Genome Sequence of the Plant Growth Promoting Fungus <i>Serendipita vermifera</i> subsp. <i>bescii</i>: The First Native Strain from North America

Ray, Prasun; Chi, Myoung‐Hwan; Guo, Yingqing; Chen, Cindy; Adam, Catherine; Kuo, Alan; LaButti, Kurt; Lipzen, Anna; Barry, Kerrie; Grigoriev, Igor V.; Tang, Yuhong; Craven, Kelly D.

doi:10.1094/pbiomes-04-17-0017-a

Cited by 23 publications

(17 citation statements)

References 10 publications

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“…We have addressed this constraint by isolating the first North American strain of Serendipita , named Serendipita vermifera subsp . bescii NFPB0129 (hereafter referred to as S. bescii ), from the roots of a switchgrass plant in Ardmore, Oklahoma (Craven and Ray, ; Ray et al, ).…”

Section: Introductionmentioning

confidence: 99%

Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro

Ray

Abraham

Guo

et al. 2019

Environ Microbiol Rep

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Summary Serendipitaceae represents a diverse fungal group in the Basidiomycota that includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal lifestyle. Plants rely upon both nitrogen and phosphorous, for essential growth processes, and are often provided by mycorrhizal fungi. In this study, we investigated the cellular proteome of Serendipita vermifera MAFF305830 and closely related Serendipita vermifera subsp. bescii NFPB0129 grown in vitro under (N) ammonium and (P) phosphate starvation conditions. Mycelial growth pattern was documented under these conditions to correlate growth‐specific responses to nutrient starvation. We found that N‐starvation accelerated hyphal radial growth, whereas P‐starvation accelerated hyphal branching. Additionally, P‐starvation triggers an integrated starvation response leading to remodelling of lipid metabolism. Higher abundance of an ammonium transporter known to serve as both an ammonium sensor and stimulator of hyphal growth was detected under N‐starvation. Additionally, N‐starvation led to strong up‐regulation of nitrate, amino acid, peptide, and urea transporters, along with several proteins predicted to have peptidase activity. Taken together, our finding suggests S. bescii and S. vermifera have the metabolic capacity for nitrogen assimilation from organic forms of N compounds. We hypothesize that the nitrogen metabolite repression is a key regulator of such organic N assimilation.

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Section: Introductionmentioning

confidence: 99%

Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro

Ray

Abraham

Guo

et al. 2019

Environ Microbiol Rep

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“…After identifying proteins with signal peptides (signalp-4.1 [ 94 ]), those predicted as transmembrane helix proteins (tmhmm [ 95 ]), mitochondrial proteins (target-1.1 [ 96 ]), and cell wall hydrolysis-associated proteins were removed. For comparative analysis of the Si (Si-2020 and DSM11827 ASM31354 v.1 [ 22 ]), Serendipita vermifera [ 97 ] and Laccaria bicolor [ 98 ] genomes, software platform EDGAR 2.3 [ 99 ] was used.…”

