Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant–fungus symbioses

Abstract

SummaryFungi (Eumycota) form close associations with plants, with which they have co-existed since the dawn of life on land, but their diversity in early terrestrial ecosystems is still poorly understood.We studied petrographic sections of exceptionally well-preserved petrified plants from the 407 million yr-old Rhynie Chert (Scotland, UK). For comparative purposes, we illustrate fungal associations in four extant lower land plants.We document two new endophytes in the plant Horneophyton lignieri: Palaeoglomus boullardii (sp. nov. Glomeromycota) colonizes parenchyma in a discontinuous zone of the outer cortex of the aerial axes, forming arbuscule-like structures, vesicles and spores; Palaeoendogone gwynne-vaughaniae (gen. nov., sp. nov. Mucoromycotina) colonizes parenchyma in the basal part of the plant, where it is present in intercellular spaces and as intracellular coils but absent from rhizoids.Critical comparisons between the newly discovered Horneophyton endophytes, fungi previously described from the Rhynie Chert and fungal colonization in extant lower land plants reveal several features characteristic of both Mucoromycotina and Glomeromycota. A reappraisal of fungal associations in early land plants indicates that they are more diverse than assumed hitherto, overturning the long-held paradigm that the early endophytes were exclusively Glomeromycota.

On plant defense signaling networks and early land plant evolution

“…400-plus million-year-old Horneophyton land plant fossils have been shown to harbor glomeromycotean- and mucoromycotean-resembling structures [38]. Together with the aforementioned molecular data, this information makes a strong case for the idea that the interaction with mycorrhizal fungi is ancient.…”

The Origin and Early Evolution of Roots

“…Plants in the earliest forests (approximately 398 million years ago) already displayed an astonishing diversity of roots encompassing extinct forms and others that are comparable in many ways to those of modern gymnosperms (Stein et al, 2007;MeyerBerthaud et al, 2010;Giesen and Berry, 2013). From the outset, symbiotic associations with fungi were important (Taylor et al, 2004;Strullu-Derrien and Strullu, 2007;Bonfante and Genre, 2008), and it is clear that mycorrhizae and plant roots have coevolved in many different ways (Brundrett, 2002;Wang and Qiu, 2006;Taylor et al, 2009b;Strullu-Derrien et al, 2014). Roots and RBRSs can be observed in many geological contexts, but much recent research has focused on a handful of exceptional fossil sites in which plants were preserved in their growth positions (Stein et al, 2012) and in some in which this was also accompanied by complete soft-tissue preservation to the cellular level (Trewin and Rice, 2004).…”

Biota and palaeoenvironment of a high middle-latitude Late Triassic peat-forming ecosystem from Hopen, Svalbard archipelago

“…Recent research provides compelling evidence that fungi and fungi-like microorganisms were also important components of early terrestrial ecosystems and were actively interacting with living plants or their remains from the earliest stages of colonization of the land surface (e.g. Taylor et al 2006Taylor et al , 2015Krings et al 2007Krings et al , 2010Dotzler et al 2008;Vajda 2012;Strullu-Derrien et al 2014). Plants, animals and fungi represent the most important sources of macro-biodiversity on the planet.…”