The fungal root endophyte <i>Serendipita vermifera</i> displays inter-kingdom synergistic beneficial effects with the microbiota in <i>Arabidopsis thaliana</i> and barley

Mahdi, Lisa K.; Miyauchi, Shingo; Uhlmann, Charles; Garrido‐Oter, Ruben; Langen, Gregor; Wawra, Stephan; Niu, Yulong; Guan, Rui; Robertson-Albertyn, Senga; Bulgarelli, Davide; Parker, Jane E.; Zuccaro, Alga

doi:10.1038/s41396-021-01138-y

Cited by 35 publications

(35 citation statements)

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“…An alternative, and not mutually exclusive, scenario is that disease resistance may have been the trait under agronomic selection. This would be in line with a recent investigation which demonstrated that bacteria isolated from the barley rhizosphere mediated the establishment of both pathogenic and mutualistic fungi in roots 73 . In this scenario, selection at QRMC-3HS may contribute to the fine-tuning of these multitrophic interactions.…”

Section: Discussionsupporting

confidence: 88%

“…The copyright holder for this preprint this version posted December 21, 2021. ; https://doi.org/10.1101/2021.12.20.472907 doi: bioRxiv preprint demonstrated that bacteria isolated from the barley rhizosphere mediated the establishment of both pathogenic and mutualistic fungi in roots 71 . In this scenario, selection at QRMC-3HS may contribute to the fine-tuning of these multitrophic interactions.…”

Section: Discussionmentioning

confidence: 99%

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Identifying Plant Genes Shaping Microbiota Composition in the Barley Rhizosphere

Escudero-Martinez

Coulter

Terrazas

et al. 2021

Preprint

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A prerequisite to exploiting soil microbes for sustainable crop production is the identification of the plant genes shaping microbiota composition in the rhizosphere, the interface between roots and soil. Here we used metagenomics information as an external quantitative phenotype to map the host genetic determinants of the rhizosphere microbiota in wild and domesticated genotypes of barley, the fourth most cultivated cereal globally. We identified a small number of loci with a major effect on the composition of rhizosphere communities. One of those, designated the QRMC-3HS locus, emerged as a major determinant of microbiota composition. We then subjected soil-grown sibling lines harbouring contrasting alleles at QRMC-3HS and hosting contrasting microbiotas to comparative root RNA-seq profiling. This allowed us to identify three primary candidate genes, including a Nucleotide-Binding-Leucine-Rich-Repeat (NLR) gene in a region of structural variation of the barley genome. Our results provide novel insights into the footprint of crop improvement on the plants capacity of shaping rhizosphere microbes.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Identifying Plant Genes Shaping Microbiota Composition in the Barley Rhizosphere

Escudero-Martinez

Coulter

Terrazas

et al. 2021

Preprint

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“…Under current global change scenarios, the abundance of plant pathogens in soil is predicted to increase (Delgado‐Baquerizo et al ., 2020), implying that plant protection by endophytic mycorrhizal‐like fungi could improve plant adaptation to increased disease pressure. Serendipita indica has been shown to promote plant resistance by modulating plant defences, but also by interacting with various rhizosphere bacteria acting through microbial processes involving lytic enzymes (Mahdi et al ., 2021). Similarly, H. chaetospira induces plant defence and has been described as a plant protection agent (Lahlali et al ., 2014).…”

Section: Will Mycorrhiza‐like Associations Help Plants Adapt To Globa...mentioning

confidence: 99%

Unearthing the plant–microbe quid pro quo in root associations with beneficial fungi

2022

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Mutualistic symbiotic associations between multicellular eukaryotes and their microbiota are driven by the exchange of nutrients in a quid pro quo manner. In the widespread arbuscular mycorrhizal (AM) symbiosis involving plant roots and Glomeromycotina fungi, the mycobiont is supplied with carbon through photosynthesis, which in return supplies the host plant with essential minerals such as phosphorus (P). Most terrestrial plants are largely dependent on AM fungi for nutrients, which raises the question of how plants that are unable to form a functional AM sustain their P nutrition. AM nonhost plants can form alternative, evolutionarily younger, mycorrhizal associations such as the ectomycorrhiza, ericoid and orchid mycorrhiza. However, it is unclear how plants such as the Brassicaceae species Arabidopsis thaliana, which do not form known mycorrhizal symbioses, have adapted to the loss of these essential mycorrhizal traits. Isotope tracing experiments with root-colonizing fungi have revealed the existence of new 'mycorrhizallike' fungi capable of transferring nutrients such as nitrogen (N) and P to plants, including Brassicaceae. Here, we provide an overview of the biology of trophic relationships between roots and fungi and how these associations might support plant adaptation to climate change.

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“…Recently, we described a soluble extracellular β-glucan matrix produced by endophytic fungi during root colonization of Arabidopsis thaliana (hereafter Arabidopsis) and Hordeum vulgare (hereafter barley; Wawra et al, 2019 ). Little is known about the biochemical properties, composition, and function of this EPS matrix, but its detection in beneficial and pathogenic fungi strongly suggests a conserved role in counteracting environmental and immunological challenges during fungal growth and plant colonization ( El Oirdi et al, 2011 ; Mahdi et al, 2021 ; Wanke et al, 2021 ). It is therefore crucial to investigate the structure and function of these soluble β-glucans and the hydrolytic events mediated by host apoplastic CAZymes during plant–fungal interactions.…”

Section: Introductionmentioning

confidence: 99%

Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses

et al. 2022

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Plant pathogenic and beneficial fungi have evolved several strategies to evade immunity and cope with host-derived hydrolytic enzymes and oxidative stress in the apoplast, the extracellular space of plant tissues. Fungal hyphae are surrounded by an inner insoluble cell wall (CW) layer and an outer soluble extracellular polysaccharide (EPS) matrix. Here we show by proteomics and glycomics that these two layers have distinct protein and carbohydrate signatures, and hence likely have different biological functions. The barley (Hordeum vulgare) β-1,3-endoglucanase HvBGLUII, which belongs to the widely distributed apoplastic glycoside hydrolase 17 family (GH17), releases a conserved β-1,3;1,6-glucan decasaccharide (β-GD) from the EPS matrices of fungi with different lifestyles and taxonomic positions. This low molecular weight β-GD does not activate plant immunity, is resilient to further enzymatic hydrolysis by β-1,3-endoglucanases due to the presence of three β-1,6-linked glucose branches and can scavenge reactive oxygen species. Exogenous application of β-GD leads to enhanced fungal colonization in barley, confirming its role in the fungal counterdefensive strategy to subvert host immunity. Our data highlight the hitherto undescribed capacity of this often-overlooked EPS matrix from plant-associated fungi to act as an outer protective barrier important for fungal accommodation within the hostile environment at the apoplastic plant-microbe interface.

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The fungal root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with the microbiota in Arabidopsis thaliana and barley

Cited by 35 publications

References 96 publications

Identifying Plant Genes Shaping Microbiota Composition in the Barley Rhizosphere

Identifying Plant Genes Shaping Microbiota Composition in the Barley Rhizosphere

Unearthing the plant–microbe quid pro quo in root associations with beneficial fungi

Fungi hijack a ubiquitous plant apoplastic endoglucanase to release a ROS scavenging β-glucan decasaccharide to subvert immune responses

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