Conservation of symbiotic signaling since the most recent common ancestor of land plants

Plants have colonized lands 450 million years ago. This terrestrialization was facilitated by developmental and functional innovations. Recent evo-devo approaches have demonstrated that one of these innovations was the mutualistic arbuscular mycorrhizal symbiosis (AMS). The genetic pathways that have been involved in the establishment and functioning of AMS since its evolution remain poorly described. Here, we found that intracellular colonization by AM fungi induces a transcriptional reporter of the common symbiosis pathway, well-described in angiosperms, in the liverwort <i>Marchantia paleacea</i>. Mutants of either of the three main genes of this pathway, <i>SYMRK</i>, <i>CCaMK,</i> and <i>CYCLOPS,</i> disrupt the ability of <i>M. paleacea</i> to associate with AM fungi. Finally, overexpressing gain-of-function CCaMK or CYCLOPS leads to convergent transcriptomic signatures that partially overlap with AMS. Altogether, our data indicate that plants have maintained three genes of the common symbiotic pathway to support symbiotic interactions since their most recent common ancestor.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-12-31
DOI
https://doi.org/10.1073/pnas.2408539121
Citations
20
Primary Topic
Mycorrhizal Fungi and Plant Interactions
Type
article
Field-Weighted Citation Impact
11.99

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article

Conservation of symbiotic signaling since the most recent common ancestor of land plants

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20 citations
Proceedings of the National Academy of Sciences
Mycorrhizal Fungi and Plant Interactions
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article

Conservation of symbiotic signaling since the most recent common ancestor of land plants

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article en
20 citations

Abstract

Plants have colonized lands 450 million years ago. This terrestrialization was facilitated by developmental and functional innovations. Recent evo-devo approaches have demonstrated that one of these innovations was the mutualistic arbuscular mycorrhizal symbiosis (AMS). The genetic pathways that have been involved in the establishment and functioning of AMS since its evolution remain poorly described. Here, we found that intracellular colonization by AM fungi induces a transcriptional reporter of the common symbiosis pathway, well-described in angiosperms, in the liverwort <i>Marchantia paleacea</i>. Mutants of either of the three main genes of this pathway, <i>SYMRK</i>, <i>CCaMK,</i> and <i>CYCLOPS,</i> disrupt the ability of <i>M. paleacea</i> to associate with AM fungi. Finally, overexpressing gain-of-function CCaMK or CYCLOPS leads to convergent transcriptomic signatures that partially overlap with AMS. Altogether, our data indicate that plants have maintained three genes of the common symbiotic pathway to support symbiotic interactions since their most recent common ancestor.

Proceedings of the National Academy of SciencesVol. 122(1)
Université Claude Bernard Lyon 1 (FR), École Normale Supérieure de Lyon (FR), Centre National de la Recherche Scientifique (FR), Université Toulouse III - Paul Sabatier (FR), University of Fribourg (CH), Université Fédérale de Toulouse Midi-Pyrénées (FR), Tohoku University (JP), Laboratoire de Recherche en Sciences Végétales (FR), Laboratoire Reproduction et Développement des Plantes (FR)
Agence Nationale de la Recherche, European Research Council
Life in Land
Openalex Percentile: Top 1%
Mycorrhizal Fungi and Plant Interactions
11.99
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