2):171-84
pubmed: 16972165
J Vis Exp. 2019 Jan 7;(143):
pubmed: 30663666
BMC Plant Biol. 2012 Oct 01;12:175
pubmed: 23025749
Proc Natl Acad Sci U S A. 2012 Feb 28;109(9):3582-7
pubmed: 22334645
Planta. 2015 Aug;242(2):407-26
pubmed: 25998524
Cell Rep. 2019 Dec 17;29(12):4186-4199.e3
pubmed: 31851942
New Phytol. 2011 Jun;190(4):1032-1044
pubmed: 21323928
Genome Biol. 2014;15(12):550
pubmed: 25516281
Curr Opin Plant Biol. 2011 Feb;14(1):38-44
pubmed: 20884277
Mol Plant. 2011 Jul;4(4):748-58
pubmed: 21596687
Mol Cells. 2011 May;31(5):447-54
pubmed: 21399993
Elife. 2016 Apr 04;5:e13568
pubmed: 27043937
Physiol Plant. 2014 Aug;151(4):544-58
pubmed: 24372077
Proc Natl Acad Sci U S A. 2014 Jul 15;111(28):10371-6
pubmed: 24958886
Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7441-5
pubmed: 9750104
Plant Cell. 2004 Nov;16(11):2940-53
pubmed: 15472079
Plant Physiol. 2010 Feb;152(2):821-36
pubmed: 20007451
Int J Mol Sci. 2020 Jan 29;21(3):
pubmed: 32013254
Mol Biol Evol. 2014 Aug;31(8):2094-107
pubmed: 24803640
Trends Plant Sci. 2011 Feb;16(2):108-16
pubmed: 21177137
Plant Physiol. 2005 Oct;139(2):909-19
pubmed: 16183838
Gene. 2009 Jul 15;441(1-2):36-44
pubmed: 18640249
Plant Physiol Biochem. 2013 Dec;73:405-11
pubmed: 24220572
Development. 2006 Nov;133(21):4163-72
pubmed: 17021044
Plant Cell. 2020 Feb;32(2):295-318
pubmed: 31776234
Plant Cell Environ. 2016 Aug;39(8):1818-34
pubmed: 27038434
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Plant Physiol. 2018 Jan;176(1):790-803
pubmed: 29133369
Nat Commun. 2016 Dec 01;7:13522
pubmed: 27905394
Plant Physiol. 2017 May;174(1):421-434
pubmed: 28314795
Ann Bot. 2009 Feb;103(4):551-60
pubmed: 18662937
Annu Rev Cell Dev Biol. 2004;20:125-51
pubmed: 15473837
Plant Physiol. 2014 Sep;166(1):370-83
pubmed: 25049361
Plant Physiol. 2013 Jul;162(3):1583-98
pubmed: 23735509
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4392-7
pubmed: 10760305
Plant Physiol. 2013 Jun;162(2):1164-77
pubmed: 23596192
Plant Physiol. 2013 Jun;162(2):831-41
pubmed: 23616603
Sci Signal. 2013 Jun 18;6(280):ra48
pubmed: 23779086
Plant Physiol. 2009 Feb;149(2):1154-65
pubmed: 19052149
Sci Signal. 2011 May 10;4(172):ra29
pubmed: 21558554
Mol Ecol. 2010 Oct;19(19):4144-54
pubmed: 20831645
Plant Physiol. 2018 Nov;178(3):972-988
pubmed: 30237204
Plant Cell. 2007 Aug;19(8):2403-16
pubmed: 17704213
Plant Physiol. 1991 Feb;95(2):628-35
pubmed: 16668029
J Plant Res. 2012 May;125(3):429-38
pubmed: 21938515
Nat Plants. 2018 Oct;4(10):824-835
pubmed: 30250277
Proc Natl Acad Sci U S A. 2021 Nov 16;118(46):
pubmed: 34725254
J Exp Bot. 2015 Jun;66(12):3599-609
pubmed: 25750425
Nat Commun. 2021 Jul 12;12(1):4247
pubmed: 34253727
Plant Cell. 1997 Feb;9(2):199-207
pubmed: 9061951
Biol Open. 2014 Aug 01;3(9):794-802
pubmed: 25086063
Front Plant Sci. 2017 Aug 29;8:1488
pubmed: 28900436
Development. 2001 Dec;128(23):4847-58
pubmed: 11731464
Plant Cell Environ. 2021 Jul;44(7):2018-2033
pubmed: 33314270
Plant Physiol. 2014 Apr;164(4):2123-38
pubmed: 24563282
Mol Biol Evol. 2020 Jul 1;37(7):2052-2068
pubmed: 32167553
Genetics. 2004 Jun;167(2):919-29
pubmed: 15238540
Front Plant Sci. 2017 Jan 17;7:1992
pubmed: 28144244
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
J Exp Bot. 2009;60(12):3367-77
pubmed: 19502535
Nat Commun. 2021 Jun 7;12(1):3376
pubmed: 34099660
BMC Plant Biol. 2018 Apr 23;18(1):68
pubmed: 29685101
Plant Mol Biol. 2002 Sep;50(2):249-59
pubmed: 12175017
R Soc Open Sci. 2018 Jan 17;5(1):171198
pubmed: 29410831
BMC Plant Biol. 2016 Nov 14;16(1):252
pubmed: 27842501
Funct Integr Genomics. 2010 Nov;10(4):523-32
pubmed: 20107865
Comput Appl Biosci. 1997 Oct;13(5):555-6
pubmed: 9367129
