Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus

Abstract

Summary Most land plants establish mutualistic interactions with arbuscular mycorrhizal (AM) fungi. Intracellular accommodation of AM fungal symbionts remodels important host traits like root morphology and nutrient acquisition. How mycorrhizal colonization impacts plant microbiota is unclear. To understand the impact of AM symbiosis on fungal microbiota, ten Lotus japonicus mutants impaired at different stages of AM formation were grown in non‐sterile natural soil and their root‐associated fungal communities were studied. Plant mutants lacking the capacity to form mature arbuscules (arb−) exhibited limited growth performance associated with altered phosphorus (P) acquisition and reduction–oxidation (redox) processes. Furthermore, arb− plants assembled moderately but consistently different root‐associated fungal microbiota, characterized by the depletion of Glomeromycota and the concomitant enrichment of Ascomycota, including Dactylonectria torresensis. Single and co‐inoculation experiments showed a strong reduction of root colonization by D. torresensis in the presence of AM fungus Rhizophagus irregularis, particularly in arbuscule‐forming plants. Our results suggest that impairment of central symbiotic functions in AM host plants leads to specific changes in root microbiomes and in tripartite interactions between the host plant, AM and non‐AM fungi. This lays the foundation for mechanistic studies on microbe–microbe and microbe–host interactions in AM symbiosis of the model L. japonicus.

Neighboring plants divergently modulate effects of loss-of-function in maize mycorrhizal phosphate uptake on host physiology and root fungal microbiota

“…Previously, a statistically significant small effect of the development of functional arbuscules on root fungal communities was observed in the legume Lotus japonicus, in which depletion of Glomeromycotina OTUs in roots resulted in increased abundance of Ascomycota fungal species e.g. belonging to the orders Hypocreales and Helotiales [42,43]. In these studies mutants affected in genes acting upstream of mycorrhiza-dependent Pi transport were explored.…”

“…However, how maize mycorrhizal microbial community homeostasis is affected by functional AM symbiosis traits is elusive. Recent studies performed with mycorrhizal Lotus japonicus mutants disrupted in the common symbiosis signaling pathway (CSSP) or downstream processes showed that an almost complete depletion of Glomeromycotina taxa and impaired arbuscule formation in roots were accompanied by an enrichment of few Ascomycota fungi and shifts in bacterial communities under greenhouse conditions [42,43]. On the other hand, knocking out CSSP genes didn´t affect the life cycle of the growth-promoting basidiomycete fungus Piriformospora indica (also known as Serendipita indica) in L. japonicus nor did silencing of CCaMK affect bacterial or fungal communities in roots of field-grown Nicotiana attenuata [44,45].…”

The genetic architecture of host response reveals the importance of arbuscular mycorrhizae to maize cultivation

“…It has been shown that certain bacterial taxa exert beneficial and synergistic effects on AM symbiosis, acting as so-called ‘mycorrhiza helpers’ ( Frey-Klett et al, 2007 ; van der Heijden et al, 2016 ; Ferreira et al, 2020 ). In Lotus japonicus , disruption of the AM symbiosis impacts other members of the root-associated microbial community ( Xue et al, 2019 ). Characterization of the root microbiome of AMF-S and AMF-R families will provide insight into the interplay between AMF, the broader microbial community, and host response.…”

Stéphane Hacquard

“…In the second article, Xue et al . () used Lotus japonicus mutants impaired at different stages of AM formation to investigate the role of the AM symbiosis pathway and AM fungi on the structure of root‐associated fungal communities. They found that roots of L. japonicus mutants perturbed in AM symbiosis largely lack AM fungi and assemble ‘abnormal’ fungal consortia when grown in natural soils.…”