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Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum

Major phenotypic innovations in social amoeba evolution occurred at the transition between the Polysphondylia and group 4 Dictyostelia, which comprise the model organism Dictyostelium discoideum, such as the formation of a new structure, the basal disk. Basal disk differentiation and robust stalk fo...

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Autores principales: Narita, Takaaki B, Kawabe, Yoshinori, Kin, Koryu, Gibbs, Richard A, Kuspa, Adam, Muzny, Donna M, Richards, Stephen, Strassmann, Joan E, Sucgang, Richard, Worley, Kim C, Schaap, Pauline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7259674/
https://www.ncbi.nlm.nih.gov/pubmed/32386295
http://dx.doi.org/10.1093/gbe/evaa079
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author Narita, Takaaki B
Kawabe, Yoshinori
Kin, Koryu
Gibbs, Richard A
Kuspa, Adam
Muzny, Donna M
Richards, Stephen
Strassmann, Joan E
Sucgang, Richard
Worley, Kim C
Schaap, Pauline
author_facet Narita, Takaaki B
Kawabe, Yoshinori
Kin, Koryu
Gibbs, Richard A
Kuspa, Adam
Muzny, Donna M
Richards, Stephen
Strassmann, Joan E
Sucgang, Richard
Worley, Kim C
Schaap, Pauline
author_sort Narita, Takaaki B
collection PubMed
description Major phenotypic innovations in social amoeba evolution occurred at the transition between the Polysphondylia and group 4 Dictyostelia, which comprise the model organism Dictyostelium discoideum, such as the formation of a new structure, the basal disk. Basal disk differentiation and robust stalk formation require the morphogen DIF-1, synthesized by the polyketide synthase StlB, the des-methyl-DIF-1 methyltransferase DmtA, and the chlorinase ChlA, which are conserved throughout Dictyostelia. To understand how the basal disk and other innovations evolved in group 4, we sequenced and annotated the Polysphondylium violaceum (Pvio) genome, performed cell type-specific transcriptomics to identify cell-type marker genes, and developed transformation and gene knock-out procedures for Pvio. We used the novel methods to delete the Pvio stlB gene. The Pvio stlB(−) mutants formed misshapen curly sorogens with thick and irregular stalks. As fruiting body formation continued, the upper stalks became more regular, but structures contained 40% less spores. The stlB(−) sorogens overexpressed a stalk gene and underexpressed a (pre)spore gene. Normal fruiting body formation and sporulation were restored in Pvio stlB(−) by including DIF-1 in the supporting agar. These data indicate that, although conserved, stlB and its product(s) acquired both a novel role in the group 4 Dictyostelia and a role opposite to that in its sister group.
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spelling pubmed-72596742020-06-03 Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum Narita, Takaaki B Kawabe, Yoshinori Kin, Koryu Gibbs, Richard A Kuspa, Adam Muzny, Donna M Richards, Stephen Strassmann, Joan E Sucgang, Richard Worley, Kim C Schaap, Pauline Genome Biol Evol Research Article Major phenotypic innovations in social amoeba evolution occurred at the transition between the Polysphondylia and group 4 Dictyostelia, which comprise the model organism Dictyostelium discoideum, such as the formation of a new structure, the basal disk. Basal disk differentiation and robust stalk formation require the morphogen DIF-1, synthesized by the polyketide synthase StlB, the des-methyl-DIF-1 methyltransferase DmtA, and the chlorinase ChlA, which are conserved throughout Dictyostelia. To understand how the basal disk and other innovations evolved in group 4, we sequenced and annotated the Polysphondylium violaceum (Pvio) genome, performed cell type-specific transcriptomics to identify cell-type marker genes, and developed transformation and gene knock-out procedures for Pvio. We used the novel methods to delete the Pvio stlB gene. The Pvio stlB(−) mutants formed misshapen curly sorogens with thick and irregular stalks. As fruiting body formation continued, the upper stalks became more regular, but structures contained 40% less spores. The stlB(−) sorogens overexpressed a stalk gene and underexpressed a (pre)spore gene. Normal fruiting body formation and sporulation were restored in Pvio stlB(−) by including DIF-1 in the supporting agar. These data indicate that, although conserved, stlB and its product(s) acquired both a novel role in the group 4 Dictyostelia and a role opposite to that in its sister group. Oxford University Press 2020-04-18 /pmc/articles/PMC7259674/ /pubmed/32386295 http://dx.doi.org/10.1093/gbe/evaa079 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Narita, Takaaki B
Kawabe, Yoshinori
Kin, Koryu
Gibbs, Richard A
Kuspa, Adam
Muzny, Donna M
Richards, Stephen
Strassmann, Joan E
Sucgang, Richard
Worley, Kim C
Schaap, Pauline
Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title_full Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title_fullStr Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title_full_unstemmed Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title_short Loss of the Polyketide Synthase StlB Results in Stalk Cell Overproduction in Polysphondylium violaceum
title_sort loss of the polyketide synthase stlb results in stalk cell overproduction in polysphondylium violaceum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7259674/
https://www.ncbi.nlm.nih.gov/pubmed/32386295
http://dx.doi.org/10.1093/gbe/evaa079
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