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

Li Xue,Marcel Bucher,Izabela Fabiańska,Georgios Saridis,Juliana Almario

doi:10.1111/nph.15958

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.

Highlights

Understanding how microbial communities assemble in plant roots from a soil species pool is a central issue in microbial ecology and could affect modern breeding of climate-resilient crops with their associated microbiota (Dumbrell et al, 2010; Orrock & Watling, 2010)
Lines symrk-10, cyclops-3, ram1-1, ram12 and ram2-2 showed no arbuscule formation or only degenerated arbuscules accompanied by strongly reduced expression of LjPT4, a plant marker gene indicating functional arbuscular mycorrhizal (AM) symbiosis (Gutjahr & Parniske, 2013), while lines rad1-2 and rad1-3 showed a wild type (WT)-like AM fungal colonization level with reduced levels of LjPT4 transcripts (Fig. S2a–c)
To assess the contribution of common symbiosis signaling pathway’ (CSSP) and downstream genetic factors to the growth performance in natural soil, these mutant lines and WT were grown on an agricultural soil (‘NPK soil’; Table S2)

Summary

Introduction

Understanding how microbial communities assemble in plant roots from a soil species pool is a central issue in microbial ecology and could affect modern breeding of climate-resilient crops with their associated microbiota (Dumbrell et al, 2010; Orrock & Watling, 2010). A few symbiotic associations of land plants with soil microbes have been extensively studied mechanistically, including root nodule (RN) symbiosis with Rhizobia and Frankia bacteria in leguminous and actinorhizal plants, and the arbuscular mycorrhizal (AM) symbiosis with soil fungi from the phylum Glomeromycota in most land plants (Benson & Silvester, 1993; Parniske, 2008; Oldroyd et al, 2011). Symbiotic nutrient exchange takes place at the interface between specialized fungal tree-like cellular structures, so called arbuscules, and the host root. The accommodation of AM fungi within root cells is coordinated by a complex network of signals and plant proteins. Receptor-like kinase SYMRK/DMI2 is involved in the sensing and transduction of the fungal signal (Endre et al, 2002; Stracke et al, 2002), which triggers calcium spiking in the plant nucleus. The calcium–calmodulin-dependent protein kinase CCaMK/ DMI3 decodes the calcium signal and mediates subsequent transcriptional regulation in the nucleus (Levy et al, 2004). Forming a protein complex with CCaMK and DELLA protein, CYCLOPS/IPD3 acts as a transcriptional activator and directly regulates expression of the RAM1 gene (Pimprikar et al, 2016), encoding a GRAS transcription factor which regulates RAM2

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