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  1. Pub 'PMID:30661644'

Title

Evolution of embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians.

Authors

Madgwick A, Magri M, Dantec C, Gailly D, Fiuza U, Guignard L, Hettinger S, Gomez-Skarmeta J, Lemaire P

Journal

Dev. Biol. 2019; 448(2):71-87

PubMed ID

PMID:30661644

Abstract

Ascidian species of the Phallusia and Ciona genera are distantly related, their last common ancestor dating several hundred million years ago. Although their genome sequences have extensively diverged since this radiation, Phallusia and Ciona species share almost identical early morphogenesis and stereotyped cell lineages. Here, we explored the evolution of transcriptional control between P. mammillata and C. robusta. We combined genome-wide mapping of open chromatin regions in both species with a comparative analysis of the regulatory sequences of a test set of 10 pairs of orthologous early regulatory genes with conserved expression patterns. We find that ascidian chromatin accessibility landscapes obey similar rules as in other metazoa. Open-chromatin regions are short, highly conserved within each genus and cluster around regulatory genes. The dynamics of chromatin accessibility and closest-gene expression are strongly correlated during early embryogenesis. Open-chromatin regions are highly enriched in cis-regulatory elements: 73% of 49 open chromatin regions around our test genes behaved as either distal enhancers or proximal enhancer/promoters following electroporation in Phallusia eggs. Analysis of this datasets suggests a pervasive use in ascidians of "shadow" enhancers with partially overlapping activities. Cross-species electroporations point to a deep conservation of both the trans-regulatory logic between these distantly-related ascidians and the cis-regulatory activities of individual enhancers. Finally, we found that the relative order and approximate distance to the transcription start site of open chromatin regions can be conserved between Ciona and Phallusia species despite extensive sequence divergence, a property that can be used to identify orthologous enhancers, whose regulatory activity can partially diverge.

Data related to this article

Fates affected

No result

Gene involved Fates

Genes functionally analyzed

No result

Gene Name Experimental evidence

Genes with description of Wild Type Expression

26 results

Gene Name Experimental evidence
Phmamm.CG.MTP2014.S242.g05996 (SFRP1; SFRP2; SFRP5) Show experimental evidence
Phmamm.CG.MTP2014.S160.g04451 (EPHA4; EPHA7; EPHB1) Show experimental evidence
Phmamm.CG.MTP2014.S597.g10419 (NKX2-1; NKX2-2; NKX2-6) Show experimental evidence
Phmamm.CG.MTP2014.S362.g07801 (BMP10; LEFTY1; LEFTY2) Show experimental evidence
Phmamm.CG.MTP2014.S70.g02476 (SOCS6; SOCS7) Show experimental evidence
Phmamm.CG.MTP2014.S411.g08422 (ELK1; ELK3; ELK4) Show experimental evidence
Phmamm.CG.MTP2014.S74.g02578 (BMP2; BMP3; BMP7) Show experimental evidence
Phmamm.CG.MTP2014.S128.g03805 (FGF16; FGF20; FGF9) Show experimental evidence
Phmamm.CG.MTP2014.S50.g01891 (FOXA1; FOXA2; FOXA3) Show experimental evidence
Phmamm.CG.MTP2014.S253.g06179 (FOXD1; FOXD3; FOXD4) Show experimental evidence
Phmamm.CG.MTP2014.S2332.g16546 (LHX1; LHX3; LHX4) Show experimental evidence
Phmamm.CG.MTP2014.S1711.g15500 (BMP10; GDF6; NODAL) Show experimental evidence
Phmamm.CG.MTP2014.S166.g04580 (CRX; OTX1; OTX2) Show experimental evidence
Phmamm.CG.MTP2014.S14.g00600 (BMP1; TLL1; TLL2) Show experimental evidence
Phmamm.CG.MTP2014.S180.g04861 (HES1; HES4; HES6) Show experimental evidence
Phmamm.CG.MTP2014.S224.g05660 (ZFP36; ZFP36L1; ZFP36L2) Show experimental evidence
Phmamm.CG.MTP2014.S272.g06489 (SOX14; SOX2; SOX21) Show experimental evidence
Phmamm.CG.MTP2014.S669.g11097 (TFAP2A; TFAP2B; TFAP2E) Show experimental evidence
Phmamm.CG.MTP2014.S333.g07410 (ADAMTS1; ADAMTS15; ADAMTS9) Show experimental evidence
Phmamm.CG.MTP2014.S641.g10833 (ERF; ETV3; ETV3L) Show experimental evidence
Phmamm.CG.MTP2014.S58.g02081 (PCDH10; PCDH12; PCDH18) Show experimental evidence
Phmamm.CG.MTP2014.S232.g05813 (CDH11; CDH18; CDH6) Show experimental evidence
Phmamm.CG.MTP2014.S1645.g15327 (TBX2; TBX3; TBX4) Show experimental evidence
Phmamm.CG.MTP2014.S369.g07899 (Phmamm.CG.MTP2014.S369.g07899) Show experimental evidence
Phmamm.CG.MTP2014.S428.g08617 (WNT4; WNT5A; WNT5B) Show experimental evidence
Phmamm.CG.MTP2014.S1371.g14629 (SP7; SP8; SP9) Show experimental evidence

