Adaptive protein divergence of BMP ligands takes place under developmental and evolutionary constraints

Petra Tauscher, Jinghua Gui, Osamu Shimmi

Tutkimustuotos: ArtikkelijulkaisuArtikkeliTieteellinenvertaisarvioitu

Kuvaus

The bone morphogenetic protein (BMP) signaling network, comprising evolutionary conserved BMP2/4/Decapentaplegic (Dpp) and Chordin/Short gastrulation (Sog), is widely utilized for dorsal-ventral (DV) patterning during animal development. A similar network is required for posterior crossvein (PCV) formation in the Drosophila pupal wing. Although both transcriptional and post-transcriptional regulation of co-factors in the network gives rise to tissue-specific and species-specific properties, their mechanisms are incompletely understood. In Drosophila, BMP5/6/7/8-type ligands, Screw (Scw) and Glass bottom boat (Gbb), form heterodimers with Dpp for DV patterning and PCV development, respectively. Sequence analysis indicates that the Scw ligand contains two N-glycosylation motifs: one being highly conserved between BMP2/4- and BMP5/6/7/8-type ligands, and the other being Scw ligand specific. Our data reveal that N-glycosylation of the Scw ligand boosts BMP signaling both in cell culture and in the embryo. In contrast, N-glycosylation modifications of Gbb or Scw ligands reduce the consistency of PCV development. These results suggest that tolerance for structural changes of BMP5/6/7/8-type ligands is dependent on developmental constraints. Furthermore, gain and loss of N-glycosylation motifs in conserved signaling molecules under evolutionary constraints appear to constitute flexible modules to adapt to developmental processes.
Alkuperäiskielienglanti
LehtiDevelopment
Vuosikerta143
Numero20
Sivut3742-3750
Sivumäärä9
ISSN0950-1991
DOI - pysyväislinkit
TilaJulkaistu - 18 lokakuuta 2016
OKM-julkaisutyyppiA1 Alkuperäisartikkeli tieteellisessä aikakauslehdessä, vertaisarvioitu

Tieteenalat

  • 1184 Genetiikka, kehitysbiologia, fysiologia
  • 1182 Biokemia, solu- ja molekyylibiologia

Lainaa tätä

Tauscher, Petra ; Gui, Jinghua ; Shimmi, Osamu. / Adaptive protein divergence of BMP ligands takes place under developmental and evolutionary constraints. Julkaisussa: Development. 2016 ; Vuosikerta 143, Nro 20. Sivut 3742-3750.
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title = "Adaptive protein divergence of BMP ligands takes place under developmental and evolutionary constraints",
abstract = "The bone morphogenetic protein (BMP) signaling network, comprising evolutionary conserved BMP2/4/Decapentaplegic (Dpp) and Chordin/Short gastrulation (Sog), is widely utilized for dorsal-ventral (DV) patterning during animal development. A similar network is required for posterior crossvein (PCV) formation in the Drosophila pupal wing. Although both transcriptional and post-transcriptional regulation of co-factors in the network gives rise to tissue-specific and species-specific properties, their mechanisms are incompletely understood. In Drosophila, BMP5/6/7/8-type ligands, Screw (Scw) and Glass bottom boat (Gbb), form heterodimers with Dpp for DV patterning and PCV development, respectively. Sequence analysis indicates that the Scw ligand contains two N-glycosylation motifs: one being highly conserved between BMP2/4- and BMP5/6/7/8-type ligands, and the other being Scw ligand specific. Our data reveal that N-glycosylation of the Scw ligand boosts BMP signaling both in cell culture and in the embryo. In contrast, N-glycosylation modifications of Gbb or Scw ligands reduce the consistency of PCV development. These results suggest that tolerance for structural changes of BMP5/6/7/8-type ligands is dependent on developmental constraints. Furthermore, gain and loss of N-glycosylation motifs in conserved signaling molecules under evolutionary constraints appear to constitute flexible modules to adapt to developmental processes.",
keywords = "1184 Genetics, developmental biology, physiology, Drosophila melanogaster, PROTEIN EVOLUTION, 1182 Biochemistry, cell and molecular biology, Glycosylation",
author = "Petra Tauscher and Jinghua Gui and Osamu Shimmi",
year = "2016",
month = "10",
day = "18",
doi = "10.1242/dev.130427",
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volume = "143",
pages = "3742--3750",
journal = "Development",
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Adaptive protein divergence of BMP ligands takes place under developmental and evolutionary constraints. / Tauscher, Petra; Gui, Jinghua; Shimmi, Osamu.

julkaisussa: Development, Vuosikerta 143, Nro 20, 18.10.2016, s. 3742-3750.

