The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment

Chloé Beaulieu; Cyril Libourel; Duchesse Lacourt Mbadinga Zamar; Karima El Mahboubi; David J. Hoey; George R. L. Greiff; Jean Keller; Camille Girou; Helene San Clemente; Issa Diop; Emilie Amblard; Baptiste Castel; Anthony Théron; Stéphane Cauet; Nathalie Rodde; Sabine Zachgo; Wiebke Halpape; Anja Meierhenrich; Bianca Laker; Andrea Bräutigam; Peter Szovenyi; Shifeng Cheng; Yasuhiro Tanizawa; Simon Aziz; James H. Leebens-Mack; Jeremy Schmutz; Jenell Webber; Jane Grimwood; Christophe Jacquet; Christophe Dunand; Jessica M. Nelson; Fabrice Roux; Hervé Philippe; Sebastian Schornack; Maxime Bonhomme; Pierre-Marc Delaux

doi:10.1038/s41588-024-02071-4

The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment

Chloé Beaulieu, Cyril Libourel, Duchesse Lacourt Mbadinga Zamar, Karima El Mahboubi, David J. Hoey, George R. L. Greiff, Jean Keller, Camille Girou, Helene San Clemente, Issa Diop, Emilie Amblard, Baptiste Castel, Anthony Théron, Stéphane Cauet, Nathalie Rodde, Sabine Zachgo, Wiebke Halpape, Anja Meierhenrich, Bianca Laker, Andrea BräutigamPeter Szovenyi, Shifeng Cheng, Yasuhiro Tanizawa, Simon Aziz, James H. Leebens-Mack, Jeremy Schmutz, Jenell Webber, Jane Grimwood, Christophe Jacquet, Christophe Dunand, Jessica M. Nelson, Fabrice Roux, Hervé Philippe, Sebastian Schornack, Maxime Bonhomme^*, Pierre-Marc Delaux^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

3 Citations (Scopus)

Abstract

Plant adaptation to terrestrial life started 450 million years ago and has played a major role in the evolution of life on Earth. The genetic mechanisms allowing this adaptation to a diversity of terrestrial constraints have been mostly studied by focusing on flowering plants. Here, we gathered a collection of 133 accessions of the model bryophyte Marchantia polymorpha and studied its intraspecific diversity using selection signature analyses, a genome–environment association study and a pangenome. We identified adaptive features, such as peroxidases or nucleotide-binding and leucine-rich repeats (NLRs), also observed in flowering plants, likely inherited from the first land plants. The M. polymorpha pangenome also harbors lineage-specific accessory genes absent from seed plants. We conclude that different land plant lineages still share many elements from the genetic toolkit evolved by their most recent common ancestor to adapt to the terrestrial habitat, refined by lineage-specific polymorphisms and gene family evolution.

Original language	English
Article number	eaba6605
Pages (from-to)	729-740
Number of pages	12
Journal	Nature Genetics
Volume	57
Issue number	3
Early online date	17 Feb 2025
DOIs	https://doi.org/10.1038/s41588-024-02071-4
Publication status	Published - 1 Mar 2025

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Beaulieu, C., Libourel, C., Mbadinga Zamar, D. L., El Mahboubi, K., Hoey, D. J., Greiff, G. R. L., Keller, J., Girou, C., San Clemente, H., Diop, I., Amblard, E., Castel, B., Théron, A., Cauet, S., Rodde, N., Zachgo, S., Halpape, W., Meierhenrich, A., Laker, B., ... Delaux, P.-M. (2025). The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment. Nature Genetics, 57(3), 729-740. Article eaba6605. https://doi.org/10.1038/s41588-024-02071-4

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title = "The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment",

abstract = "Plant adaptation to terrestrial life started 450 million years ago and has played a major role in the evolution of life on Earth. The genetic mechanisms allowing this adaptation to a diversity of terrestrial constraints have been mostly studied by focusing on flowering plants. Here, we gathered a collection of 133 accessions of the model bryophyte Marchantia polymorpha and studied its intraspecific diversity using selection signature analyses, a genome–environment association study and a pangenome. We identified adaptive features, such as peroxidases or nucleotide-binding and leucine-rich repeats (NLRs), also observed in flowering plants, likely inherited from the first land plants. The M. polymorpha pangenome also harbors lineage-specific accessory genes absent from seed plants. We conclude that different land plant lineages still share many elements from the genetic toolkit evolved by their most recent common ancestor to adapt to the terrestrial habitat, refined by lineage-specific polymorphisms and gene family evolution.",

author = "Chlo{\'e} Beaulieu and Cyril Libourel and {Mbadinga Zamar}, {Duchesse Lacourt} and {El Mahboubi}, Karima and Hoey, {David J.} and Greiff, {George R. L.} and Jean Keller and Camille Girou and {San Clemente}, Helene and Issa Diop and Emilie Amblard and Baptiste Castel and Anthony Th{\'e}ron and St{\'e}phane Cauet and Nathalie Rodde and Sabine Zachgo and Wiebke Halpape and Anja Meierhenrich and Bianca Laker and Andrea Br{\"a}utigam and Peter Szovenyi and Shifeng Cheng and Yasuhiro Tanizawa and Simon Aziz and Leebens-Mack, {James H.} and Jeremy Schmutz and Jenell Webber and Jane Grimwood and Christophe Jacquet and Christophe Dunand and Nelson, {Jessica M.} and Fabrice Roux and Herv{\'e} Philippe and Sebastian Schornack and Maxime Bonhomme and Pierre-Marc Delaux",