Molecular Tools

No result

Molecular Tool Name

Cis-regulatory regions

83 results

Cis-reg Name
CibpFoxAa
Cirobu.REG.KH2012.S215.4:99820-100244|Lhx3
Cirobu.REG.KH2012.C11:4406300-4406535|FoxA
Cirobu.REG.KH2012.C11:4405311-4406043|FoxA
Cirobu.REG.KH2012.L106:34858-35128|Nodal
Cirobu.REG.KH2012.C4:4314434-4314799|Otx
Phmamm.REG.CG.MTP2014.S128:60456-61171|Fgf9/16/20
Phmamm.REG.CG.MTP2014.S128:57500-58015|Fgf9/16/20
Phmamm.REG.CG.MTP2014.S128:56761-57079|Fgf9/16/20
Phmamm.REG.CG.MTP2014.S128:58085-58550|Fgf9/16/20
Phmamm.REG.CG.MTP2014.S128:58720-59379|Fgf9/16/20
Phmamm.REG.CG.MTP2014.S50:172500-172959|FoxAa
Phmamm.REG.CG.MTP2014.S50:168459-169203|FoxAa
Phmamm.REG.CG.MTP2014.S50:170660-171585|FoxAa
Phmamm.REG.CG.MTP2014.S50:171674-172329|FoxAa
Phmamm.REG.CG.MTP2014.S253:124203-124750|FoxD
Phmamm.REG.CG.MTP2014.S253:122472-122988|FoxD
Phmamm.REG.CG.MTP2014.S253:122003-122412|FoxD
Phmamm.REG.CG.MTP2014.S253:120353-121461|FoxD
Phmamm.REG.CG.MTP2014.S253:125661-126068|FoxD
Phmamm.REG.CG.MTP2014.S253:130353-130823|FoxD
Phmamm.REG.CG.MTP2014.S2332:6677-7993|Lhx3/4
Phmamm.REG.CG.MTP2014.S2332:10795-11099|Lhx3/4
Phmamm.REG.CG.MTP2014.S1711:7214-7423|Nodal
Phmamm.REG.CG.MTP2014.S1711:8255-8854|Nodal
Phmamm.REG.CG.MTP2014.S1711:9130-9419|Nodal
Phmamm.REG.CG.MTP2014.S1711:9716-10015|Nodal
Phmamm.REG.CG.MTP2014.S166:47798-48149|Otx
Phmamm.REG.CG.MTP2014.S166:49113-49319|Otx
Phmamm.REG.CG.MTP2014.S166:50503-50840|Otx
Phmamm.REG.CG.MTP2014.S166:47119-47469|Otx
Phmamm.REG.CG.MTP2014.S166:46706-46976|Otx
Phmamm.REG.CG.MTP2014.S166:45338-45692|Otx
Phmamm.REG.CG.MTP2014.S166:44529-44800|Otx
Phmamm.REG.CG.MTP2014.S160:16086-16385|Eph1
Phmamm.REG.CG.MTP2014.S160:15388-15940|Eph1
Phmamm.REG.CG.MTP2014.S160:17202-17589|Eph1
Phmamm.REG.CG.MTP2014.S160:17627-17879|Eph1
Phmamm.REG.CG.MTP2014.S160:19347-19784|Eph1
Phmamm.REG.CG.MTP2014.S597:19236-19686|TTF1/Nkx2-1
Phmamm.REG.CG.MTP2014.S597:21405-21785|TTF1/Nkx2-1
Phmamm.REG.CG.MTP2014.S597:17594-18238|TTF1/Nkx2-1
Phmamm.REG.CG.MTP2014.S597:16901-17288|TTF1/Nkx2-1
Phmamm.REG.CG.MTP2014.S597:19759-20374|TTF1/Nkx2-1
Phmamm.REG.CG.MTP2014.S362:35908-36277|Lefty
Phmamm.REG.CG.MTP2014.S362:37650-37908|Lefty
Phmamm.REG.CG.MTP2014.S70:155422-155594|SOCS7
Phmamm.REG.CG.MTP2014.S411:119129-121273|ELK
Phmamm.REG.CG.MTP2014.S411:109256-109999|ELK
Phmamm.REG.CG.MTP2014.S58:56959-57277|Hes-a
Phmamm.REG.CG.MTP2014.S58:57311-57665|Hes-a
Phmamm.REG.CG.MTP2014.S58:57901-58298|Hes-a
Phmamm.REG.CG.MTP2014.S58:59345-59813|Hes-a
Phmamm.REG.CG.MTP2014.S242:23509-24055|sFRP2
Phmamm.REG.CG.MTP2014.S242:26006-26968|sFRP2
Phmamm.REG.CG.MTP2014.S229:71129-71430|Neurogenin
Phmamm.REG.CG.MTP2014.S229:72352-72621|Neurogenin
Phmamm.REG.CG.MTP2014.S229:75185-75749|Neurogenin
Phmamm.REG.CG.MTP2014.S229:79141-79402|Neurogenin
Phmamm.REG.CG.MTP2014.S229:80505-80700|Neurogenin
Phmamm.REG.CG.MTP2014.S229:85795-86004|Neurogenin
Phmamm.REG.CG.MTP2014.S229:90042-90375|Neurogenin
Phmamm.REG.CG.MTP2014.S229:90811-91212|Neurogenin
Phmamm.REG.CG.MTP2014.S14:100241-100570|Tolloid
Phmamm.REG.CG.MTP2014.S14:106625-107597|Tolloid
Phmamm.REG.CG.MTP2014.S14:101721-102143|Tolloid
Phmamm.REG.CG.MTP2014.S23:114940-115172|EphrinA-c
Phmamm.REG.CG.MTP2014.S23:115350-115650|EphrinA-c
Phmamm.REG.CG.MTP2014.S23:115670-115899|EphrinA-c
Phmamm.REG.CG.MTP2014.S23:116184-116569|EphrinA-c
Phmamm.REG.CG.MTP2014.S362:36202-36498|Lefty
Phmamm.REG.CG.MTP2014.S50:168458-169207|FoxAa
Cirobu.REG.KH2012.C1.979450-980209
Cirobu.REG.KH2012.C1.978600-979199
Cirobu.REG.KH2012.C1.984600-985399
Cirobu.REG.KH2012.C1.988300-989199
Cirobu.REG.KH2012.C3.6290100-6290899
Cirobu.REG.KH2012.C3.6291450-6291999
Cirobu.REG.KH2012.C3.6292000-6292899
Cirobu.REG.KH2012.C10.3633300-3633899
Cirobu.REG.KH2012.C10.3633890-3634509
Cirobu.REG.KH2012.C10.3635600-3636699
Cirobu.REG.KH2012.C12.3766830-3767619

