Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Xuehuan Feng; Jinfang Zheng; Iker Irisarri; Huihui Yu; Bo Zheng; Zahin Ali; Sophie de Vries; Jean Keller; Janine M.R. Fürst-Jansen; Armin Dadras; Jaccoline M.S. Zegers; Tim P. Rieseberg; Amra Dhabalia Ashok; Tatyana Darienko; Maaike J. Bierenbroodspot; Lydia Gramzow; Romy Petroll; Fabian B. Haas; Noe Fernandez-Pozo; Orestis Nousias; Tang Li; Elisabeth Fitzek; W. Scott Grayburn; Nina Rittmeier; Charlotte Permann; Florian Rümpler; John M. Archibald; Günter Theißen; Jeffrey P. Mower; Maike Lorenz; Henrik Buschmann; Klaus von Schwartzenberg; Lori Boston; Richard D. Hayes; Chris Daum; Kerrie Barry; Igor V. Grigoriev; Xiyin Wang; Fay Wei Li; Stefan A. Rensing; Julius Ben Ari; Noa Keren; Assaf Mosquna; Andreas Holzinger; Pierre Marc Delaux; Chi Zhang; Jinling Huang; Marek Mutwil; Jan de Vries; Yanbin Yin

doi:10.1038/s41588-024-01737-3

Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Xuehuan Feng, Jinfang Zheng, Iker Irisarri, Huihui Yu, Bo Zheng, Zahin Ali, Sophie de Vries, Jean Keller, Janine M.R. Fürst-Jansen, Armin Dadras, Jaccoline M.S. Zegers, Tim P. Rieseberg, Amra Dhabalia Ashok, Tatyana Darienko, Maaike J. Bierenbroodspot, Lydia Gramzow, Romy Petroll, Fabian B. Haas, Noe Fernandez-Pozo, Orestis NousiasTang Li, Elisabeth Fitzek, W. Scott Grayburn, Nina Rittmeier, Charlotte Permann, Florian Rümpler, John M. Archibald, Günter Theißen, Jeffrey P. Mower, Maike Lorenz, Henrik Buschmann, Klaus von Schwartzenberg, Lori Boston, Richard D. Hayes, Chris Daum, Kerrie Barry, Igor V. Grigoriev, Xiyin Wang, Fay Wei Li, Stefan A. Rensing, Julius Ben Ari, Noa Keren, Assaf Mosquna, Andreas Holzinger, Pierre Marc Delaux, Chi Zhang, Jinling Huang, Marek Mutwil, Jan de Vries^*, Yanbin Yin^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Zygnematophyceae are the algal sisters of land plants. Here we sequenced four genomes of filamentous Zygnematophyceae, including chromosome-scale assemblies for three strains of Zygnema circumcarinatum. We inferred traits in the ancestor of Zygnematophyceae and land plants that might have ushered in the conquest of land by plants: expanded genes for signaling cascades, environmental response, and multicellular growth. Zygnematophyceae and land plants share all the major enzymes for cell wall synthesis and remodifications, and gene gains shaped this toolkit. Co-expression network analyses uncover gene cohorts that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.

Original language	English
Pages (from-to)	1018-1031
Number of pages	14
Journal	Nature Genetics
Volume	56
Issue number	5
DOIs	https://doi.org/10.1038/s41588-024-01737-3
State	Published - May 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Access to Document

10.1038/s41588-024-01737-3

Cite this

Feng, X., Zheng, J., Irisarri, I., Yu, H., Zheng, B., Ali, Z., de Vries, S., Keller, J., Fürst-Jansen, J. M. R., Dadras, A., Zegers, J. M. S., Rieseberg, T. P., Dhabalia Ashok, A., Darienko, T., Bierenbroodspot, M. J., Gramzow, L., Petroll, R., Haas, F. B., Fernandez-Pozo, N., ... Yin, Y. (2024). Genomes of multicellular algal sisters to land plants illuminate signaling network evolution. Nature Genetics, 56(5), 1018-1031. https://doi.org/10.1038/s41588-024-01737-3

@article{90cb815d11564a1a847aaca6cbc0b5ca,

title = "Genomes of multicellular algal sisters to land plants illuminate signaling network evolution",

abstract = "Zygnematophyceae are the algal sisters of land plants. Here we sequenced four genomes of filamentous Zygnematophyceae, including chromosome-scale assemblies for three strains of Zygnema circumcarinatum. We inferred traits in the ancestor of Zygnematophyceae and land plants that might have ushered in the conquest of land by plants: expanded genes for signaling cascades, environmental response, and multicellular growth. Zygnematophyceae and land plants share all the major enzymes for cell wall synthesis and remodifications, and gene gains shaped this toolkit. Co-expression network analyses uncover gene cohorts that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.",

author = "Xuehuan Feng and Jinfang Zheng and Iker Irisarri and Huihui Yu and Bo Zheng and Zahin Ali and {de Vries}, Sophie and Jean Keller and F{\"u}rst-Jansen, {Janine M.R.} and Armin Dadras and Zegers, {Jaccoline M.S.} and Rieseberg, {Tim P.} and {Dhabalia Ashok}, Amra and Tatyana Darienko and Bierenbroodspot, {Maaike J.} and Lydia Gramzow and Romy Petroll and Haas, {Fabian B.} and Noe Fernandez-Pozo and Orestis Nousias and Tang Li and Elisabeth Fitzek and Grayburn, {W. Scott} and Nina Rittmeier and Charlotte Permann and Florian R{\"u}mpler and Archibald, {John M.} and G{\"u}nter Thei{\ss}en and Mower, {Jeffrey P.} and Maike Lorenz and Henrik Buschmann and {von Schwartzenberg}, Klaus and Lori Boston and Hayes, {Richard D.} and Chris Daum and Kerrie Barry and Grigoriev, {Igor V.} and Xiyin Wang and Li, {Fay Wei} and Rensing, {Stefan A.} and {Ben Ari}, Julius and Noa Keren and Assaf Mosquna and Andreas Holzinger and Delaux, {Pierre Marc} and Chi Zhang and Jinling Huang and Marek Mutwil and {de Vries}, Jan and Yanbin Yin",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = may,