Section: Methodsmentioning

confidence: 99%

A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis

et al. 2021

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Background Beneficial associations between plants and microbes are widespread in nature and have been studied extensively in the microbial-dominant environment of the rhizosphere. Such associations are highly advantageous for the organisms involved, benefiting soil microbes by providing them access to plant metabolites, while plant growth and development are enhanced through the promotion of nutrient uptake and/or protection against (a)biotic stresses. While the establishment and maintenance of mutualistic associations have been shown to require genetic and epigenetic reprogramming, as well as an exchange of effector molecules between microbes and plants, whether short RNAs are able to effect such changes is currently unknown. Here, we established an interaction between the model grass species Brachypodium distachyon (Bd, Pooideae) and the beneficial fungal root endophyte Serendipita indica (Si, syn. Piriformospora indica, Sebacinales) to elucidate RNA interference-based regulatory changes in gene expression and small (s)RNA profiles that occurred during establishment of a Sebacinalean symbiosis. Results Colonization of Bd roots with Si resulted in higher grain yield, confirming the mutualistic character of this interaction. Resequencing of the Si genome using the Oxford Nanopore technique, followed by de novo assembly yielded in 57 contigs and 9441 predicted genes, including putative members of several families involved in sRNA production. Transcriptome analysis at an early stage of the mutualistic interaction identified 2963 differentially expressed genes (DEG) in Si and 317 in Bd line 21-3. The fungal DEGs were largely associated with carbohydrate metabolism, cell wall degradation, and nutrient uptake, while plant DEGs indicated modulation of (a)biotic stress responses and defense pathways. Additionally, 10% of the upregulated fungal DEGs encode candidate protein effectors, including six DELD proteins typical for Sebacinales. Analysis of the global changes in the sRNA profiles of both associated organisms revealed several putative endogenous plant sRNAs expressed during colonization belonging to known micro (mi)RNA families involved in growth and developmental regulation. Among Bd- and Si-generated sRNAs with putative functions in the interacting organism, we identified transcripts for proteins involved in circadian clock and flowering regulation as well as immunity as potential targets of fungal sRNAs, reflecting the beneficial activity of Si. Conclusions We detected beneficial effects of Si colonization on Bd growth and development, and established a novel plant-mutualist interaction model between these organisms. Together, the changes in gene expression and identification of interaction-induced sRNAs in both organisms support sRNA-based regulation of defense responses and plant development in Bd, as well as nutrient acquisition and cell growth in Si. Our data suggests that a Sebacinalean symbiosis involves reciprocal sRNA targeting of genes during the interaction.

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“…Fungal material and culture conditions Serendipita bescii strain NFPB0129 was isolated from a switchgrass plot located in Oklahoma, USA (Ray et al, 2018b) and used in this study. The strain was routinely maintained in Modified Melin Norkan's (MMN) media (Marx, 1969), with 1% glucose as a C source at pH 6.0 in 24 C.…”

Section: Methodsmentioning

confidence: 99%

“…Our group has previously identified a new strain of Serendipita , Serendipita vermifera ssp. bescii (hereafter referred to as S. bescii ), which seems to be well adapted to the specific agro‐climatic conditions of the Southern Great Plains, USA (Craven and Ray, 2017; Ray et al ., 2018b).…”

Section: Introductionmentioning

confidence: 99%

Serendipita besciipromotes winter wheat growth and modulates the host root transcriptome under phosphorus and nitrogen starvation

Ray

Guo

Chi

et al. 2020

Environmental Microbiology

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Serendipita vermifera ssp. bescii, hereafter referred to as S. bescii, is a root-associated fungus that promotes plant growth in both its native switchgrass host and a variety of monocots and dicots. Winter wheat (Triticum aestivum L.), a dual-purpose crop, used for both forage and grain production, significantly contributes to the agricultural economies of the Southern Great Plains, USA. In this study, we investigated the influence of S. bescii on growth and transcriptome regulation of nitrogen (N) and phosphorus (P) metabolism in winter wheat. Serendipita bescii significantly improved lateral root growth and forage biomass under a limited N or P regime. Further, S. bescii activated sets of host genes regulating N and P starvation responses. These genes include, root-specific auxin transport, strigolactone and gibberellin biosynthesis, degradation of phospholipids and biosynthesis of glycerolipid, downregulation of ammonium transport and nitrate assimilation, restriction of protein degradation by autophagy and subsequent N remobilization. All these genes are hypothesized to regulate acquisition, assimilation and remobilization of N and P. Based on transcriptional level gene regulation and physiological responses to N or P limitation, we suggest S. bescii plays a critical role in modulating stress imposed by limitation of these two critical nutrients in winter wheat.

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Genome Sequence of the Plant Growth Promoting Fungus Serendipita vermifera subsp. bescii: The First Native Strain from North America

Cited by 23 publications

References 10 publications

Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro

Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro

A novel plant-fungal association reveals fundamental sRNA and gene expression reprogramming at the onset of symbiosis

Serendipita besciipromotes winter wheat growth and modulates the host root transcriptome under phosphorus and nitrogen starvation

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