A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis

Trang Hieu Nguyen; Louis Thiers; Alex Van Moerkercke; Yuechen Bai; Patricia Fernández-Calvo; Max Minne; Thomas Depuydt; Maite Colinas; Kevin Verstaen; Gert Van Isterdael; Hans Wilhelm Nützmann; Anne Osbourn; Yvan Saeys; Bert De Rybel; Klaas Vandepoele; Andrés Ritter; Alain Goossens

doi:10.1038/s41477-023-01419-8

A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis

Trang Hieu Nguyen, Louis Thiers, Alex Van Moerkercke, Yuechen Bai, Patricia Fernández-Calvo, Max Minne, Thomas Depuydt, Maite Colinas, Kevin Verstaen, Gert Van Isterdael, Hans Wilhelm Nützmann, Anne Osbourn, Yvan Saeys, Bert De Rybel, Klaas Vandepoele, Andrés Ritter, Alain Goossens

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Abstract

Plant specialized metabolites modulate developmental and ecological functions and comprise many therapeutic and other high-value compounds. However, the mechanisms determining their cell-specific expression remain unknown. Here we describe the transcriptional regulatory network that underlies cell-specific biosynthesis of triterpenes in Arabidopsis thaliana root tips. Expression of thalianol and marneral biosynthesis pathway genes depends on the phytohormone jasmonate and is limited to outer tissues. We show that this is promoted by the activity of redundant bHLH-type transcription factors from two distinct clades and coactivated by homeodomain factors. Conversely, the DOF-type transcription factor DAG1 and other regulators prevent expression of the triterpene pathway genes in inner tissues. We thus show how precise expression of triterpene biosynthesis genes is determined by a robust network of transactivators, coactivators and counteracting repressors.

Original language	English
Pages (from-to)	926-937
Number of pages	12
Journal	Nature Plants
Volume	9
Issue number	6
Early online date	15 May 2023
DOIs	https://doi.org/10.1038/s41477-023-01419-8
Publication status	Published - 1 Jun 2023

Bibliographical note

Funding Information:
This Article was written in loving memory of A. Van Moerkercke (1979–2021). The authors thank A. Bleys for critically reading the manuscript; D. Gasperini for kindly sharing the ProMYCs:NLS-VENUS reporter lines, and P. Vittorioso for the dag1 mutant, ProDAG1:GUS and DAG1 over-expressing lines; J. R. Wendrich and T. Eekhout for assistance in the launching and analysis of the scRNAseq experiment; and S. Desmet and G. Goeminne from the VIB Metabolomics Core – Ghent for the thalianol profiling. This work was supported by the European Community’s Seventh Framework Program (FP7/2007–2013) under grant agreement 613692-TriForC and H2020 Program under grant agreement 760331-Newcotiana to A.G.; the Special Research Fund from Ghent University to A.G. and A.R. (project BOF18/GOA/013), and M.M. (project BOF20/GOA/012); the Flemish Government (AI Research program) to Y.S.; the Research Foundation Flanders with research project grants to A.G. (G004515N and G008417N) and a postdoctoral fellowship to P.F.-C.; a Swiss National Science Foundation postdoctoral fellowship (P300PA_177831) to M.C.; and a China Scholarship Council PhD scholarship to Y.B. A.O. acknowledges funding support from the John Innes Foundation and the BBSRC Institute Strategic Program Grant ‘Molecules from Nature – Products and Pathways’ (BBS/E/J/000PR9790).

ASJC Scopus subject areas

Plant Science

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10.1038/s41477-023-01419-8

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This is a post-peer-review, pre-copyedit version of an article published in Nature Plants. The final authenticated version is available online at: https://doi.org/10.1038/s41477-023-01419-8
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Nguyen, T. H., Thiers, L., Van Moerkercke, A., Bai, Y., Fernández-Calvo, P., Minne, M., Depuydt, T., Colinas, M., Verstaen, K., Van Isterdael, G., Nützmann, H. W., Osbourn, A., Saeys, Y., De Rybel, B., Vandepoele, K., Ritter, A., & Goossens, A. (2023). A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis. Nature Plants, 9(6), 926-937. https://doi.org/10.1038/s41477-023-01419-8

Nguyen, TH, Thiers, L, Van Moerkercke, A, Bai, Y, Fernández-Calvo, P, Minne, M, Depuydt, T, Colinas, M, Verstaen, K, Van Isterdael, G, Nützmann, HW, Osbourn, A, Saeys, Y, De Rybel, B, Vandepoele, K, Ritter, A & Goossens, A 2023, 'A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis', Nature Plants, vol. 9, no. 6, pp. 926-937. https://doi.org/10.1038/s41477-023-01419-8

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title = "A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis",

abstract = "Plant specialized metabolites modulate developmental and ecological functions and comprise many therapeutic and other high-value compounds. However, the mechanisms determining their cell-specific expression remain unknown. Here we describe the transcriptional regulatory network that underlies cell-specific biosynthesis of triterpenes in Arabidopsis thaliana root tips. Expression of thalianol and marneral biosynthesis pathway genes depends on the phytohormone jasmonate and is limited to outer tissues. We show that this is promoted by the activity of redundant bHLH-type transcription factors from two distinct clades and coactivated by homeodomain factors. Conversely, the DOF-type transcription factor DAG1 and other regulators prevent expression of the triterpene pathway genes in inner tissues. We thus show how precise expression of triterpene biosynthesis genes is determined by a robust network of transactivators, coactivators and counteracting repressors.",

