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Role of plant-fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi.

ABSTRACT: Multiple ectomycorrhizal fungi (EMF) compete to colonise the roots of a host plant, but it is not known whether their success is under plant or fungal control, or a combination of both. We assessed whether plants control EMF colonisation by preferentially allocating more carbon to more beneficial partners in terms of nitrogen supply or if other factors drive competitive success. We combined stable isotope labelling and RNA-sequencing approaches to characterise nutrient exchange between the plant host Eucalyptus grandis and three Pisolithus isolates when growing alone and when competing either indirectly (with a physical barrier) or directly. Overall, we found that nitrogen provision to the plant does not explain the amount of carbon that an isolate receives nor the number of roots that it colonises. Differences in nutrient exchange among isolates were related to differences in expression of key fungal and plant nitrogen and carbon transporter genes. When given a choice of partners, the plant was able to limit colonisation by the least cooperative isolate. This was not explained by a reduction in allocated carbon. Instead, our results suggest that partner choice in EMF could operate through the upregulation of defence-related genes against those fungi providing fewer nutrients.

SUBMITTER: Hortal S

PROVIDER: S-EPMC5702723 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Role of plant-fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi.

Hortal Sara S Plett Krista Lynn KL Plett Jonathan Michael JM Cresswell Tom T Johansen Mathew M Pendall Elise E Anderson Ian Charles IC

The ISME journal 20170721 12

Multiple ectomycorrhizal fungi (EMF) compete to colonise the roots of a host plant, but it is not known whether their success is under plant or fungal control, or a combination of both. We assessed whether plants control EMF colonisation by preferentially allocating more carbon to more beneficial partners in terms of nitrogen supply or if other factors drive competitive success. We combined stable isotope labelling and RNA-sequencing approaches to characterise nutrient exchange between the plant ...[more]

PMID: 28731478

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Project description:Nonmycorrhizal root-colonizing fungi are key determinants of plant growth, driving processes ranging from pathogenesis to stress alleviation. Evidence suggests that they might also facilitate host access to soil nutrients in a mycorrhiza-like manner, but the extent of their direct contribution to plant nutrition is unknown. To study how widespread such capacity is across root-colonizing fungi, we surveyed soils in nutrient-limiting habitats using plant baits to look for fungal community changes in response to nutrient conditions. We established a fungal culture collection and used Arabidopsis thaliana inoculation bioassays to assess the ability of fungi to facilitate host's growth in the presence of organic nutrients unavailable to plants. Plant baits captured a representation of fungal communities extant in natural habitats and showed that nutrient limitation has little influence on community assembly. Arabidopsis thaliana inoculated with 31 phylogenetically diverse fungi exhibited a consistent fungus-driven growth promotion when supplied with organic nutrients compared to untreated plants. However, direct phosphorus measurement and RNA-seq data did not support enhanced nutrient uptake but rather that growth effects may result from changes in the plant's immune response to colonization. The widespread and consistent host responses to fungal colonization suggest that distinct, locally adapted nonmycorrhizal fungi affect plant performance across habitats. IMPORTANCE Recent studies have shown that root-associated fungi that do not engage in classical mycorrhizal associations can facilitate the hosts' access to nutrients in a mycorrhiza-like manner. However, the generality of this capacity remains to be tested. Root-associated fungi are frequently deemed major determinants of plant diversity and performance, but in the vast majority of cases their ecological roles in nature remain unknown. Assessing how these plant symbionts affect plant productivity, diversity, and fitness is important to understanding how plant communities function. Recent years have seen important advances in the understanding of the main drivers of the diversity and structure of plant microbiomes, but a major challenge is still linking community properties with function. This study contributes to the understanding of the cryptic function of root-associated fungi by testing their ability to participate in a specific process: nutrient acquisition by plants.

Project description:Ectomycorrhizal fungi (EMF) can form symbiotic relationships with plants, aiding in plant growth by providing access to nutrients and defense against phytopathogenic fungi. In this context, factors such as plant assemblages and soil properties can impact the interaction between EMF and phytopathogenic fungi in forest soil. However, there is little understanding of how these fungal interactions evolve as forests move through succession stages. In this study, we used high-throughput sequencing to investigate fungal communities in young, intermediate, and old subtropical forests. At the genus level, EMF communities were dominated by Sebacina, Russula, and Lactarius, while Mycena was the most abundant genus in pathogenic fungal communities. The relative abundances of EMF and phytopathogenic fungi in different stages showed no significant difference with the regulation of different factors. We discovered that interactions between phytopathogenic fungi and EMF maintained a dynamic balance under the influence of the differences in soil quality attributed to each forest successional stage. The community composition of phytopathogenic fungi is one of the strong drivers in shaping EMF communities over successions. In addition, the EMF diversity was significantly related to plant diversity, and these relationships varied among successional stages. Despite the regulation of various factors, the positive relationship between the diversity of phytopathogenic fungi and EMF remained unchanged. However, there is no significant difference in the ratio of the abundance of EMF and phytopathogenic fungi over the course of successions. These results will advance our understanding of the biodiversity-ecosystem functioning during forest succession. KEY POINTS: •Community composition of both EMF and phytopathogenic fungi changed significantly over forest succession. •Phytopathogenic fungi is a key driver in shaping EMF community. •The effect of plant Shannon's diversity on EMF communities changed during the forest aging process.

Dataset Information

Role of plant-fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi.

Publications

Role of plant-fungal nutrient trading and host control in determining the competitive success of ectomycorrhizal fungi.

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