Tutkimustuotos: ArtikkelijulkaisuArtikkeliTieteellinenvertaisarvioitu

TY - JOUR

T1 - Adaptive protein divergence of BMP ligands takes place under developmental and evolutionary constraints

AU - Tauscher, Petra

AU - Gui, Jinghua

AU - Shimmi, Osamu

PY - 2016/10/18

Y1 - 2016/10/18

N2 - The bone morphogenetic protein (BMP) signaling network, comprising evolutionary conserved BMP2/4/Decapentaplegic (Dpp) and Chordin/Short gastrulation (Sog), is widely utilized for dorsal-ventral (DV) patterning during animal development. A similar network is required for posterior crossvein (PCV) formation in the Drosophila pupal wing. Although both transcriptional and post-transcriptional regulation of co-factors in the network gives rise to tissue-specific and species-specific properties, their mechanisms are incompletely understood. In Drosophila, BMP5/6/7/8-type ligands, Screw (Scw) and Glass bottom boat (Gbb), form heterodimers with Dpp for DV patterning and PCV development, respectively. Sequence analysis indicates that the Scw ligand contains two N-glycosylation motifs: one being highly conserved between BMP2/4- and BMP5/6/7/8-type ligands, and the other being Scw ligand specific. Our data reveal that N-glycosylation of the Scw ligand boosts BMP signaling both in cell culture and in the embryo. In contrast, N-glycosylation modifications of Gbb or Scw ligands reduce the consistency of PCV development. These results suggest that tolerance for structural changes of BMP5/6/7/8-type ligands is dependent on developmental constraints. Furthermore, gain and loss of N-glycosylation motifs in conserved signaling molecules under evolutionary constraints appear to constitute flexible modules to adapt to developmental processes.

AB - The bone morphogenetic protein (BMP) signaling network, comprising evolutionary conserved BMP2/4/Decapentaplegic (Dpp) and Chordin/Short gastrulation (Sog), is widely utilized for dorsal-ventral (DV) patterning during animal development. A similar network is required for posterior crossvein (PCV) formation in the Drosophila pupal wing. Although both transcriptional and post-transcriptional regulation of co-factors in the network gives rise to tissue-specific and species-specific properties, their mechanisms are incompletely understood. In Drosophila, BMP5/6/7/8-type ligands, Screw (Scw) and Glass bottom boat (Gbb), form heterodimers with Dpp for DV patterning and PCV development, respectively. Sequence analysis indicates that the Scw ligand contains two N-glycosylation motifs: one being highly conserved between BMP2/4- and BMP5/6/7/8-type ligands, and the other being Scw ligand specific. Our data reveal that N-glycosylation of the Scw ligand boosts BMP signaling both in cell culture and in the embryo. In contrast, N-glycosylation modifications of Gbb or Scw ligands reduce the consistency of PCV development. These results suggest that tolerance for structural changes of BMP5/6/7/8-type ligands is dependent on developmental constraints. Furthermore, gain and loss of N-glycosylation motifs in conserved signaling molecules under evolutionary constraints appear to constitute flexible modules to adapt to developmental processes.

KW - 1184 Genetics, developmental biology, physiology

KW - Drosophila melanogaster

KW - PROTEIN EVOLUTION

KW - 1182 Biochemistry, cell and molecular biology

KW - Glycosylation

U2 - 10.1242/dev.130427

DO - 10.1242/dev.130427

M3 - Article

VL - 143

SP - 3742

EP - 3750

JO - Development

JF - Development

SN - 0950-1991

IS - 20

ER -