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

Abstract

Plants are the foundation of terrestrial ecosystems and their colonization of land was facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that 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. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification. Introductory paragraphSince they colonized land 450 million years ago, plants have been the foundation of most terrestrial ecosystems 1 . Such successful colonization occurred only once in the plant kingdom and was supported by the symbiotic association formed with arbuscular mycorrhizal fungi 2,3 . Following that founding event, plant diversification was accompanied by the emergence of alternative or additional symbionts 4 . Among alternative symbioses, the association between orchids and basidiomycetes and between Ericales and ascomycetes or basidiomycetes are two endosymbioses with specific intracellular structures in two plant lineages that lost the ability to form the Arbuscular Mycorrhizal Symbiosis (AMS) 5 . As such, orchid mycorrhiza and ericoid-mycorrhiza represent two clear symbiosis switches, whereby intracellular associations are sustained, but the nature of the symbionts are radically different. Similarly, within the liverworts, the Jungermanniales engage in ericoid-like endosymbioses but not AM symbiosis and represent another symbiont switch that occurred during plant evolution 6 . Other symbioses can occur simultaneously with AMS, for example the root nodule symbiosis, an association with nitrogen-fixing bacteria that evolved in the last common ancestor of Fabales, Fagales, Cucurbitales and Rosales 7 . Another example is ectomycorrhizae, an extracellular symbiosis found in several gymnosperm and angiosperm lineages: in some lineages both AMS and ectomycorrhizae have been retained; while other lineages have switched from AMS to ectomycorrhizae 8 . Finally, associations with cyanobacteria, which occur only in the intercellular spaces of the plant tissue, can be found in diverse species within the embryophytes, in hornworts, liverworts, ferns, gymnosperms and angiosperms 9 . Despite the improved nutrient acquisition afforded to plants by these different types of mutualistic symbioses, e...

The genome of Geosiphon pyriformis reveals ancestral traits linked to the emergence of the arbuscular mycorrhizal symbiosis

“…Comparative phylogenomics could be used to understand the evolution of AMS [7,8]. However, the availability of genome data covering basal AMF phylogenetic nodes (Archaeosporales, Paraglomerales) is presently based on fragmentary protein coding datasets [9].…”

Gamete expression of TALE class HD genes activates the diploid sporophyte program in Marchantia polymorpha

“…Predicted TALE HD sequences were assembled from land plants, charophytes and Chlorophytes, via Genbank or additional sources as detailed below. Gymnosperm sequences were obtained from Congenie (congenie.org), fern sequences from Equisetum and Azolla transcriptomes (de Vries et al, 2016, Vanneste et al, 2015, bryophyte sequences, other than M. polymorpha (Phytozome) and P. patens (Genbank), from available transcriptomes (Wickett et al, 2014, Dong et al, 2019, Radhakrishnan et al, 2020, Klebsormidium and Caulerpa sequences derived from genome sequences (Hori et al, 2014, Arimoto et al, 2019, and other charophyte and Chlorophyte sequences from Genbank and additional transcriptomes Delwiche, 2016, Ju et al, 2015).…”

Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system

“…Predicted orthologs of M. polymorpha gametolog were collected from available liverwort genome and transcriptome sequence data. [82][83][84][85][86] Since the available liverwort transcriptomes were not generated to investigate sex chromosome evolution, we initially applied two filters. First, sequences derived from monooicous species were removed as monoicy is associated with a loss of sex chromosomes.…”