Abstract
As a newly characterized class of noncoding RNAs, circular RNAs (circRNAs) have been identified in many plant species, and play important roles in plant stress responses. However, little is known about how salt stress mediates the expression of circRNAs in rice. In this study, we identified circRNAs from root tissues of salt-susceptible recipient cultivar 93–11 and salt-tolerant introgression line 9L136. A total of 190 circRNAs were identified. Among them, 93 circRNAs were differentially expressed under salt stress in 93–11 (36 up- and 57 down-regulated) and 95 in 9L136 (46 up- and 49 down-regulated). Salt stress significantly decreased the average expression level of circRNAs in 93–11, but circRNA expression levels were slightly increased in 9L136, suggesting that circRNAs had different response patterns in these two cultivars. Function annotation and enrichment analysis indicated that, through cis-regulation and circRNA-miRNA-mRNA network regulation, those induced circRNAs were commonly involved in transcription, signal transduction, ion transportation, and secondary metabolism. Compared to 93–11, salt-induced circRNAs in line 9L136 targeted more stress response genes participating in transcription regulation, ion transportation, and signal transduction, which may contribute to the salt tolerance of 9L136. Summarily, this study revealed the common response of rice circRNAs to salt stress, and the possible circRNA-related salt tolerance mechanisms of 9L136.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files. The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Adler D, Kelly ST (2021) vioplot: violin plot. R package version 0.3.6 https://github.com/TomKellyGenetics/vioplot
Arbelaez JD, Maron LG, Jobe TO, Piñeros MA, Famoso AN, Rebelo AR, Singh N, Ma Q, Fei Z, Kochian LV, Mccouch SR (2017) Aluminum resistance transcription factor 1 (ART1) contributes to natural variation in aluminum resistance in diverse genetic backgrounds of rice (O. sativa). Plant Direct 1:e00014. https://doi.org/10.1002/pld3.14
Chen L, Zhang P, Fan Y, Lu Q, Li Q, Yan J, Muehlbauer GJ, Schnable PS, Dai M, Li L (2018) Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytol 217:1292–1306. https://doi.org/10.1111/nph.14901
Cheng J, Zhang Y, Li Z, Wang T, Zhang X, Zheng B (2018) A lariat-derived circular RNA is required for plant development in Arabidopsis. Sci China Life Sci 61:204–213. https://doi.org/10.1007/s11427-017-9182-3
Chu Q, Zhang X, Zhu X, Liu C, Mao L, Ye C, Zhu Q, Fan L (2017) Plantcirc Base: a database for plant circular RNAs. Mol Plant 10:1126–1128. https://doi.org/10.1016/j.molp.2017.03.003
Chu Q, Bai P, Zhu X, Zhang X, Mao L, Zhu QH, Fan L, Ye CY (2020) Characteristics of plant circular RNAs. Brief Bioinform 21:135–143. https://doi.org/10.1093/bib/bby111
Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G, Cildir G, Jourdain A, Tergaonkar V, Schmid M, Zubieta C, Conn SJ (2017) A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants 3:17053. https://doi.org/10.1038/nplants.2017.53
Fang Z, Jiang W, He Y, Ma D, Liu Y, Wang S, Zhang Y, Yin J (2020) Genome-wide identification, structure characterization, and expression profiling of Dof transcription factor gene family in wheat (Triticum aestivum L.). Agronomy 10:294. https://doi.org/10.3390/agronomy10020294
Gao Y, Zhang J, Zhao F (2017) Circular RNA identification based on multiple seed matching. Brief Bioinform 19:803–810. https://doi.org/10.1093/bib/bbx014
Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979. https://doi.org/10.1111/j.1365-3040.2006.01572.x
