Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants

Abstract

Summary• The colonization of land by plants fundamentally altered environmental conditions on earth. Plant-mycorrhizal fungus symbiosis likely played a key role in this process by assisting plants to absorb water and nutrients from soil.• Here, in a diverse set of land plants, we investigated the evolutionary histories and functional conservation of three genes required for mycorrhiza formation in legumes and rice (Oryza sativa), DMI1, DMI3 and IPD3.• The genes were isolated from nearly all major plant lineages. Phylogenetic analyses showed that they had been vertically inherited since the origin of land plants. Further, cross-species mutant rescue experiments demonstrated that DMI3 genes from liverworts and hornworts could rescue Medicago truncatula dmi3 mutants for mycorrhiza formation. Yeast two-hybrid assays also showed that bryophyte DMI3 proteins could bind to downstream-acting M. trunculata IPD3 protein.Finally, molecular evolutionary analyses revealed that these genes were under purifying selection for maintenance of their ancestral functions in all mycorrhizal plant lineages.• These results indicate that the mycorrhizal genes were present in the common ancestor of land plants, and that their functions were largely conserved during land plant evolution. The evidence presented here strongly suggests that plant-mycorrhizal fungus symbiosis was one of the key processes that contributed to the origin of land flora.

Phylogenetic, structural, and functional characterization of AMT3;1, an ammonium transporter induced by mycorrhization among model grasses

“…Our results support the hypothesis of Wang et al (2010) and Delaux et al (2013) that genes that are important for AM symbiosis were already present in a common ancestor of land plants, and remained conserved in most plants until today. In M. truncatula mutants lacking MtPT4, a phosphate transporter (PHT) located in the periarbuscular membrane and essential for symbiotic Pi transport (Harrison et al 2002), arbuscules are prematurely degenerated and the symbiosis is not maintained (Javot et al 2007).…”

Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis

“…Like the rhizobium-legume symbiosis, Ca2+ oscillations were detected in dmi3 but not in dmi1 and dmi2 Medicago mutants in response to AMFs that support the hierarchical distribution of the SYM pathway with the nuclear kinase DMI3 located downstream as the decoder of the calcium spiking [24 and 30]. On the one hand, it seems evolutionary convenient that the same subset of genes, which are common in plant taxa [ 31] and have been shown to function in mycorrhizal signaling in non-legumes [ 32], could control two diverse biological systems. On the other hand, this common response again raises the problem of specificity: how do legumes distinguish between AMFs and rhizobia and organize the appropriate accommodation of the microbe inside the root tissues?…”

On plant defense signaling networks and early land plant evolution

“…While many liverworts (outlined above) and hornworts [30,31] exhibit interactions with mycorrhizal fungi, mosses generally do not form mycorrhizae [32,33]; for a recent and comprehensive overview see [29]. That mosses do not form mycorrhizae is further corroborated by Wang and colleagues [34], who showed that moss arbuscular mycorrhizal symbiosis genes show high sequence divergence as compared to their homologous counterparts in all other land plants. Yet, in light of the recently supported monophyly of the bryophytes [35], the phenomenon that mosses do not form mycorrhizae likely represents a case of secondary loss [29].…”

“…On balance, symbiosis with arbuscular mycorrhizal fungi appears to be an ancestral feature of all land plants [36]. Indeed, molecular data presented by Wang et al [34] indicate that genes associated with interactions with mycorrhizal fungi were likely present in the last common ancestor of land plants, which was corroborated by Delaux et al [18]. But what about the algal progenitors of land plants?…”