Systemic paralogy and function of retinal determination network homologs in arachnids.
Amblypygi
Cave blindness
Parasteatoda tepidariorum
RNAi
Six1
sine oculis
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
23 Nov 2020
23 Nov 2020
Historique:
received:
11
05
2020
accepted:
13
10
2020
entrez:
23
11
2020
pubmed:
24
11
2020
medline:
15
5
2021
Statut:
epublish
Résumé
Arachnids are important components of cave ecosystems and display many examples of troglomorphisms, such as blindness, depigmentation, and elongate appendages. Little is known about how the eyes of arachnids are specified genetically, let alone the mechanisms for eye reduction and loss in troglomorphic arachnids. Additionally, duplication of Retinal Determination Gene Network (RDGN) homologs in spiders has convoluted functional inferences extrapolated from single-copy homologs in pancrustacean models. We investigated a sister species pair of Israeli cave whip spiders, Charinus ioanniticus and C. israelensis (Arachnopulmonata, Amblypygi), of which one species has reduced eyes. We generated embryonic transcriptomes for both Amblypygi species, and discovered that several RDGN homologs exhibit duplications. We show that duplication of RDGN homologs is systemic across arachnopulmonates (arachnid orders that bear book lungs), rather than being a spider-specific phenomenon. A differential gene expression (DGE) analysis comparing the expression of RDGN genes in field-collected embryos of both species identified candidate RDGN genes involved in the formation and reduction of eyes in whip spiders. To ground bioinformatic inference of expression patterns with functional experiments, we interrogated the function of three candidate RDGN genes identified from DGE using RNAi in the spider Parasteatoda tepidariorum. We provide functional evidence that one of these paralogs, sine oculis/Six1 A (soA), is necessary for the development of all arachnid eye types. Our work establishes a foundation to investigate the genetics of troglomorphic adaptations in cave arachnids, and links differential gene expression to an arthropod eye phenotype for the first time outside of Pancrustacea. Our results support the conservation of at least one RDGN component across Arthropoda and provide a framework for identifying the role of gene duplications in generating arachnid eye diversity.
Sections du résumé
BACKGROUND
BACKGROUND
Arachnids are important components of cave ecosystems and display many examples of troglomorphisms, such as blindness, depigmentation, and elongate appendages. Little is known about how the eyes of arachnids are specified genetically, let alone the mechanisms for eye reduction and loss in troglomorphic arachnids. Additionally, duplication of Retinal Determination Gene Network (RDGN) homologs in spiders has convoluted functional inferences extrapolated from single-copy homologs in pancrustacean models.
RESULTS
RESULTS
We investigated a sister species pair of Israeli cave whip spiders, Charinus ioanniticus and C. israelensis (Arachnopulmonata, Amblypygi), of which one species has reduced eyes. We generated embryonic transcriptomes for both Amblypygi species, and discovered that several RDGN homologs exhibit duplications. We show that duplication of RDGN homologs is systemic across arachnopulmonates (arachnid orders that bear book lungs), rather than being a spider-specific phenomenon. A differential gene expression (DGE) analysis comparing the expression of RDGN genes in field-collected embryos of both species identified candidate RDGN genes involved in the formation and reduction of eyes in whip spiders. To ground bioinformatic inference of expression patterns with functional experiments, we interrogated the function of three candidate RDGN genes identified from DGE using RNAi in the spider Parasteatoda tepidariorum. We provide functional evidence that one of these paralogs, sine oculis/Six1 A (soA), is necessary for the development of all arachnid eye types.
CONCLUSIONS
CONCLUSIONS
Our work establishes a foundation to investigate the genetics of troglomorphic adaptations in cave arachnids, and links differential gene expression to an arthropod eye phenotype for the first time outside of Pancrustacea. Our results support the conservation of at least one RDGN component across Arthropoda and provide a framework for identifying the role of gene duplications in generating arachnid eye diversity.