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Beaulieu, C, Libourel, C, Mbadinga Zamar, DL, El Mahboubi, K, Hoey, DJ, Greiff, GRL, Keller, J, Girou, C, San Clemente, H, Diop, I, Amblard, E, Castel, B, Théron, A, Cauet, S, Rodde, N, Zachgo, S, Halpape, W, Meierhenrich, A, Laker, B, Bräutigam, A, Szovenyi, P, Cheng, S, Tanizawa, Y, Aziz, S, Leebens-Mack, JH, Schmutz, J, Webber, J, Grimwood, J, Jacquet, C, Dunand, C, Nelson, JM, Roux, F, Philippe, H, Schornack, S, Bonhomme, M & Delaux, P-M 2025, 'The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment', Nature Genetics, vol. 57, no. 3, eaba6605, pp. 729-740. https://doi.org/10.1038/s41588-024-02071-4

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T1 - The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment

AU - Beaulieu, Chloé

AU - Libourel, Cyril

AU - Mbadinga Zamar, Duchesse Lacourt

AU - El Mahboubi, Karima

AU - Hoey, David J.

AU - Greiff, George R. L.

AU - Keller, Jean

AU - Girou, Camille

AU - San Clemente, Helene

AU - Diop, Issa

AU - Amblard, Emilie

AU - Castel, Baptiste

AU - Théron, Anthony

AU - Cauet, Stéphane

AU - Rodde, Nathalie

AU - Zachgo, Sabine

AU - Halpape, Wiebke

AU - Meierhenrich, Anja

AU - Laker, Bianca

AU - Bräutigam, Andrea

AU - Szovenyi, Peter

AU - Cheng, Shifeng

AU - Tanizawa, Yasuhiro

AU - Aziz, Simon

AU - Leebens-Mack, James H.

AU - Schmutz, Jeremy

AU - Webber, Jenell

AU - Grimwood, Jane

AU - Jacquet, Christophe

AU - Dunand, Christophe

AU - Nelson, Jessica M.

AU - Roux, Fabrice

AU - Philippe, Hervé

AU - Schornack, Sebastian

AU - Bonhomme, Maxime

AU - Delaux, Pierre-Marc

PY - 2025/3/1

Y1 - 2025/3/1

N2 - Plant adaptation to terrestrial life started 450 million years ago and has played a major role in the evolution of life on Earth. The genetic mechanisms allowing this adaptation to a diversity of terrestrial constraints have been mostly studied by focusing on flowering plants. Here, we gathered a collection of 133 accessions of the model bryophyte Marchantia polymorpha and studied its intraspecific diversity using selection signature analyses, a genome–environment association study and a pangenome. We identified adaptive features, such as peroxidases or nucleotide-binding and leucine-rich repeats (NLRs), also observed in flowering plants, likely inherited from the first land plants. The M. polymorpha pangenome also harbors lineage-specific accessory genes absent from seed plants. We conclude that different land plant lineages still share many elements from the genetic toolkit evolved by their most recent common ancestor to adapt to the terrestrial habitat, refined by lineage-specific polymorphisms and gene family evolution.

AB - Plant adaptation to terrestrial life started 450 million years ago and has played a major role in the evolution of life on Earth. The genetic mechanisms allowing this adaptation to a diversity of terrestrial constraints have been mostly studied by focusing on flowering plants. Here, we gathered a collection of 133 accessions of the model bryophyte Marchantia polymorpha and studied its intraspecific diversity using selection signature analyses, a genome–environment association study and a pangenome. We identified adaptive features, such as peroxidases or nucleotide-binding and leucine-rich repeats (NLRs), also observed in flowering plants, likely inherited from the first land plants. The M. polymorpha pangenome also harbors lineage-specific accessory genes absent from seed plants. We conclude that different land plant lineages still share many elements from the genetic toolkit evolved by their most recent common ancestor to adapt to the terrestrial habitat, refined by lineage-specific polymorphisms and gene family evolution.

U2 - 10.1038/s41588-024-02071-4

DO - 10.1038/s41588-024-02071-4

M3 - Article (Academic Journal)

C2 - 39962240

SN - 1061-4036

VL - 57

SP - 729

EP - 740

JO - Nature Genetics

JF - Nature Genetics

IS - 3

M1 - eaba6605

ER -

The Marchantia polymorpha pangenome reveals ancient mechanisms of plant adaptation to the environment

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