Evolution of plasticity in production and transgenerational inheritance of small RNAs under dynamic environmental conditions.
Journal
PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074
Informations de publication
Date de publication:
05 2021
05 2021
Historique:
received:
14
08
2020
accepted:
05
05
2021
revised:
08
06
2021
pubmed:
27
5
2021
medline:
23
9
2021
entrez:
26
5
2021
Statut:
epublish
Résumé
In a changing environment, small RNAs (sRNAs) play an important role in the post-transcriptional regulation of gene expression and can vary in abundance depending on the conditions experienced by an individual (phenotypic plasticity) and its parents (non-genetic inheritance). Many sRNAs are unusual in that they can be produced in two ways, either using genomic DNA as the template (primary sRNAs) or existing sRNAs as the template (secondary sRNAs). Thus, organisms can evolve rapid plastic responses to their current environment by adjusting the amplification rate of sRNA templates. sRNA levels can also be transmitted transgenerationally by the direct transfer of either sRNAs or the proteins involved in amplification. Theory is needed to describe the selective forces acting on sRNA levels, accounting for the dual nature of sRNAs as regulatory elements and templates for amplification and for the potential to transmit sRNAs and their amplification agents to offspring. Here, we develop a model to study the dynamics of sRNA production and inheritance in a fluctuating environment. We tested the selective advantage of mutants capable of sRNA-mediated phenotypic plasticity within resident populations with fixed levels of sRNA transcription. Even when the resident was allowed to evolve an optimal constant rate of sRNA production, plastic amplification rates capable of responding to environmental conditions were favored. Mechanisms allowing sRNA transcripts or amplification agents to be inherited were favored primarily when parents and offspring face similar environments and when selection acts before the optimal level of sRNA can be reached within the organism. Our study provides a clear set of testable predictions for the evolution of sRNA-related mechanisms of phenotypic plasticity and transgenerational inheritance.
Identifiants
pubmed: 34038409
doi: 10.1371/journal.pgen.1009581
pii: PGENETICS-D-20-01255
pmc: PMC8186813
doi:
Substances chimiques
RNA
63231-63-0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1009581Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Genetics. 2008 Nov;180(3):1275-88
pubmed: 18757930
Ecol Lett. 2016 Oct;19(10):1267-76
pubmed: 27600658
Genes Dev. 2014 Jul 1;28(13):1410-28
pubmed: 24939875
Trends Biochem Sci. 2012 Oct;37(10):436-46
pubmed: 22921610
Curr Opin Microbiol. 2010 Feb;13(1):18-23
pubmed: 20022798
Trends Genet. 2017 Nov;33(11):882-894
pubmed: 28964526
Cell. 2007 Aug 10;130(3):413-26
pubmed: 17693253
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6516-21
pubmed: 11353867
Mol Metab. 2015 Dec 25;5(3):184-197
pubmed: 26977389
Nat Rev Mol Cell Biol. 2015 Dec;16(12):727-41
pubmed: 26530390
Wiley Interdiscip Rev RNA. 2012 May-Jun;3(3):351-68
pubmed: 22086843
Sci Rep. 2014 Dec 09;4:7387
pubmed: 25552271
Nat Commun. 2016 Dec 21;7:13856
pubmed: 28000665
Cell. 2005 Dec 29;123(7):1279-91
pubmed: 16377568
Microbiol Spectr. 2018 Apr;6(2):
pubmed: 29623872
BMC Genomics. 2017 Jun 26;18(1):481
pubmed: 28651543
FEBS Lett. 2007 Jul 31;581(19):3592-7
pubmed: 17451688
Am Nat. 2015 Mar;185(3):E55-69
pubmed: 25674697
Nat Rev Mol Cell Biol. 2009 Feb;10(2):126-39
pubmed: 19165215
Nat Rev Genet. 2011 Nov 18;12(12):846-60
pubmed: 22094948
Trends Cell Biol. 2014 Apr;24(4):212-20
pubmed: 24231398
RNA. 2017 Sep;23(9):1352-1364
pubmed: 28630141
Elife. 2017 Apr 06;6:
pubmed: 28384097
Science. 2002 May 17;296(5571):1260-3
pubmed: 12016301