Identifiants
pubmed: 33225889
doi: 10.1186/s12864-020-07149-x
pii: 10.1186/s12864-020-07149-x
pmc: PMC7681978
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
811Subventions
Organisme : NIGMS NIH HHS
ID : T32 GM135066
Pays : United States
Organisme : National Geographic Society
ID : NGS-271R-18
Organisme : National Science Foundation
ID : IOS-1552610
Références
BMC Evol Biol. 2013 Sep 08;13:186
pubmed: 24010579
Evol Dev. 2012 Jul;14(4):383-92
pubmed: 22765209
PLoS One. 2015 Oct 13;10(10):e0140484
pubmed: 26462237
Proc Natl Acad Sci U S A. 1998 Sep 1;95(18):10671-5
pubmed: 9724762
PLoS One. 2013 Oct 16;8(10):e75989
pubmed: 24146804
Biochim Biophys Acta. 2009 Apr;1789(4):333-42
pubmed: 18976722
Genome Biol Evol. 2016 Jun 03;8(5):1571-89
pubmed: 27189985
Nature. 2018 Mar 29;555(7698):647-651
pubmed: 29562229
Wiley Interdiscip Rev Dev Biol. 2012 Nov-Dec;1(6):823-45
pubmed: 23580903
Mol Biol Evol. 2016 Jan;33(1):109-21
pubmed: 26443673
Proc Biol Sci. 2017 Apr 26;284(1853):
pubmed: 28446696
Dev Biol. 2017 Oct 1;430(1):224-236
pubmed: 28764892
Nat Genet. 2018 Jul;50(7):908-909
pubmed: 29955176
Curr Top Dev Biol. 2009;86:191-221
pubmed: 19361694
Genetics. 2000 Jul;155(3):1281-95
pubmed: 10880488
Biol Bull. 2017 Aug;233(1):21-38
pubmed: 29182503
Curr Top Dev Biol. 2009;89:115-35
pubmed: 19737644
Curr Biol. 2014 May 5;24(9):1017-23
pubmed: 24726154
Front Zool. 2016 Aug 11;13:35
pubmed: 27525029
Science. 2012 Jan 27;335(6067):469-71
pubmed: 22282813
Nat Commun. 2016 Feb 09;7:10507
pubmed: 26856261
Mol Ecol. 2018 Nov;27(22):4397-4416
pubmed: 30252986
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
BMC Evol Biol. 2008 Jul 29;8:222
pubmed: 18664266
Evodevo. 2013 Aug 30;4(1):23
pubmed: 23991696
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Dev Biol. 2017 Dec 1;432(1):192-200
pubmed: 28993201
Nature. 2009 Feb 12;457(7231):818-23
pubmed: 19212399
Proc Biol Sci. 2019 Dec 18;286(1917):20192426
pubmed: 31847768
Dev Growth Differ. 2004 Apr;46(2):115-29
pubmed: 15066191
Cell. 1997 Dec 26;91(7):881-91
pubmed: 9428512
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Genome Biol. 2014;15(12):550
pubmed: 25516281
Curr Biol. 2009 Aug 25;19(16):1333-40
pubmed: 19631543
Genesis. 2013 Dec;51(12):803-18
pubmed: 24166799
BMC Genomics. 2020 Feb 10;21(1):137
pubmed: 32041526
Proc Biol Sci. 2018 Jun 27;285(1881):
pubmed: 30051856
Nature. 2011 Nov 23;479(7374):487-92
pubmed: 22113690
PLoS One. 2017 May 9;12(5):e0176746
pubmed: 28486514
Mol Ecol. 2010 Sep;19(18):3865-80
pubmed: 20637049
Mol Biol Evol. 2018 Sep 1;35(9):2240-2253
pubmed: 29924328
Science. 2014 Jan 24;343(6169):411-3
pubmed: 24458639
Genome Biol. 2010;11(2):R14
pubmed: 20132535
Dev Genes Evol. 2001 Mar;211(3):138-44
pubmed: 11455425
Dev Growth Differ. 2012 Feb;54(2):227-40
pubmed: 22348272
Arthropod Struct Dev. 2007 Dec;36(4):420-48
pubmed: 18089120
Dev Biol. 2009 Sep 1;333(1):202-14
pubmed: 19324029
J Exp Biol. 2013 Nov 1;216(Pt 21):4103-8
pubmed: 23948480
PLoS One. 2014 Aug 13;9(8):e104885
pubmed: 25118601
Evodevo. 2015 Apr 28;6:16
pubmed: 26034575
Nucleic Acids Res. 2015 Jul 1;43(W1):W30-8
pubmed: 25943547
Curr Biol. 2015 May 18;25(10):R403-4
