Morpho-anatomical differences among mycoheterotrophic Afrothismia spp. (Thismiaceae) indicate an evolutionary progression towards improved mycorrhizal benefit

Stephan Imhof,Anna Heser,Benjamin Feller

doi:10.1007/s00572-020-00951-1

Abstract

Achlorophyllous, mycoheterotrophic plants depend on their mycorrhizal fungi for 100% of their carbon supply. Hence, there is strong evolutionary pressure towards a well-organized functioning of the association from the plant’s perspective. Members of the mycoheterotrophic genus Afrothismia have evolved elaborate fungal colonization patterns allowing a sustained benefit from external fungal penetration events. On the basis of anatomical details of the root-shoot systems of A. korupensis and A. hydra, we elucidate an evolutionary progression between the comparatively simple mycorrhizal pattern in A. gesnerioides and the so far most complex mycorrhiza in A. saingei. We detected two major advancements: (1) two species, A. korupensis and A. saingei, use the fungus itself as energy storage, replacing starch depositions used by A. gesnerioides and A. hydra, and (2) the morphological complexity of hyphal forms in plant tissue compartments increases from A. gesnerioides to A. saingei. We discuss the omitting of starch metabolism as well as the morpho-anatomical differences as an evolutionary fine-tuning of the compartmented mycorrhizal organization in Afrothismia. Our results support the idea of a taxonomic distinction between Afrothismia and other Thismiaceae.

Highlights

Mycoheterotrophic plants (MHP; Leake 1994) depend on their mycorrhizal fungus for water and nutrients and for 100% of their carbon supply
The morphology of root fungi in Afrothismia has been interpreted as a complex morphotype of a Paris-type arbuscular mycorrhiza (AM, Imhof 1999a, 2006); its identity as an AM fungus was later corroborated by molecular methods (Franke et al 2006; Merckx and Bidartondo 2008; Merckx et al 2012)
The fungi found in Afrothismia spp. belong to only one (IN A. hydra, A. korupensis, A. saingei) or to three (IN A. gesnerioides) virtual taxa from the Glomeraceae

Summary

Introduction

Mycoheterotrophic plants (MHP; Leake 1994) depend on their mycorrhizal fungus for water and nutrients and for 100% of their carbon supply This essential dependency should increase the evolutionary pressure towards a wellorganized mycorrhiza in MHP. Most MHP have mycorrhizal colonization patterns that achieve a sustained use of the fungus by the plant even with few colonization events (e.g., Gentianaceae, Imhof 1997; Triuridaceae, Imhof 1998; Burmanniaceae, Imhof 2001) This is realized by anatomical compartmentalization: tissues. In A. saingei (Franke 2004), the rootshoot combination harbors one of the most complex mycorrhizal colonization patterns described to date It shows four different hyphal shapes (straight, looped, inflated coils, degenerating coils) in six separate tissue compartments (filiform root, root epidermis, third root layer, root cortex parenchyma, shoot cortex at root clusters, shoot cortex apart from root clusters). The mycorrhizal pattern in A. gesnerioides is comparatively simple, with three hyphal forms in five tissue compartments (Imhof 2006; see Table 1)

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Conclusion