Gu ZG, Gu L, Eils R, Schlesner M, Brors B (2014) circlize implements and enhances circular visualization in R. Bioinformatics 30:2811–2812. https://doi.org/10.1093/bioinformatics/btu393
He X, Guo S, Wang Y, Wang L, Shu S, Sun J (2020) Systematic identification and analysis of heat-stress-responsive lncRNAs, circRNAs and miRNAs with associated co-expression and ceRNA networks in cucumber (Cucumis sativus L.). Physiol Plantarum 168:736–754. https://doi.org/10.1111/ppl.12997
Huang X, Feng J, Wang R, Zhang H, Huang J (2019) Comparative analysis of microRNAs and their targets in the roots of two cultivars with contrasting salt tolerance in rice (Oryza sativa L.). Plant Growth Regul 87:139–148. https://doi.org/10.1007/s10725-018-0459-4
Li HM, Ma XL, Li HG (2019) Intriguing circles: Conflicts and controversies in circular RNA research. Wires RNA 10:e1538. https://doi.org/10.1002/wrna.1538
Li X, Liu C, Xue W, Zhang Y, Jiang S, Yin Q, Wei J, Yao R, Yang L, Chen L (2017) Coordinated circRNA biogenesis and function with NF90/NF110 in viral infection. Mol Cell 67:214–227. https://doi.org/10.1016/j.molcel.2017.05.023
Liu J, Liu T, Wang X, He A (2017a) Circles reshaping the RNA world: from waste to treasure. Mol Cancer 16:58. https://doi.org/10.1186/s12943-017-0630-y
Liu T, Zhang L, Chen G, Shi T (2017b) Identifying and characterizing the circular RNAs during the lifespan of Arabidopsis leaves. Front Plant Sci 8:1278. https://doi.org/10.3389/fpls.2017.01278
Lu T, Cui L, Zhou Y, Zhu C, Fan D, Gong H, Zhao Q, Zhou C, Zhao Y, Lu D, Luo J, Wang Y, Tian Q, Feng Q, Huang T, Han B (2015) Transcriptome-wide investigation of circular RNAs in rice. RNA 21:2076–2087. https://doi.org/10.1261/rna.052282.115
Mangrauthia SK, Bhogireddy S, Agarwal S, Prasanth VV, Voleti SR, Neelamraju S, Subrahmanyam D (2017) Genome-wide changes in microRNA expression during short and prolonged heat stress and recovery in contrasting rice cultivars. J Exp Bot 68:2399–2412
Meng X, Li X, Zhang P, Wang J, Zhou Y, Chen M (2016) Circular RNA: an emerging key player in RNA world. Brief Bioinform 18:547–557. https://doi.org/10.1093/bib/bbw045
Pan T, Sun X, Liu Y, Li H, Deng G, Lin H, Wang S (2018) Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis. Plant Mol Biol 96:217–229. https://doi.org/10.1007/s11103-017-0684-7
Qin Z, Chen J, Jin L, Duns GJ, Ouyang P (2015) Differential expression of miRNAs under salt stress in Spartina alterniflora leaf tissues. J Nanosc Nanotechno 15:1554–1561. https://doi.org/10.1166/jnn.2015.9004
Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 1:538–551. https://doi.org/10.1093/mplant/ssn012
Tan J, Zhou Z, Niu Y, Sun X, Deng Z (2017) Identification and functional characterization of tomato circRNAs derived from genes involved in fruit pigment accumulation. Sci Rep 7:8594. https://doi.org/10.1038/s41598-017-08806-0
Tong W, Yu J, Hou Y, Li F, Zhou Q, Wei C, Bennetzen JL (2018) Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis). Planta 248:1417–1429. https://doi.org/10.1007/s00425-018-2983-x
Vijayan J, Jain S, Jain N, Devanna B, Rathour R, Variar M, Prashanthi S, Singh A, Singh U, Singh N, Sharma T (2013) Identification of differentially expressed genes in rice during its early phases of interaction with Magnaporthe oryzae. Indian J Genet 73:233–243. https://doi.org/10.5958/j.0975-6906.73.3.035
Wang K, Wang C, Guo B, Song K, Shi C, Jiang X, Wang K, Tan Y, Wang L, Wang L, Li J, Li Y, Cai Y, Zhao H, Sun X (2019) CropCircDB: a comprehensive circular RNA resource for crops in response to abiotic stress. Database 2019:baz053. https://doi.org/10.1093/database/baz053