pubmed: 25989075
Mol Biol Evol. 2013 Nov;30(11):2383-400
pubmed: 23927992
BMC Evol Biol. 2018 Dec 27;18(1):205
pubmed: 30587109
Integr Comp Biol. 2018 Sep 1;58(3):421-430
pubmed: 29790967
Mol Phylogenet Evol. 2015 Dec;93:107-17
pubmed: 26220837
PLoS One. 2010 May 07;5(5):e10388
pubmed: 20479884
Mol Phylogenet Evol. 2014 Oct;79:368-74
pubmed: 25014568
F1000Res. 2015 Dec 30;4:1521
pubmed: 26925227
BMC Biol. 2017 Jul 31;15(1):62
pubmed: 28756775
Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5702-7
pubmed: 21422298
Proc Biol Sci. 2015 Jun 7;282(1808):20150698
pubmed: 25948691
Dev Genes Evol. 2004 Jul;214(7):342-51
pubmed: 15221378
Evol Dev. 2015 Nov-Dec;17(6):347-55
pubmed: 26492826
Development. 2006 Jun;133(12):2347-57
pubmed: 16720876
Sci Rep. 2018 Nov 8;8(1):16589
pubmed: 30409988
Evol Dev. 2012 Sep-Oct;14(5):450-63
pubmed: 22947318
Trends Genet. 1999 Sep;15(9):371-7
pubmed: 10461206
Development. 2002 Mar;129(5):1143-54
pubmed: 11874910
Mol Biol Evol. 2014 Nov;31(11):2963-84
pubmed: 25107551
Evol Dev. 2013 Jul-Aug;15(4):280-92
pubmed: 23809702
Evol Dev. 2013 May;15(3):186-96
pubmed: 23607302
Dev Dyn. 2018 Jan;247(1):239-249
pubmed: 28850769
Heredity (Edinb). 2016 Feb;116(2):190-9
pubmed: 26419336
Dev Biol. 2015 Jun 15;402(2):276-90
pubmed: 25257304
Gigascience. 2014 May 14;3:9
pubmed: 24987520
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Evodevo. 2020 Aug 28;11:18
pubmed: 32874529
Evol Dev. 2013 Jul-Aug;15(4):228-42
pubmed: 23809698
Nat Commun. 2019 May 24;10(1):2295
pubmed: 31127117
Mol Phylogenet Evol. 2010 Jan;54(1):107-21
pubmed: 19699807
Dev Genes Evol. 2020 Mar;230(2):95-104
pubmed: 32040712
Dev Genes Evol. 2020 Mar;230(2):137-153
pubmed: 31927629
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
Cell Rep. 2017 Jan 17;18(3):762-776
pubmed: 28099853
Am Nat. 1993 Jul;142 Suppl 1:S65-77
pubmed: 19425953
Dev Biol. 2020 May 15;461(2):132-144
pubmed: 32044379
Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4525-9
pubmed: 10781056
Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):4921-6
pubmed: 22421434
Dev Genes Evol. 2012 Jul;222(4):189-216
pubmed: 22569930
Proc Natl Acad Sci U S A. 2009 Feb 3;106(5):1468-72
pubmed: 19147844
Nat Genet. 2006 Jan;38(1):107-11
pubmed: 16341223
Genome Biol Evol. 2016 Jun 27;8(6):1762-75
pubmed: 26951779
Evodevo. 2011 Apr 04;2(1):8
pubmed: 21463500
Bioessays. 2007 May;29(5):489-96
pubmed: 17450600
Nat Protoc. 2013 Aug;8(8):1494-512
pubmed: 23845962
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Syst Biol. 2019 Nov 1;68(6):896-917
pubmed: 30917194
Philos Trans R Soc Lond B Biol Sci. 2009 Oct 12;364(1531):2819-32
pubmed: 19720647
Mol Biol Evol. 2018 Mar 1;35(3):543-548
pubmed: 29220515
Genome Biol Evol. 2016 Dec 1;8(12):3640-3652
pubmed: 28172965
Bioinformatics. 2007 May 15;23(10):1289-91
pubmed: 17379693
Proc Biol Sci. 2014 Oct 7;281(1792):
pubmed: 25122224
Evodevo. 2015 Apr 28;6:15
pubmed: 26034574
Cell. 2008 Jul 11;134(1):25-36
pubmed: 18614008
Evodevo. 2020 Mar 20;11:6
pubmed: 32206294
Proc Biol Sci. 2011 Jan 22;278(1703):298-306
pubmed: 20702459
Biochim Biophys Acta. 2009 Apr;1789(4):306-14
pubmed: 19013263