doi = "10.1038/s41588-024-01737-3",

language = "אנגלית",

volume = "56",

pages = "1018--1031",

journal = "Nature Genetics",

issn = "1061-4036",

publisher = "Nature Publishing Group",

number = "5",

}

Feng, X, Zheng, J, Irisarri, I, Yu, H, Zheng, B, Ali, Z, de Vries, S, Keller, J, Fürst-Jansen, JMR, Dadras, A, Zegers, JMS, Rieseberg, TP, Dhabalia Ashok, A, Darienko, T, Bierenbroodspot, MJ, Gramzow, L, Petroll, R, Haas, FB, Fernandez-Pozo, N, Nousias, O, Li, T, Fitzek, E, Grayburn, WS, Rittmeier, N, Permann, C, Rümpler, F, Archibald, JM, Theißen, G, Mower, JP, Lorenz, M, Buschmann, H, von Schwartzenberg, K, Boston, L, Hayes, RD, Daum, C, Barry, K, Grigoriev, IV, Wang, X, Li, FW, Rensing, SA, Ben Ari, J, Keren, N, Mosquna, A, Holzinger, A, Delaux, PM, Zhang, C, Huang, J, Mutwil, M, de Vries, J & Yin, Y 2024, 'Genomes of multicellular algal sisters to land plants illuminate signaling network evolution', Nature Genetics, vol. 56, no. 5, pp. 1018-1031. https://doi.org/10.1038/s41588-024-01737-3

TY - JOUR

T1 - Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

AU - Feng, Xuehuan

AU - Zheng, Jinfang

AU - Irisarri, Iker

AU - Yu, Huihui

AU - Zheng, Bo

AU - Ali, Zahin

AU - de Vries, Sophie

AU - Keller, Jean

AU - Fürst-Jansen, Janine M.R.

AU - Dadras, Armin

AU - Zegers, Jaccoline M.S.

AU - Rieseberg, Tim P.

AU - Dhabalia Ashok, Amra

AU - Darienko, Tatyana

AU - Bierenbroodspot, Maaike J.

AU - Gramzow, Lydia

AU - Petroll, Romy

AU - Haas, Fabian B.

AU - Fernandez-Pozo, Noe

AU - Nousias, Orestis

AU - Li, Tang

AU - Fitzek, Elisabeth

AU - Grayburn, W. Scott

AU - Rittmeier, Nina

AU - Permann, Charlotte

AU - Rümpler, Florian

AU - Archibald, John M.

AU - Theißen, Günter

AU - Mower, Jeffrey P.

AU - Lorenz, Maike

AU - Buschmann, Henrik

AU - von Schwartzenberg, Klaus

AU - Boston, Lori

AU - Hayes, Richard D.

AU - Daum, Chris

AU - Barry, Kerrie

AU - Grigoriev, Igor V.

AU - Wang, Xiyin

AU - Li, Fay Wei

AU - Rensing, Stefan A.

AU - Ben Ari, Julius

AU - Keren, Noa

AU - Mosquna, Assaf

AU - Holzinger, Andreas

AU - Delaux, Pierre Marc

AU - Zhang, Chi

AU - Huang, Jinling

AU - Mutwil, Marek

AU - de Vries, Jan

AU - Yin, Yanbin

PY - 2024/5

Y1 - 2024/5

N2 - Zygnematophyceae are the algal sisters of land plants. Here we sequenced four genomes of filamentous Zygnematophyceae, including chromosome-scale assemblies for three strains of Zygnema circumcarinatum. We inferred traits in the ancestor of Zygnematophyceae and land plants that might have ushered in the conquest of land by plants: expanded genes for signaling cascades, environmental response, and multicellular growth. Zygnematophyceae and land plants share all the major enzymes for cell wall synthesis and remodifications, and gene gains shaped this toolkit. Co-expression network analyses uncover gene cohorts that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.

AB - Zygnematophyceae are the algal sisters of land plants. Here we sequenced four genomes of filamentous Zygnematophyceae, including chromosome-scale assemblies for three strains of Zygnema circumcarinatum. We inferred traits in the ancestor of Zygnematophyceae and land plants that might have ushered in the conquest of land by plants: expanded genes for signaling cascades, environmental response, and multicellular growth. Zygnematophyceae and land plants share all the major enzymes for cell wall synthesis and remodifications, and gene gains shaped this toolkit. Co-expression network analyses uncover gene cohorts that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.

UR - http://www.scopus.com/inward/record.url?scp=85191978305&partnerID=8YFLogxK

U2 - 10.1038/s41588-024-01737-3

DO - 10.1038/s41588-024-01737-3

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

C2 - 38693345

AN - SCOPUS:85191978305

SN - 1061-4036

VL - 56

SP - 1018

EP - 1031

JO - Nature Genetics

JF - Nature Genetics

IS - 5

ER -

Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this