Active and repressed biosynthetic gene clusters have spatially distinct chromosome states

Nützmann, Hans-Wilhelm; Dörr, Daniel; Ramírez-Colmenero, América; Sotelo-Fonseca, Jesús Emiliano; Wegel, Eva; Di Stefano, Marco; Wingett, Steven W.; Fraser, Peter; Hurst, Laurence; Fernandez-Valverde, Selene L.; Osbourn, Anne

Active and repressed biosynthetic gene clusters have spatially distinct chromosome states

Nützmann H-W, Dörr D, Ramírez-Colmenero A, Sotelo-Fonseca JE, Wegel E, Di Stefano M, Wingett SW, Fraser P, Hurst L, Fernandez-Valverde SL, Osbourn A (2020)
Proceedings of the National Academy of Sciences: 201920474.

Zeitschriftenaufsatz | E-Veröff. vor dem Druck | Englisch

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DOI

https://doi.org/10.1073/pnas.1920474117

Autor*in

Nützmann, Hans-Wilhelm; Dörr, Daniel^UniBi ; Ramírez-Colmenero, América; Sotelo-Fonseca, Jesús Emiliano; Wegel, Eva; Di Stefano, Marco; Wingett, Steven W.; Fraser, Peter; Hurst, Laurence; Fernandez-Valverde, Selene L.; Osbourn, Anne

Einrichtung

Technische Fakultät > AG Genome Data Science

Abstract / Bemerkung

While colocalization within a bacterial operon enables coexpression of the constituent genes, the mechanistic logic of clustering of nonhomologous monocistronic genes in eukaryotes is not immediately obvious. Biosynthetic gene clusters that encode pathways for specialized metabolites are an exception to the classical eukaryote rule of random gene location and provide paradigmatic exemplars with which to understand eukaryotic cluster dynamics and regulation. Here, using 3C, Hi-C, and Capture Hi-C (CHi-C) organ-specific chromosome conformation capture techniques along with high-resolution microscopy, we investigate how chromosome topology relates to transcriptional activity of clustered biosynthetic pathway genes in Arabidopsis thaliana. Our analyses reveal that biosynthetic gene clusters are embedded in local hot spots of 3D contacts that segregate cluster regions from the surrounding chromosome environment. The spatial conformation of these cluster-associated domains differs between transcriptionally active and silenced clusters. We further show that silenced clusters associate with heterochromatic chromosomal domains toward the periphery of the nucleus, while transcriptionally active clusters relocate away from the nuclear periphery. Examination of chromosome structure at unrelated clusters in maize, rice, and tomato indicates that integration of clustered pathway genes into distinct topological domains is a common feature in plant genomes. Our results shed light on the potential mechanisms that constrain coexpression within clusters of nonhomologous eukaryotic genes and suggest that gene clustering in the one-dimensional chromosome is accompanied by compartmentalization of the 3D chromosome.

Stichworte

Multidisciplinary

Erscheinungsjahr

2020

Zeitschriftentitel

Proceedings of the National Academy of Sciences

Art.-Nr.

201920474

ISSN

0027-8424

eISSN

1091-6490

Page URI

https://pub.uni-bielefeld.de/record/2943733

Zitieren

Nützmann H-W, Dörr D, Ramírez-Colmenero A, et al. Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proceedings of the National Academy of Sciences. 2020: 201920474.

Nützmann, H. - W., Dörr, D., Ramírez-Colmenero, A., Sotelo-Fonseca, J. E., Wegel, E., Di Stefano, M., Wingett, S. W., et al. (2020). Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proceedings of the National Academy of Sciences, 201920474. doi:10.1073/pnas.1920474117

Nützmann, Hans-Wilhelm, Dörr, Daniel, Ramírez-Colmenero, América, Sotelo-Fonseca, Jesús Emiliano, Wegel, Eva, Di Stefano, Marco, Wingett, Steven W., et al. 2020. “Active and repressed biosynthetic gene clusters have spatially distinct chromosome states”. Proceedings of the National Academy of Sciences: 201920474.

Nützmann, H. - W., Dörr, D., Ramírez-Colmenero, A., Sotelo-Fonseca, J. E., Wegel, E., Di Stefano, M., Wingett, S. W., Fraser, P., Hurst, L., Fernandez-Valverde, S. L., et al. (2020). Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proceedings of the National Academy of Sciences:201920474.

Nützmann, H.-W., et al., 2020. Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proceedings of the National Academy of Sciences, : 201920474.

H.-W. Nützmann, et al., “Active and repressed biosynthetic gene clusters have spatially distinct chromosome states”, Proceedings of the National Academy of Sciences, 2020, : 201920474.

Nützmann, H.-W., Dörr, D., Ramírez-Colmenero, A., Sotelo-Fonseca, J.E., Wegel, E., Di Stefano, M., Wingett, S.W., Fraser, P., Hurst, L., Fernandez-Valverde, S.L., Osbourn, A.: Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proceedings of the National Academy of Sciences. : 201920474 (2020).

Nützmann, Hans-Wilhelm, Dörr, Daniel, Ramírez-Colmenero, América, Sotelo-Fonseca, Jesús Emiliano, Wegel, Eva, Di Stefano, Marco, Wingett, Steven W., Fraser, Peter, Hurst, Laurence, Fernandez-Valverde, Selene L., and Osbourn, Anne. “Active and repressed biosynthetic gene clusters have spatially distinct chromosome states”. Proceedings of the National Academy of Sciences (2020): 201920474.

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