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Transcriptome Analysis of Wheat Roots Reveals a Differential Regulation of Stress Responses Related to Arbuscular Mycorrhizal Fungi and Soil Disturbance

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Transcriptome Analysis of Wheat Roots Reveals a Differential Regulation of Stress Responses Related to Arbuscular Mycorrhizal Fungi and Soil Disturbance

Catarina Campos et al. Biology (Basel).

Abstract

Symbioses with soil microorganisms are central in shaping the diversity and productivity of land plants and provide protection against a diversity of stresses, including metal toxicity. Arbuscular mycorrhizal fungi (AMF) can form extensive extraradical mycelial networks (ERM), which are very efficient in colonizing a new host. We quantified the responses of transcriptomes of wheat and one AMF partner, Rhizoglomus irregulare, to soil disturbance (Undisturbed vs. Disturbed) and to two different preceding mycotrophic species (Ornithopus compressus and Lolium rigidum). Soil disturbance and preceding plant species engender different AMF communities in wheat roots, resulting in a differential tolerance to soil manganese (Mn) toxicity. Soil disturbance negatively impacted wheat growth under manganese toxicity, probably due to the disruption of the ERM, and activated a large number of stress and starvation-related genes. The O. compressus treatment, which induces a greater Mn protection in wheat than L. rigidum, activated processes related to cellular division and growth, and very few related to stress. The L. rigidum treatment mostly induced genes that were related to oxidative stress, disease protection, and metal ion binding. R. irregulare cell division and molecular exchange between nucleus and cytoplasm were increased by O. compressus. These findings are highly relevant for sustainable agricultural systems, when considering a fit-for-purpose symbiosis.

Keywords: Triticum aestivum; arbuscular mycorrhizal fungi; manganese stress; soil disturbance; transcriptomic response.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Differentially expressed genes in wheat roots at 1 week post-planting, according to the preceding plant species, in the Undisturbed regime. (a) Heatmap of the top 50 differentially expressed wheat genes between the Undisturbed L. rigidum and O. compressus treatments (green indicates down-regulated genes, red indicates up-regulated genes); and, (b) Comparison of the distribution of GO terms in wheat after L. rigidum and wheat after O. compressus.
Figure 2
Figure 2
GO enrichment of differentially expressed genes in wheat root at five weeks post-planting, between the Undisturbed and Disturbed regimes (a), or according to the preceding plant species (O. compressus or L. rigidum) in the Undisturbed regime (b).
Figure 3
Figure 3
(a) Network visualization of interactions between wheat genes in the “greenyellow” module, related to O. compressus. Larger nodes correspond to hub genes. (b) Pie-charts of GO terms distribution of genes in the “greenyellow” module belonging to the Biological Process, Molecular Function and Cellular Component classes.
Figure 4
Figure 4
(a) Network visualization of interactions between wheat genes in the “green” module, related to L. rigidum. Larger nodes correspond to hub genes. (b) Pie-charts of GO terms distribution of genes in the “green” module belonging to the Biological Process, Molecular Function, and Cellular Component classes.
Figure 5
Figure 5
GO enrichment of R. irregulare genes in the “orange” and “lightyellow” modules in the Biological Process, Molecular Function and Cellular Component classes. “orange” module shows genes related to O. compressus, and “lightyellow” module contains genes connected to L. rigidum.

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