Elucidating the Molecular Mechanisms by which Seed-Borne Endophytic Fungi, Epichloë gansuensis, Increases the Tolerance of Achnatherum inebrians to NaCl Stress

Seed-borne endophyte Epichloë gansuensis enhance NaCl tolerance in Achnatherum inebrians and increase its biomass. However, the molecular mechanism by which E. gansuensis increases the tolerance of host grasses to NaCl stress is unclear. Hence, we firstly explored the full-length transcriptome information of A. inebrians by PacBio RS II. In this work, we obtained 738,588 full-length non-chimeric reads, 36,105 transcript sequences and 27,202 complete CDSs from A. inebrians. We identified 3558 transcription factors (TFs), 15,945 simple sequence repeats and 963 long non-coding RNAs of A. inebrians. The present results show that 2464 and 1817 genes were differentially expressed by E. gansuensis in the leaves of E+ and E− plants at 0 mM and 200 mM NaCl concentrations, respectively. In addition, NaCl stress significantly regulated 4919 DEGs and 502 DEGs in the leaves of E+ and E− plants, respectively. Transcripts associated with photosynthesis, plant hormone signal transduction, amino acids metabolism, flavonoid biosynthetic process and WRKY TFs were differentially expressed by E. gansuensis; importantly, E. gansuensis up-regulated biology processes (brassinosteroid biosynthesis, oxidation–reduction, cellular calcium ion homeostasis, carotene biosynthesis, positive regulation of proteasomal ubiquitin-dependent protein catabolism and proanthocyanidin biosynthesis) of host grass under NaCl stress, which indicated an increase in the ability of host grasses’ adaptation to NaCl stress. In conclusion, our study demonstrates the molecular mechanism for E. gansuensis to increase the tolerance to salt stress in the host, which provides a theoretical basis for the molecular breed to create salt-tolerant forage with endophytes.

Correction: Liu et al. Epichloë gansuensis Increases the Tolerance of Achnatherum inebrians to Low-P Stress by Modulating Amino Acids Metabolism and Phosphorus Utilization Efficiency. J. Fungi 2021, 7, 390

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Transcriptome Analysis Revealed Plant Hormone Biosynthesis and Response Pathway Modification by Epichloë gansuensis in Achnatherum inebrians under Different Soil Moisture Availability

The present study was designed to explore the effects of the endophyte Epichloë gansuensis on gene expression related to plant hormone biosynthesis and response pathways and the content of salicylic acid (SA) and jasmonic acid (JA) hormones of Achnatherum inebrians, under different moisture conditions. Through a pot experiment and transcriptome analysis, we found a total of 51 differentially expressed genes (DEGs) related to hormone biosynthesis and response pathways, including 12 auxin related genes, 8 cytokinin (CTK) related genes, 3 gibberellin (GA) related genes, 7 abscisic acid (ABA) related genes, 7 ethylene (ET) related genes, 12 JA related genes and 4 SA related genes. Furthermore, key genes of JA and SA biosynthesis and response pathways, such as LOX2S, AOS, OPR, ACX, JMT, JAZ, PAL, NPR1, TGA and PR-1, showed different degrees of upregulation or downregulation. Under 60% soil moisture content, the JA content of endophyte-free (EF) A. inebrians was significantly (p < 0.05) higher than that of endophyte-infected (EI) A. inebrians. Under 30% and 60% soil moisture content, the SA content of EF A. inebrians was significantly (p < 0.05) higher than that of EI A. inebrians. SA content of EI A. inebrians under 30% and 60% soil moisture content was significantly (p < 0.05) higher than that under 15% soil moisture content. With both EI and EF plants, the SA and JA levels, respectively, are very similar at 15% soil moisture content. This study has revealed that E. gansuensis differentially activated plant hormone synthesis and signal transduction pathways of A. inebrians plants under different soil moisture availability.

Epichloë gansuensis Increases the Tolerance of Achnatherum inebrians to Low-P Stress by Modulating Amino Acids Metabolism and Phosphorus Utilization Efficiency

In the long-term evolutionary process, Achnatherum inebrians and seed-borne endophytic fungi, Epichloë gansuensis, formed a mutually beneficial symbiosis relationship, and Epichloë gansuensis has an important biological role in improving the tolerance of host grasses to abiotic stress. In this work, we first assessed the effects of Epichloë gansuensis on dry weight, the content of C, N, P and metal ions, and metabolic pathway of amino acids, and phosphorus utilization efficiency (PUE) of Achnatherum inebrians at low P stress. Our results showed that the dry weights, the content of alanine, arginine, aspartic acid, glycine, glutamine, glutamic acid, L-asparagine, lysine, phenylalanine, proline, serine, threonine, and tryptophan were higher in leaves of Epichloë gansuensis-infected (E+) Achnatherum inebrians than Epichloë gansuensis-uninfected (E−) Achnatherum inebrians at low P stress. Further, Epichloë gansuensis increased C content of roots compared to the root of E− plant at 0.01 mM P and 0.5 mM P; Epichloë gansuensis increased K content of leaves compared to the leaf of E− plant at 0.01 mM P and 0.5 mM P. Epichloë gansuensis reduced Ca content of roots compared to the root of E− plant at 0.01 mM P and 0.5 mM P; Epichloë gansuensis reduced the content of Mg and Fe in leaves compared to the leaf of E− plant at 0.01 mM P and 0.5 mM P. In addition, at low P stress, Epichloë gansuensis most probably influenced aspartate and glutamate metabolism; valine, leucine, and isoleucine biosynthesis in leaves; and arginine and proline metabolism; alanine, aspartate, and glutamate metabolism in roots. Epichloë gansuensis also affected the content of organic acid and stress-related metabolites at low P stress. In conclusion, Epichloë gansuensis improves Achnatherum inebrians growth at low P stress by regulating the metabolic pathway of amino acids, amino acids content, organic acid content, and increasing PUE.