BMC Bioinformatics. 2020 Apr 10;21(1):139
pubmed: 32272889
BMC Bioinformatics. 2019 Mar 29;20(1):163
pubmed: 30925894
Nature. 2016 Jan 7;529(7584):84-7
pubmed: 26738594
Mol Plant. 2009 Jan;2(1):3-12
pubmed: 19529830
Chem Rev. 2006 Feb;106(2):753-66
pubmed: 16464023
BMC Plant Biol. 2014 Feb 24;14:54
pubmed: 24564815
Nature. 2008 May 15;453(7193):391-5
pubmed: 18425111
Biochem Biophys Res Commun. 2011 Oct 14;414(1):96-100
pubmed: 21945443
PLoS One. 2015 Jun 30;10(6):e0130430
pubmed: 26125619
BMC Bioinformatics. 2008 Dec 29;9:559
pubmed: 19114008
J Exp Bot. 2012 Jan;63(1):503-15
pubmed: 21963612
Sci Signal. 2011 May 10;4(172):pe25
pubmed: 21558552
Plant Cell. 2017 Nov;29(11):2854-2870
pubmed: 29061866
Plant Physiol. 2022 Dec 09;:
pubmed: 36493387
Cell. 2001 Jan 12;104(1):131-42
pubmed: 11163246
EMBO J. 2009 Nov 4;28(21):3428-38
pubmed: 19763086
New Phytol. 2020 Jan;225(1):21-25
pubmed: 31454419
New Phytol. 2022 May;234(4):1161-1167
pubmed: 35278228
Front Plant Sci. 2018 Jul 04;9:950
pubmed: 30022993
Funct Plant Biol. 2016 Jul;43(7):575-589
pubmed: 32480488
Plant Cell Environ. 2006 Dec;29(12):2216-27
pubmed: 17081254
Plant Cell. 2015 Mar;27(3):908-25
pubmed: 25700484
Oecologia. 1981 Jan;51(3):400-403
pubmed: 28310026
Front Plant Sci. 2013 Jun 11;4:189
pubmed: 23781226
Plant Cell Physiol. 2014 Jan;55(1):e3
pubmed: 24259684
Plant Physiol. 2009 Sep;151(1):290-305
pubmed: 19625635
BMC Syst Biol. 2010 Aug 12;4:111
pubmed: 20704717
AoB Plants. 2019 Nov 27;11(6):plz076
pubmed: 31832127
Plant Cell Physiol. 2003 Jun;44(6):555-64
pubmed: 12826620
Annu Rev Biochem. 1986;55:1151-91
pubmed: 2427013
Plant Physiol. 2020 Apr;182(4):1979-1990
pubmed: 31980572
Ann Bot. 2015 Feb;115(3):419-31
pubmed: 25466549
Nat Rev Genet. 2015 May;16(5):285-98
pubmed: 25854181
Plant Cell. 2019 Sep;31(9):2152-2168
pubmed: 31221737
Plant Cell Environ. 2021 Jul;44(7):2200-2210
pubmed: 33866576
New Phytol. 2021 May;230(3):1034-1048
pubmed: 33496342
Nucleic Acids Res. 2010 Jul;38(Web Server issue):W64-70
pubmed: 20435677
Nat Commun. 2019 Aug 27;10(1):3871
pubmed: 31455787
Plant Cell. 2011 May;23(5):1876-88
pubmed: 21558544
Plant Physiol. 2010 Jul;153(3):1074-84
pubmed: 20463090
Plant J. 2014 Oct;80(1):122-35
pubmed: 25060324

Auteurs

Gil Eshel (G)

Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Nick Duppen (N)

Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Guannan Wang (G)

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.

Dong-Ha Oh (DH)

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.

Yana Kazachkova (Y)

Albert Katz International School for Desert Studies, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Pawel Herzyk (P)

Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK.

Anna Amtmann (A)

Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK.

Michal Gordon (M)

Bioinformatics Core Facility, The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 8410501, Israel.

Vered Chalifa-Caspi (V)

Bioinformatics Core Facility, The National Institute for Biotechnology in the Negev, Ben-Gurion University of the Negev, Beer-Sheva, 8410501, Israel.

Michelle Arland Oscar (MA)

Blaustein Center for Scientific Cooperation, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Shirli Bar-David (S)

Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Amy Marshall-Colon (A)

Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA.

Maheshi Dassanayake (M)

Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.

Simon Barak (S)

French Associates' Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sde Boqer Campus, Midreshet Ben-Gurion, 8499000, Israel.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis

Classifications MeSH