PLoS Genet. 2008 Jan;4(1):e22
pubmed: 18225959
Am Nat. 2006 Mar;167(3):367-76
pubmed: 16673345
Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13699-704
pubmed: 26483456
Cell. 2003 Apr 4;113(1):25-36
pubmed: 12679032
Sci Rep. 2016 Oct 18;6:35558
pubmed: 27752116
Cell Rep. 2018 May 22;23(8):2482-2494
pubmed: 29791857
PLoS Comput Biol. 2014 Apr 10;10(4):e1003550
pubmed: 24722346
Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
pubmed: 20980440
Nat Rev Genet. 2014 Jun;15(6):394-408
pubmed: 24805120
RNA Biol. 2018 Mar 4;15(3):308-313
pubmed: 29345184
Cell. 2002 Apr 19;109(2):141-4
pubmed: 12007399
Proc Biol Sci. 2015 Jul 22;282(1811):
pubmed: 26136447
Genetics. 2017 Jul;206(3):1403-1416
pubmed: 28533440
Cell. 2014 Jul 17;158(2):277-287
pubmed: 25018105
Plant Physiol Biochem. 2014 Nov;84:105-114
pubmed: 25261853
Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9272-7
pubmed: 18583475
Nat Rev Genet. 2005 Mar;6(3):206-20
pubmed: 15703763
Compr Physiol. 2012 Apr;2(2):1417-39
pubmed: 23798305
Evolution. 2018 Feb;72(2):220-233
pubmed: 29210448
Nat Rev Genet. 2010 Dec;11(12):855-66
pubmed: 21085204
Biol Cell. 2018 Oct;110(10):217-224
pubmed: 30132958
Science. 2004 Apr 23;304(5670):594-6
pubmed: 15105502
Cell Cycle. 2005 Sep;4(9):1179-84
pubmed: 16096373
Genome Res. 2012 Jul;22(7):1350-9
pubmed: 22466169
Curr Biol. 2003 Apr 29;13(9):790-5
pubmed: 12725740
Front Genet. 2015 May 19;6:179
pubmed: 26042146
Nature. 1973 Nov 9;246(5428):96-8
pubmed: 4585855
Nat Genet. 2006 Jun;38 Suppl:S31-6
pubmed: 16736022
Trends Cell Biol. 2014 Feb;24(2):100-7
pubmed: 24012194
Science. 2004 Jan 2;303(5654):83-6
pubmed: 14657504
Science. 2018 Jun 8;360(6393):1126-1129
pubmed: 29773668
Curr Biol. 2001 Jul 10;11(13):1017-27
pubmed: 11470406
Adv Exp Med Biol. 2016;886:51-77
pubmed: 26659487
Genes Dev. 2014 Aug 1;28(15):1667-80
pubmed: 25085419
J Exp Zool B Mol Dev Evol. 2006 Nov 15;306(6):575-88
pubmed: 16838302
Evolution. 2015 Apr;69(4):950-68
pubmed: 25809121
Cell. 2009 Feb 20;136(4):656-68
pubmed: 19239887
Nat Rev Genet. 2004 Jul;5(7):522-31
pubmed: 15211354
Trends Biochem Sci. 2016 Apr;41(4):324-337
pubmed: 26810602
Nat Rev Genet. 2013 Aug;14(8):523-34
pubmed: 23797853
Curr Opin Microbiol. 2008 Dec;11(6):574-9
pubmed: 18935980
Science. 2006 Jul 21;313(5785):320-4
pubmed: 16809489
Curr Biol. 2017 Jul 24;27(14):R720-R730
pubmed: 28743023
J Biol Chem. 2004 Dec 10;279(50):52361-5
pubmed: 15504739
Trends Genet. 2017 Jan;33(1):46-57
pubmed: 27939252
Mol Cell. 2011 Sep 16;43(6):880-91
pubmed: 21925377
Biol Chem. 2011 Apr;392(4):299-304
pubmed: 21294682
Nat Rev Genet. 2013 Jul;14(7):447-59
pubmed: 23732335
Epigenetics Chromatin. 2016 Jan 15;9:3
pubmed: 26779286
Evol Appl. 2012 Feb;5(2):192-201
pubmed: 25568041
Nature. 2004 Sep 16;431(7006):350-5
pubmed: 15372042
Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18420-4
pubmed: 16339901
Evol Lett. 2020 Jun 10;4(4):371-381
pubmed: 32774885
Science. 2008 Nov 28;322(5906):1387-92
pubmed: 19039138
Science. 2006 Apr 7;312(5770):75-9
pubmed: 16484454
Cell. 2007 Apr 6;129(1):69-82
pubmed: 17418787
Annu Rev Plant Biol. 2009;60:485-510
pubmed: 19519217
Development. 2008 Apr;135(7):1201-14
pubmed: 18287206
PLoS One. 2014 Feb 24;9(2):e89760
pubmed: 24587016
Plant Cell. 2002 Jul;14(7):1605-19
pubmed: 12119378
Annu Rev Cell Dev Biol. 2007;23:175-205
pubmed: 17506695
Genome Biol. 2008;9(2):210
pubmed: 18304383
J Evol Biol. 2016 Feb;29(2):265-76
pubmed: 26492510
Development. 2014 Sep;141(18):3458-71
pubmed: 25183868
Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):7079-82
pubmed: 19357307
Cell. 2011 Dec 9;147(6):1248-56
pubmed: 22119442
J Integr Plant Biol. 2016 Apr;58(4):312-27
pubmed: 26748943
Nat Commun. 2017 May 25;8:15332
pubmed: 28541282
BMC Genomics. 2014 May 19;15:385
pubmed: 24884623
Nat Rev Genet. 2015 Nov;16(11):641-52
pubmed: 26416311