Environmental gradients reveal stress hubs pre-dating plant terrestrialization

Plant terrestrialization brought forth the land plants (embryophytes). Embryophytes account for most of the biomass on land and evolved from streptophyte algae in a singular event. Recent advances have unravelled the first full genomes of the closest algal relatives of land plants; among the first s...

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Main Authors: Dadras, Armin, Fürst-Jansen, Janine M. R., Darienko, Tatyana, Krone, Denis, Scholz, Patricia, Sun, Siqi, Herrfurth, Cornelia, Rieseberg, Tim P., Irisarri, Iker, Steinkamp, Rasmus, Hansen, Maike, Buschmann, Henrik, Valerius, Oliver, Braus, Gerhard H., Hoecker, Ute, Feussner, Ivo, Mutwil, Marek, Ischebeck, Till, de Vries, Sophie, Lorenz, Maike, de Vries, Jan
Other Authors: School of Biological Sciences
Format: Journal Article
Language:English
Published: 2024
Subjects:
Online Access:https://hdl.handle.net/10356/174186
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author Dadras, Armin
Fürst-Jansen, Janine M. R.
Darienko, Tatyana
Krone, Denis
Scholz, Patricia
Sun, Siqi
Herrfurth, Cornelia
Rieseberg, Tim P.
Irisarri, Iker
Steinkamp, Rasmus
Hansen, Maike
Buschmann, Henrik
Valerius, Oliver
Braus, Gerhard H.
Hoecker, Ute
Feussner, Ivo
Mutwil, Marek
Ischebeck, Till
de Vries, Sophie
Lorenz, Maike
de Vries, Jan
author2 School of Biological Sciences
author_facet School of Biological Sciences
Dadras, Armin
Fürst-Jansen, Janine M. R.
Darienko, Tatyana
Krone, Denis
Scholz, Patricia
Sun, Siqi
Herrfurth, Cornelia
Rieseberg, Tim P.
Irisarri, Iker
Steinkamp, Rasmus
Hansen, Maike
Buschmann, Henrik
Valerius, Oliver
Braus, Gerhard H.
Hoecker, Ute
Feussner, Ivo
Mutwil, Marek
Ischebeck, Till
de Vries, Sophie
Lorenz, Maike
de Vries, Jan
author_sort Dadras, Armin
collection NTU
description Plant terrestrialization brought forth the land plants (embryophytes). Embryophytes account for most of the biomass on land and evolved from streptophyte algae in a singular event. Recent advances have unravelled the first full genomes of the closest algal relatives of land plants; among the first such species was Mesotaenium endlicherianum. Here we used fine-combed RNA sequencing in tandem with a photophysiological assessment on Mesotaenium exposed to a continuous range of temperature and light cues. Our data establish a grid of 42 different conditions, resulting in 128 transcriptomes and ~1.5 Tbp (~9.9 billion reads) of data to study the combinatory effects of stress response using clustering along gradients. Mesotaenium shares with land plants major hubs in genetic networks underpinning stress response and acclimation. Our data suggest that lipid droplet formation and plastid and cell wall-derived signals have denominated molecular programmes since more than 600 million years of streptophyte evolution-before plants made their first steps on land.
