Origins of the terrestrial flora: A symbiosis with fungi?

Abstract

Abstract. Land phototrophs need to exploit both atmosphere (providing gas and light) and substrate (furnishing water and minerals). Yet, their algal ancestors were poorly preadapted to such a life at the interface. We review the paleontological evidence that fungal symbioses which can exploit substrate resources, helped adaptation to land constraints. Diverse structures dating back to the Devonian present convincing evidence for lichens, (symbioses between fungi and microscopic algae) but fossils remain scarce, so that early lichen abundance and ecological relevance remain questionable. Several enigmatic but abundant fossils from the Siluro-Devonian, such as Spongiophyton or the giant Prototaxites (Nematophytes), likely represent fungus-algal symbioses, which shaped early terrestrial ecosystems. Yet, these taxa are fully extinct, and do not have clear affinities with extant groups. Finally, terrestrialization of Embryophyta (land plants), which currently dominate land ecosystems, is linked to a symbiosis with Glomeromycetes. Today, these fungi form arbuscular mycorrhizae, which help most Embryophyta to exploit soil, and molecular data combined with paleontological evidence support the idea that this type of association is ancestral. The role of symbiotic Mucoromycetes during terrestrialization is not fully understood and mycorrhizal association diversified later in the evolution of Embryophyta. Fungal-algal symbioses thus recurrently contributed to terrestrialization of phototrophs.

Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi

“…Considerable uncertainties also remain regarding the timing of the divergence of Mucoromycota, hitherto estimated to pre‐date the origin of land plants by some 100 million yr (Berbee et al ., ) and of the emergence of embryophytes, with latest estimates placing this major event earlier than generally assumed, in a middle Cambrian–Early Ordovician interval (Morris et al ., ). Given these large uncertainties, four evolutionary scenarios remain probable: (1) Glomeromycotina as the ancestral type (Mondo et al ., ; Chang et al ., ; Spatafora et al ., ); (2) Mucoromycotina as the ancestral type (Bidartondo et al ., ; Field et al ., 2015b); (3) dual colonisations involving both fungal subphyla as the ancestral type (Rimington et al ., ; Field et al ., 2016a); and (4) symbiotic interactions between the common ancestor of Mucoromycota and early land plants, or even their algal ancestors (Selosse & Strullu‐Derrien, ; Feijen et al ., ).…”

Plants, fungi and oomycetes: a 400‐million year affair that shapes the biosphere

“…The emergence of land plants is often viewed as a symbiosis between a green alga with photosynthetic abilities that is unable to access water and minerals in the substrate, and a heterotrophic fungus predisposed to exploit soil resources (e.g. Selosse & Le Tacon, ; Selosse & Strullu‐Derrien, ). Lichens have existed since the Devonian (Honegger et al ., ), but their apparent low frequency in the fossil record has argued against a major role during terrestrialization.…”

The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics

“…Also, some species have been misattributed: the fungus commonly known as ‘ Glomus tenue ’ might belong to Mucoromycotina (Orchard et al ., ). Both groups of fungi appear to be implicated in the early colonization of the land by plants, and it might be that terrestrialization involved an ancestral group from which Glomeromycotina and Mucoromycotina later diverged (Selosse & Strullu‐Derrien, ; Field et al ., ). The idea that some early Paleozoic endomycorrhizas were formed by stem group Glomeromycotina and Mucoromycotina is consistent with a cross‐species mutant rescue experiment (Wang et al ., ), where genes from Mucoromycota‐associated liverworts can rescue AM formation in Medicago , suggesting that aspects of the CMm and AM symbioses share a common origin.…”