Constructs

82 results

Construct Name Experimental evidence
p.Cirobu.REG.KH2012.S215.4:99820-100244>LacZ Show experimental evidence
p.Cirobu.REG.KH2012.C11:4406300-4406535>LacZ Show experimental evidence
p.Cirobu.REG.KH2012.C11:4405311-4406043>LacZ Show experimental evidence
p.Cirobu.REG.KH2012.L106:34858-35128>LacZ Show experimental evidence
p.Cirobu.REG.KH2012.C4:4314434-4314799>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S128:60456-61171>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S128:57500-58015>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S128:56761-57079>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S128:58085-58550>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S128:58720-59379>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S50:172500-172959>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S50:168459-169203>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S50:170660-171585>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S50:171674-172329>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:124203-124750>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:122472-122988>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:122003-122412>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:120353-121461>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:125661-126068>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S253:130353-130823>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S2332:6677-7993>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S2332:10795-11099>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S1711:7214-7423>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S1711:8255-8854>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S1711:9130-9419>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S1711:9716-10015>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:47798-48149>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:49113-49319>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:50503-50840>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:47119-47469>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:46706-46976>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:45338-45692>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S166:44529-44800>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S160:16086-16385>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S160:15388-15940>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S160:17202-17589>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S160:17627-17879>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S160:19347-19784>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S597:19236-19686>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S597:21405-21785>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S597:17594-18238>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S597:16901-17288>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S597:19759-20374>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S362:35908-36277>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S362:37650-37908>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S70:155422-155594>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S411:119129-121273>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S411:109256-109999>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S58:56959-57277>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S58:57311-57665>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S58:57901-58298>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S58:59345-59813>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S242:23509-24055>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S242:26006-26968>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:71129-71430>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:72352-72621>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:75185-75749>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:79141-79402>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:80505-80700>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:85795-86004>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:90042-90375>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S229:90811-91212>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S14:100241-100570>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S14:106625-107597>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S14:101721-102143>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S23:114940-115172>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S23:115350-115650>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S23:115670-115899>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S23:116184-116569>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S362:36202-36498>LacZ Show experimental evidence
p.Phmamm.REG.CG.MTP2014.S50:168458-169207>LacZ Show experimental evidence
pCirobu.REG00001476>NLSLacZ Show experimental evidence
pCirobu.REG00001477:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001478:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001479:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001480:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001482:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001481>NLSLacZ Show experimental evidence
pCirobu.REG00001483:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001484:Ciinte.bpFog>NLSLacZ Show experimental evidence
pCirobu.REG00001485>NLSLacZ Show experimental evidence
pCirobu.REG00001486>NLSLacZ Show experimental evidence

RNA-Seq data

No result

Studied Transcriptome Experiment ID