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

Abstract

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.

Comprehensive Analysis of Transcriptome and Metabolome Elucidates the Molecular Regulatory Mechanism of Salt Resistance in Roots of Achnatherum inebrians Mediated by Epichloë gansuensis

“…Based on PacBio Sequel technology, we have acquired the full-length transcriptome data of A. inebrians [ 7 ]. For further transcriptome analysis, samples from four treatment groups (roots of A. inebrians with or without E.gansuensis at 0 mM NaCl, 0RE+/−; roots of A. inebrians with or without E.gansuensis at 200 mM NaCl, 200RE+/−) were sequenced by Illumina platform with three biological duplicates per group.…”

“…Plants of A. inebrians with infection of E. gansuensis exhibit greater resistance to salt stress than E. gansuensis -free plants [ 6 , 20 ]. Our results have suggested that the presence of Epichloë endophytes in leaves altered multiple biological processes, including photosynthesis, oxidation-reduction, amino acid metabolism, and flavonoid biosynthetic, to enhance the adaptation of host plants to NaCl stress [ 7 ]. Despite the current knowledge, information referring to the underlying molecular mechanism in roots regulated by Epichloë gansuensis under salt stress is still elusive.…”

“…Achnatherum inebrians seedlings with or without E. gansuensis were prepared similarly to that described in our previous studies [ 6 , 7 ]. In brief, E. gansuensis -infected (E+) and E. gansuensis -free (E−) A. inebrians seedlings were sown in pots filled with sterile vermiculite (oven-dried at 150 °C for 3 h), and the vermiculite was saturated with ddH 2 O.…”

“…Epichloë endophytes are able to colonize the aerial tissues of host grasses, including seeds, stems, leaves, and peduncles, but with the exception of roots [ 5 ]. In addition, the presence of Epichloë endophytes confers increased resistance of host A. inebrians to salt stress [ 6 , 7 ], drought stress [ 8 ], low temperature [ 9 ], heavy metal stress [ 10 ], low nitrogen stress [ 11 , 12 , 13 ] and as well as improves the soil properties [ 14 ]. The increased resistance to various abiotic stress endowed by Epichloë endophytes has made A. inebrians thrive in these degraded grasslands of northwest China [ 15 ].…”

“…It has been extensively reported that the infection of Epichloë endophytes leads to the transcriptome reprogramming of host plants [ 9 , 21 , 22 , 23 , 24 ]. In our recent study, we evaluated the transcriptional response to NaCl stress in the leaves of A. inebrians based on Illumina sequencing and revealed that E. gansuensis up-regulated biology processes that were involved in the increased adaptation of host grasses to NaCl stress, such as cellular calcium ion homeostasis, proanthocyanidin biosynthesis, and brassinosteroid biosynthesis [ 7 ].…”