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spelling ntu-10356/1741862024-03-25T15:32:25Z Environmental gradients reveal stress hubs pre-dating plant terrestrialization Dadras, Armin Fürst-Jansen, Janine M. R. Darienko, Tatyana Krone, Denis Scholz, Patricia Sun, Siqi Herrfurth, Cornelia Rieseberg, Tim P. Irisarri, Iker Steinkamp, Rasmus Hansen, Maike Buschmann, Henrik Valerius, Oliver Braus, Gerhard H. Hoecker, Ute Feussner, Ivo Mutwil, Marek Ischebeck, Till de Vries, Sophie Lorenz, Maike de Vries, Jan School of Biological Sciences Medicine, Health and Life Sciences Biomass Gene regulatory network Plant terrestrialization brought forth the land plants (embryophytes). Embryophytes account for most of the biomass on land and evolved from streptophyte algae in a singular event. Recent advances have unravelled the first full genomes of the closest algal relatives of land plants; among the first such species was Mesotaenium endlicherianum. Here we used fine-combed RNA sequencing in tandem with a photophysiological assessment on Mesotaenium exposed to a continuous range of temperature and light cues. Our data establish a grid of 42 different conditions, resulting in 128 transcriptomes and ~1.5 Tbp (~9.9 billion reads) of data to study the combinatory effects of stress response using clustering along gradients. Mesotaenium shares with land plants major hubs in genetic networks underpinning stress response and acclimation. Our data suggest that lipid droplet formation and plastid and cell wall-derived signals have denominated molecular programmes since more than 600 million years of streptophyte evolution-before plants made their first steps on land. Ministry of Education (MOE) Published version We thank R. Heise for excellent technical support. J.d.V. thanks the European Research Council for funding under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 852725; ERC-StG ‘TerreStriAL’). J.d.V., U.H., I.F. and H.B. are grateful for support through the German Research Foundation (DFG), on the grant SHOAL (514060973; VR132/11-1) and within the framework of the Priority Programme ‘MAdLand – Molecular Adaptation to Land: Plant Evolution to Change’ (SPP 2237; 440231723 VR 132/4-1; BU 2301/6-1; HO 2793/5-1; FE 446/14-1), in which T.P.R. and M.H. are PhD students and A.D., J.M.R.F.-J and I.I. partake as associate members. A.D. is grateful for being supported through the International Max Planck Research School (IMPRS) for Genome Science. J.M.R.F.-J. and T.P.R. gratefully acknowledge support by the PhD programme ‘Microbiology and Biochemistry’ within the framework of the ‘Göttingen Graduate Center for Neurosciences, Biophysics, and Molecular Biosciences’ (GGNB) at the University of Goettingen. P.S. was supported by the GGNB in frame of the PRoTECT programme at the University of Goettingen. T.I. acknowledges funding from DFG (GRK 2172-PRoTECT). M.M. is supported by Singaporean Ministry of Education grant T2EP30122-0001. P.S. is grateful for support from the Studienstiftung des Deutschen Volkes. This work was further supported by the DFG through the infrastructure grant INST 211/903-1 FUGG for the used confocal microscope as operated by the Imaging Network of the University of Münster (RI_00497). 2024-03-19T02:43:03Z 2024-03-19T02:43:03Z 2023 Journal Article Dadras, A., Fürst-Jansen, J. M. R., Darienko, T., Krone, D., Scholz, P., Sun, S., Herrfurth, C., Rieseberg, T. P., Irisarri, I., Steinkamp, R., Hansen, M., Buschmann, H., Valerius, O., Braus, G. H., Hoecker, U., Feussner, I., Mutwil, M., Ischebeck, T., de Vries, S., ...de Vries, J. (2023). Environmental gradients reveal stress hubs pre-dating plant terrestrialization. Nature Plants, 9(9), 1419-1438. https://dx.doi.org/10.1038/s41477-023-01491-0 2055-026X https://hdl.handle.net/10356/174186 10.1038/s41477-023-01491-0 37640935 2-s2.0-85168920243 9 9 1419 1438 en T2EP30122-0001 Nature Plants © The Author(s) 2023. Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons. org/licenses/by/4.0/. application/pdf
spellingShingle Medicine, Health and Life Sciences
Biomass
Gene regulatory network
Dadras, Armin
Fürst-Jansen, Janine M. R.
Darienko, Tatyana
Krone, Denis
Scholz, Patricia
Sun, Siqi
Herrfurth, Cornelia
Rieseberg, Tim P.
Irisarri, Iker
Steinkamp, Rasmus
Hansen, Maike
Buschmann, Henrik
Valerius, Oliver
Braus, Gerhard H.
Hoecker, Ute
Feussner, Ivo
Mutwil, Marek
Ischebeck, Till
de Vries, Sophie
Lorenz, Maike
de Vries, Jan
Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title_full Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title_fullStr Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title_full_unstemmed Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title_short Environmental gradients reveal stress hubs pre-dating plant terrestrialization
title_sort environmental gradients reveal stress hubs pre dating plant terrestrialization
topic Medicine, Health and Life Sciences
Biomass
Gene regulatory network
url https://hdl.handle.net/10356/174186
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