author = "Nguyen, {Trang Hieu} and Louis Thiers and {Van Moerkercke}, Alex and Yuechen Bai and Patricia Fern{\'a}ndez-Calvo and Max Minne and Thomas Depuydt and Maite Colinas and Kevin Verstaen and {Van Isterdael}, Gert and N{\"u}tzmann, {Hans Wilhelm} and Anne Osbourn and Yvan Saeys and {De Rybel}, Bert and Klaas Vandepoele and Andr{\'e}s Ritter and Alain Goossens",

note = "Funding Information: This Article was written in loving memory of A. Van Moerkercke (1979–2021). The authors thank A. Bleys for critically reading the manuscript; D. Gasperini for kindly sharing the ProMYCs:NLS-VENUS reporter lines, and P. Vittorioso for the dag1 mutant, ProDAG1:GUS and DAG1 over-expressing lines; J. R. Wendrich and T. Eekhout for assistance in the launching and analysis of the scRNAseq experiment; and S. Desmet and G. Goeminne from the VIB Metabolomics Core – Ghent for the thalianol profiling. This work was supported by the European Community{\textquoteright}s Seventh Framework Program (FP7/2007–2013) under grant agreement 613692-TriForC and H2020 Program under grant agreement 760331-Newcotiana to A.G.; the Special Research Fund from Ghent University to A.G. and A.R. (project BOF18/GOA/013), and M.M. (project BOF20/GOA/012); the Flemish Government (AI Research program) to Y.S.; the Research Foundation Flanders with research project grants to A.G. (G004515N and G008417N) and a postdoctoral fellowship to P.F.-C.; a Swiss National Science Foundation postdoctoral fellowship (P300PA_177831) to M.C.; and a China Scholarship Council PhD scholarship to Y.B. A.O. acknowledges funding support from the John Innes Foundation and the BBSRC Institute Strategic Program Grant {\textquoteleft}Molecules from Nature – Products and Pathways{\textquoteright} (BBS/E/J/000PR9790). ",

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doi = "10.1038/s41477-023-01419-8",

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T1 - A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis

AU - Nguyen, Trang Hieu

AU - Thiers, Louis

AU - Van Moerkercke, Alex

AU - Bai, Yuechen

AU - Fernández-Calvo, Patricia

AU - Minne, Max

AU - Depuydt, Thomas

AU - Colinas, Maite

AU - Verstaen, Kevin

AU - Van Isterdael, Gert

AU - Nützmann, Hans Wilhelm

AU - Osbourn, Anne

AU - Saeys, Yvan

AU - De Rybel, Bert

AU - Vandepoele, Klaas

AU - Ritter, Andrés

AU - Goossens, Alain

N1 - Funding Information: This Article was written in loving memory of A. Van Moerkercke (1979–2021). The authors thank A. Bleys for critically reading the manuscript; D. Gasperini for kindly sharing the ProMYCs:NLS-VENUS reporter lines, and P. Vittorioso for the dag1 mutant, ProDAG1:GUS and DAG1 over-expressing lines; J. R. Wendrich and T. Eekhout for assistance in the launching and analysis of the scRNAseq experiment; and S. Desmet and G. Goeminne from the VIB Metabolomics Core – Ghent for the thalianol profiling. This work was supported by the European Community’s Seventh Framework Program (FP7/2007–2013) under grant agreement 613692-TriForC and H2020 Program under grant agreement 760331-Newcotiana to A.G.; the Special Research Fund from Ghent University to A.G. and A.R. (project BOF18/GOA/013), and M.M. (project BOF20/GOA/012); the Flemish Government (AI Research program) to Y.S.; the Research Foundation Flanders with research project grants to A.G. (G004515N and G008417N) and a postdoctoral fellowship to P.F.-C.; a Swiss National Science Foundation postdoctoral fellowship (P300PA_177831) to M.C.; and a China Scholarship Council PhD scholarship to Y.B. A.O. acknowledges funding support from the John Innes Foundation and the BBSRC Institute Strategic Program Grant ‘Molecules from Nature – Products and Pathways’ (BBS/E/J/000PR9790).

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N2 - Plant specialized metabolites modulate developmental and ecological functions and comprise many therapeutic and other high-value compounds. However, the mechanisms determining their cell-specific expression remain unknown. Here we describe the transcriptional regulatory network that underlies cell-specific biosynthesis of triterpenes in Arabidopsis thaliana root tips. Expression of thalianol and marneral biosynthesis pathway genes depends on the phytohormone jasmonate and is limited to outer tissues. We show that this is promoted by the activity of redundant bHLH-type transcription factors from two distinct clades and coactivated by homeodomain factors. Conversely, the DOF-type transcription factor DAG1 and other regulators prevent expression of the triterpene pathway genes in inner tissues. We thus show how precise expression of triterpene biosynthesis genes is determined by a robust network of transactivators, coactivators and counteracting repressors.

AB - Plant specialized metabolites modulate developmental and ecological functions and comprise many therapeutic and other high-value compounds. However, the mechanisms determining their cell-specific expression remain unknown. Here we describe the transcriptional regulatory network that underlies cell-specific biosynthesis of triterpenes in Arabidopsis thaliana root tips. Expression of thalianol and marneral biosynthesis pathway genes depends on the phytohormone jasmonate and is limited to outer tissues. We show that this is promoted by the activity of redundant bHLH-type transcription factors from two distinct clades and coactivated by homeodomain factors. Conversely, the DOF-type transcription factor DAG1 and other regulators prevent expression of the triterpene pathway genes in inner tissues. We thus show how precise expression of triterpene biosynthesis genes is determined by a robust network of transactivators, coactivators and counteracting repressors.

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A redundant transcription factor network steers spatiotemporal Arabidopsis triterpene synthesis

Abstract

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