An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages

Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses...

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Published in:Nature plants Vol. 6; no. 3; pp. 280 - 289
Main Authors: Radhakrishnan, Guru V., Keller, Jean, Rich, Melanie K., Vernié, Tatiana, Mbadinga Mbadinga, Duchesse L., Vigneron, Nicolas, Cottret, Ludovic, Clemente, Hélène San, Libourel, Cyril, Cheema, Jitender, Linde, Anna-Malin, Eklund, D. Magnus, Cheng, Shifeng, Wong, Gane K. S., Lagercrantz, Ulf, Li, Fay-Wei, Oldroyd, Giles E. D., Delaux, Pierre-Marc
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01-03-2020
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Abstract Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification. An extensive phylogenomics study based on hundreds of genomes and transcriptomes provides a new interpretation of the evolution of different types of symbiotic associations in land plants, and reveals a conserved ancestral symbiosis pathway.
AbstractList Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification. An extensive phylogenomics study based on hundreds of genomes and transcriptomes provides a new interpretation of the evolution of different types of symbiotic associations in land plants, and reveals a conserved ancestral symbiosis pathway.
Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification.
Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following this founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Here, through analysis of 271 transcriptomes and 116 plant genomes spanning the entire land-plant diversity, we demonstrate that a common symbiosis signalling pathway co-evolved with intracellular endosymbioses, from the ancestral arbuscular mycorrhiza to the more recent ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. By contrast, species forming exclusively extracellular symbioses, such as ectomycorrhizae, and those forming associations with cyanobacteria, have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million yr of plant diversification. An extensive phylogenomics study based on hundreds of genomes and transcriptomes provides a new interpretation of the evolution of different types of symbiotic associations in land plants, and reveals a conserved ancestral symbiosis pathway.
Author Radhakrishnan, Guru V.
Eklund, D. Magnus
Wong, Gane K. S.
Vernié, Tatiana
Libourel, Cyril
Rich, Melanie K.
Oldroyd, Giles E. D.
Linde, Anna-Malin
Cheng, Shifeng
Cheema, Jitender
Lagercrantz, Ulf
Clemente, Hélène San
Cottret, Ludovic
Keller, Jean
Vigneron, Nicolas
Li, Fay-Wei
Delaux, Pierre-Marc
Mbadinga Mbadinga, Duchesse L.
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Snippet Plants are the foundation of terrestrial ecosystems, and their colonization of land was probably facilitated by mutualistic associations with arbuscular...
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SubjectTerms 42/44
45/23
631/1647/2217
631/181/757
631/449/2669
631/449/2676
Aquatic plants
Biological Evolution
Biomedical and Life Sciences
Cyanobacteria - physiology
Fungi - physiology
Genome, Plant
Genomes
Life Sciences
Microorganisms
Mycorrhizae
Plant diversity
Plant Physiological Phenomena
Plant Sciences
Plants - microbiology
Signal Transduction
Symbiosis
Symbiosis - physiology
Terrestrial ecosystems
Transcriptome
yanobacteria / physiology
Title An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages
URI https://link.springer.com/article/10.1038/s41477-020-0613-7
https://www.ncbi.nlm.nih.gov/pubmed/32123350
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