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Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants.

ABSTRACT: Plants associate through their roots with fungal assemblages that impact their abundance and productivity. Non-mycorrhizal endophytes constitute an important component of such fungal diversity, but their implication in ecosystem processes is little known. Using a selection of 128 root-endophytic strains, we defined functional groups based on their traits and plant interactions with potential to predict community assembly and symbiotic association processes. In vitro tests of the strains' interactions with Arabidopsis thaliana, Microthlaspi erraticum and Hordeum vulgare showed a net negative effect of fungal colonization on plant growth. The effects partly depended on the phylogenetic affiliation of strains, but also varied considerably depending on the plant-strain combination. The variation was partly explained by fungal traits shared by different lineages, like growth rates or melanization. The origin of strains also affected their symbioses, with endophytes isolated from Microthlaspi spp. populations being more detrimental to M. erraticum than strains from other sources. Our findings suggest that plant-endophyte associations are subject to local processes of selection, in which particular combinations of symbionts are favored across landscapes. We also show that different common endophytic taxa have differential sets of traits found to affect interactions, hinting to a functional complementarity that can explain their frequent co-existence in natural communities.

SUBMITTER: Kia SH

PROVIDER: S-EPMC5322293 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants.

Kia Sevda Haghi SH Glynou Kyriaki K Nau Thomas T Thines Marco M Piepenbring Meike M Maciá-Vicente Jose G JG

The ISME journal 20161101 3

Plants associate through their roots with fungal assemblages that impact their abundance and productivity. Non-mycorrhizal endophytes constitute an important component of such fungal diversity, but their implication in ecosystem processes is little known. Using a selection of 128 root-endophytic strains, we defined functional groups based on their traits and plant interactions with potential to predict community assembly and symbiotic association processes. In vitro tests of the strains' interac ...[more]

PMID: 27801904

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Project description:BackgroundThe genus Tetracladium De Wild. (Ascomycota) has been traditionally regarded as a group of Ingoldian fungi or aquatic hyphomycetes-a polyphyletic group of phylogenetically diverse fungi which grow on decaying leaves and plant litter in streams. Recent sequencing evidence has shown that Tetracladium spp. may also exist as root endophytes in terrestrial environments, and furthermore may have beneficial effects on the health and growth of their host. However, the diversity of Tetracladium spp. communities in terrestrial systems and the factors which shape their distribution are largely unknown.ResultsUsing a fungal community internal transcribed spacer amplicon dataset from 37 UK Brassica napus fields we found that soils contained diverse Tetracladium spp., most of which represent previously uncharacterised clades. The two most abundant operational taxonomic units (OTUs), related to previously described aquatic T. furcatum and T. maxilliforme, were enriched in roots relative to bulk and rhizosphere soil. For both taxa, relative abundance in roots, but not rhizosphere or bulk soil was correlated with B. napus yield. The relative abundance of T. furcatum and T. maxilliforme OTUs across compartments showed very similar responses with respect to agricultural management practices and soil characteristics. The factors shaping the relative abundance of OTUs homologous to T. furcatum and T. maxilliforme OTUs in roots were assessed using linear regression and structural equation modelling. Relative abundance of T. maxilliforme and T. furcatum in roots increased with pH, concentrations of phosphorus, and increased rotation frequency of oilseed rape. It decreased with increased soil water content, concentrations of extractable phosphorus, chromium, and iron.ConclusionsThe genus Tetracladium as a root colonising endophyte is a diverse and widely distributed part of the oilseed rape microbiome that positively correlates to crop yield. The main drivers of its community composition are crop management practices and soil nutrients.

Project description:Brassicaceae family includes an important group of plants of great scientific interest, e.g., the model plant Arabidopsis thaliana, and of economic interest, such as crops of the genus Brassica (Brassica oleracea, Brassica napus, Brassica rapa, etc.). This group of plants is characterized by the synthesis and accumulation in their tissues of secondary metabolites called glucosinolates (GSLs), sulfur-containing compounds mainly involved in plant defense against pathogens and pests. Brassicaceae plants are among the 30% of plant species that cannot establish optimal associations with mycorrhizal hosts (together with other plant families such as Proteaceae, Chenopodiaceae, and Caryophyllaceae), and GSLs could be involved in this evolutionary process of non-interaction. However, this group of plants can establish beneficial interactions with endophytic fungi, which requires a reduction of defensive responses by the host plant and/or an evasion, tolerance, or suppression of plant defenses by the fungus. Although much remains to be known about the mechanisms involved in the Brassicaceae-endophyte fungal interaction, several cases have been described, in which the fungi need to interfere with the GSL synthesis and hydrolysis in the host plant, or even directly degrade GSLs before they are hydrolyzed to antifungal isothiocyanates. Once the Brassicaceae-endophyte fungus symbiosis is formed, the host plant can obtain important benefits from an agricultural point of view, such as plant growth promotion and increase in yield and quality, increased tolerance to abiotic stresses, and direct and indirect control of plant pests and diseases. This review compiles the studies on the interaction between endophytic fungi and Brassicaceae plants, discussing the mechanisms involved in the success of the symbiosis, together with the benefits obtained by these plants. Due to their unique characteristics, the family Brassicaceae can be seen as a fruitful source of novel beneficial endophytes with applications to crops, as well as to generate new models of study that allow us to better understand the interactions of these amazing fungi with plants.

Dataset Information

Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants.

Publications

Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants.

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