Abstract
Mycorrhizal symbiosis between soil fungi and land plants is one of the most widespread and ecologically important mutualisms on earth. It has long been hypothesized that the Glomeromycotina, the mycorrhizal symbionts of the majority of plants, facilitated colonization of land by plants in the Ordovician. This view was recently challenged by the discovery of mycorrhiza-like associations with Mucoromycotina in several early diverging lineages of land plants. Utilizing a large, species-level database of plants’ mycorrhiza-like associations and a Bayesian approach to state transition dynamics we here show that the recruitment of Mucoromycotina is the best supported transition from a non-mycorrhizal state. We further found that transitions between different combinations of either or both of Mucoromycotina and Glomeromycotina occur at high rates, and found similar promiscuity among combinations that include either or both of Glomeromycotina and Ascomycota with a nearly fixed association with Basidiomycota. Our results portray an evolutionary scenario of evolution of mycorrhizal symbiosis with a prominent role for Mucoromycotina in the early stages of land plant diversification.
Highlights
Land plants diverged from aquatic algae in the Neoproterozoic as a lineage that would eventually undergo the ecological transition to terrestrial life[1,2]
The great majority of land plants associate with arbuscular mycorrhizal fungi from the Mucoromycota subphylum Glomeromycotina, while other types of symbiotic associations, such as ectomycorrhiza, ericoid mycorrhiza, and orchid mycorrhiza, are formed by fungi of the Basidiomycota or Ascomycota[9]
Fossil evidence suggests that Glomeromycotina have coevolved with land plants for at least 407 Myr, as vesicles, spores, intracellular coils, and arbuscule-like structures resembling extant symbiotic colonizations were found in Rhynie Chert fossils of Horneophyton lignieri[11]
Summary
Land plants diverged from aquatic algae in the Neoproterozoic as a lineage that would eventually undergo the ecological transition to terrestrial life[1,2]. Further support for ancient origin of these interactions comes from genomics, as genes involved in the formation of arbuscular mycorrhizal colinizations are homologs and were acquired in a stepwise manner, with potentiation starting as early as the last common ancestor of Charophytes and Embryophytes[12,13,14] This evidence has led to the wide acceptance of the view that Glomeromycotina were the ancestral mycorrhizal symbionts of land plants[15,16]. Facilitated terrestrialisation[16], or that early land plants formed dual Mucoromycotina-Glomeromycotina partnerships[18,19,20,21] After this discovery, Rhynie Chert fossils where re-evaluated, revealing mycorrhiza-like colonizations resembling both Glomeromycotina and Mucoromycotina[11]. Considering the uncertainty of the evolutionary relationships of early Embryophytes[24,25], we assessed the probability of all possible combinations of mycorrhizal associations for the most recent common ancestor of land plants
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