Functional & Integrative Genomics

, Volume 19, Issue 4, pp 659–672 | Cite as

Salinity-associated microRNAs and their potential roles in mediating salt tolerance in rice colonized by the endophytic root fungus Piriformospora indica

  • Hadis Kord
  • Baratali Fakheri
  • Mehdi Ghabooli
  • Mahmood Solouki
  • Abbasali Emamjomeh
  • Behnam Khatabi
  • Mozhgan Sepehri
  • Ghasem Hosseini Salekdeh
  • Mohammad Reza GhaffariEmail author
Original Article


Piriformospora indica (P. indica), an endophytic root fungus, supports the growth and enhanced tolerance of plants to biotic and abiotic stresses. Several recent studies showed the significant role of small RNA (sRNA) molecules including microRNAs (miRNAs) in plant adaption to environmental stress, but little is known concerning the symbiosis-mediated salt stress tolerance regulated at miRNAs level. The overarching goal of this research is to elucidate the impact of miRNAs in regulating the P. indica-mediated salt tolerance in rice. Applying sRNA-seq analysis led to identify a set of 547 differentially abundant miRNAs in response to P. indica inoculation and salt stress. These included 206 rice-specific and 341 previously known miRNAs from other plant species. In silico analysis of miRNAs predictions of the differentially abundant miRNAs led to identifying of 193 putatively target genes, most of which were encoded either genes or transcription factors involved in nutrient uptake, sodium ion transporters, growth regulators, and auxin- responsive proteins. The rice-specific miRNAs targeted the transcription factors involved in the import of potassium ions into the root cells, the export of sodium ions, and plant growth and development. Interestingly, P. indica affected the differential abundance of miRNAs regulated genes and transcription factors linked to salt stress tolerance. Our data helps to understand the molecular basis of salt stress tolerance mediated by symbionts in plant and the potential impact of miRNAs for genetic improvement of rice varieties for tolerance to salt stress.


High-throughput sequencing Abiotic stress Post-transcriptional gene regulation Small RNA Target gene prediction 


Funding information

This work was supported by a grant from Agricultural Biotechnology Research Institute of Iran (ABRII) and the Iran National Science Foundation (INSF) offered Mohammad Reza Ghaffari.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10142_2019_671_Fig7_ESM.png (20 kb)
Supplementary Fig. 1.

High-throughput sequencing and Real-Time PCR Relative expression in P. indica inoculated rice roots compared to Non-inoculated plants. (PNG 9 kb)

10142_2019_671_MOESM1_ESM.tif (1.6 mb)
High Resulotion Image (TIF 1607 kb)
10142_2019_671_MOESM2_ESM.xlsx (10 kb)
Supplementary Table S1. Primer sequences used for QPCR. (XLSX 9 kb)
10142_2019_671_MOESM3_ESM.xlsx (53 kb)
Supplementary Table S2. The set of rice-specific and plant conserved mature miRNAs. (XLSX 53 kb)
10142_2019_671_MOESM4_ESM.xlsx (88 kb)
Supplementary Table S3. The set of known plant conserved and rice-specific miRNAs in response to the Piriformospora indica inoculation at different levels of salt stress (0, 50. 100 mM NaCl). (XLSX 88 kb)
10142_2019_671_MOESM5_ESM.xlsx (37 kb)
Supplementary Table S4. The set of novel miRNAs in response to the Piriformospora indica inoculation of rice plants exposed to t different levels of salt stress (0, 50. 100 mM NaCl), and alongside their chromosomal location of coding sequence. (XLSX 36 kb)
10142_2019_671_MOESM6_ESM.xlsx (18 kb)
Supplementary Table S5. The set of known miRNAs from a comparison between S0-vs S0+, S50-vs S50+ and S100-vs S100+. (XLSX 18 kb)
10142_2019_671_MOESM7_ESM.xlsx (39 kb)
Supplementary Table S6. Predicted target genes for differentially abundant miRNAs from a comparison between S0-vs S0+, S50-vs S50+ and S100-vs S100+. (XLSX 38 kb)
10142_2019_671_MOESM8_ESM.xlsx (11 kb)
Supplementary Table S7. Predicted target genes for highly abundance novel miRNAs identified from the contrasts S0-vs S0+, S50-vs S50+ and S100-vs S100+. (XLSX 10 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Hadis Kord
    • 1
  • Baratali Fakheri
    • 1
  • Mehdi Ghabooli
    • 2
  • Mahmood Solouki
    • 1
  • Abbasali Emamjomeh
    • 1
  • Behnam Khatabi
    • 3
  • Mozhgan Sepehri
    • 4
  • Ghasem Hosseini Salekdeh
    • 5
    • 6
  • Mohammad Reza Ghaffari
    • 6
    Email author
  1. 1.Department of Plant Breeding and Biotechnology (PBB), Faculty of AgricultureUniversity of ZabolZabolIran
  2. 2.Department of Agronomy, Faculty of AgricultureMalayer UniversityMalayerIran
  3. 3.Department of Agriculture, Food and Resource SciencesUniversity of Maryland Eastern ShorePrincess AnneUSA
  4. 4.Department of Soil Science, School of AgricultureShiraz UniversityShirazIran
  5. 5.Department of Molecular SciencesMacquarie UniversitySydneyAustralia
  6. 6.Department of Systems and Synthetic Biology, Agricultural Biotechnology Research Institute of Iran (ABRII)Agricultural Research, Education, and Extension Organization (AREEO)KarajIran

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