Microbiome and ecotypic adaption of Holcus lanatus (L.) to extremes of its soil pH range, investigated through transcriptome sequencing

Abstract

BackgroundPlants can adapt to edaphic stress, such as nutrient deficiency, toxicity and biotic challenges, by controlled transcriptomic responses, including microbiome interactions. Traditionally studied in model plant species with controlled microbiota inoculation treatments, molecular plant-microbiome interactions can be functionally investigated via RNA-Seq. Complex, natural plant-microbiome studies are limited, typically focusing on microbial rRNA and omitting functional microbiome investigations, presenting a fundamental knowledge gap. Here, root and shoot meta-transcriptome analyses, in tandem with shoot elemental content and root staining, were employed to investigate transcriptome responses in the wild grass Holcus lanatus and its associated natural multi-species eukaryotic microbiome. A full factorial reciprocal soil transplant experiment was employed, using plant ecotypes from two widely contrasting natural habitats, acid bog and limestone quarry soil, to investigate naturally occurring, and ecologically meaningful, edaphically driven molecular plant-microbiome interactions.ResultsArbuscular mycorrhizal (AM) and non-AM fungal colonization was detected in roots in both soils. Staining showed greater levels of non-AM fungi, and transcriptomics indicated a predominance of Ascomycota-annotated genes. Roots in acid bog soil were dominated by Phialocephala-annotated transcripts, a putative growth-promoting endophyte, potentially involved in N nutrition and ion homeostasis. Limestone roots in acid bog soil had greater expression of other Ascomycete genera and Oomycetes and lower expression of Phialocephala-annotated transcripts compared to acid ecotype roots, which corresponded with reduced induction of pathogen defense processes, particularly lignin biosynthesis in limestone ecotypes. Ascomycota dominated in shoots and limestone soil roots, but Phialocephala-annotated transcripts were insignificant, and no single Ascomycete genus dominated. Fusarium-annotated transcripts were the most common genus in shoots, with Colletotrichum and Rhizophagus (AM fungi) most numerous in limestone soil roots. The latter coincided with upregulation of plant genes involved in AM symbiosis initiation and AM-based P acquisition in an environment where P availability is low.ConclusionsMeta-transcriptome analyses provided novel insights into H. lanatus transcriptome responses, associated eukaryotic microbiota functions and taxonomic community composition. Significant edaphic and plant ecotype effects were identified, demonstrating that meta-transcriptome-based functional analysis is a powerful tool for the study of natural plant-microbiome interactions.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0434-3) contains supplementary material, which is available to authorized users.

Host-microbiota interactions: from holobiont theory to analysis

“…Meng and colleagues [16] propose a new method to separate the transcriptome of each member of the holobiont using metatranscriptomic datasets, allowing to access for the first time the whole functional diversity associated with the host and its microbiota. Young and co-workers [17] also used metatranscriptomics to characterize the microbiota associated with the wild grass Holcus lanatus and its changes in relation with soil types. In particular, they detected shifts in arbuscular mycorrhizal fungal communities according to phosphorus availability in the soil.…”

Variation of soil microbiome in licorice rhizosphere driven with inoculating dark septate endophytes under drought stress

“…However, Ascomycota, Proteobacteria, Actinobacteria, Chloro exi, and Firmicutes were the dominant phyla under both well-watered and drought conditions. The predominance of Ascomycota in arid and semi-arid regions was previously reported [27,28]. Dai et al [29] found that Actinobacteria, Proteobacteria, Saccharibacteria, Chloro exi, Acidobacteria, and Cyanobacteria were the predominant phyla in drought-treated and untreated peanut rhizosphere.…”

Evolutionary and ecological functional genomics, from lab to the wild

“…The attention to different environments goes hand‐in‐hand with increased interest in modeling evolutionary responses in relation to climate change and environmental stress (Nagano et al ., ; Plessis et al ., ; Fournier‐Level et al ., ; Watson‐Lazowski et al ., ). Because transcriptional reprogramming was the standard in examining plant defense responses, in the EEFG framework, the transcriptional implications of responses to biotic interactors are more rigorously being considered at the systems level in natural environments (Turner et al ., ; Liao et al ., ; Nobori et al ., ; Young et al ., ).…”