Wang L, Chu H, Li Z, Wang J, Li J, Qiao Y, Fu Y, Mou T, Chen C, Xu J (2014a) Origin and development of the root cap in rice. Plant Physiol 166:603–613. https://doi.org/10.1104/pp.114.240929
Wang S, Cao M, Ma X, Chen W, Zhao J, Sun C, Tan L, Liu F (2017a) Integrated RNA sequencing and QTL mapping to identify candidate genes from Oryza rufipogon associated with salt tolerance at the seedling stage. Front Plant Sci 8:1427. https://doi.org/10.3389/fpls.2017.01427
Wang Y, Yang M, Wei S, Qin F, Zhao H, Suo B (2017b) Identification of circular RNAs and their targets in leaves of Triticum aestivum L under dehydration stress. Front Plant Sci 7: 2024 Doi: https://doi.org/10.3389/fpls.2016.02024
Wang Z, Liu Y, Li D, Li L, Zhang Q (2017c) Identification of circular RNAs in kiwifruit and their species-specific response to bacterial canker pathogen invasion. Front Plant Sci 8:413. https://doi.org/10.3389/fpls.2017.00413
Wang YG, An M, Zhou SF, She YH, Li WC, Fu FL (2014b) Expression profile of maize microRNAs corresponding to their target genes under drought stress. Biochem Genet 52:474–493. https://doi.org/10.1007/s10528-014-9661-x
Wilkins O, Hafemeister C, Plessis A, Holloway-Phillips M-M, Pham GM, Nicotra AB, Gregorio GB, Jagadish SVK, Septiningsih EM, Bonneau R, Purugganan M (2016) EGRINs (Environmental Gene Regulatory Influence Networks) in rice that function in the response to water deficit, high temperature, and agricultural environments. Plant Cell 28:2365–2384. https://doi.org/10.1105/tpc.16.00158
Xu X, Bai H, Liu C, Chen E, Chen Q, Zhuang J, Shen B (2014) Genome-wide analysis of microRNAs and their target genes related to leaf senescence of rice. PLoS ONE 9:e114313. https://doi.org/10.1371/journal.pone.0114313
Yang YW, Chen HC, Jen WF, Liu LY, Chang MC (2015) Comparative transcriptome analysis of shoots and roots of TNG67 and TCN1 rice seedlings under cold stress and following subsequent recovery: Insights into metabolic pathways, phytohormones, and transcription factors. PLoS ONE 10:e0131391. https://doi.org/10.1371/journal.pone.0131391
Ye C, Zhang X, Chu Q, Liu C, Yu Y, Jiang W, Zhu Q, Fan L, Guo L (2016) Full-length sequence assembly reveals circular RNAs with diverse non-GT/AG splicing signals in rice. RNA Biol 14:1055–1063. https://doi.org/10.1080/15476286.2016.1245268
Ye CY, Chen L, Liu C, Zhu QH, Fan L (2015) Widespread noncoding circular RNAs in plants. New Phytol 208:88–95. https://doi.org/10.1111/nph.13585
Yin J, Liu M, Ma D, Wu J, Li S, Zhu Y, Han B (2018) Identification of circular RNAs and their targets during tomato fruit ripening. Postharvest Biol Tec 136:90–98. https://doi.org/10.1016/j.postharvbio.2017.10.013
You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang M, Glock C, Quedenau C, Wang X, Hou J, Liu H, Sun W, Sambandan S, Chen T, Schuman EM, Chen W (2015) Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci 18:603–610. https://doi.org/10.1038/nn.3975
Zare S, Nazarian-Firouzabadi F, Ismaili A, Pakniyat H (2019) Identification of miRNAs and evaluation of candidate genes expression profile associated with drought stress in barley. Plant Gene 20:100205. https://doi.org/10.1016/j.plgene.2019.100205
Zhang M, Huang N, Yang X, Luo J, Yan S, Xiao F, Chen W, Gao X, Zhao K, Zhou H, Li Z, Ming L, Xie B, Zhang N (2018) A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis. Oncogene 37:1805–1814. https://doi.org/10.1038/s41388-017-0019-9
Zhao W, Cheng Y, Zhang C, You Q, Shen X, Guo W, Jiao Y (2017) Genome-wide identification and characterization of circular RNAs by high throughput sequencing in soybean. Sci Rep 7:5636
Zhao W, Chu S, Jiao Y (2019) Present scenario of circular RNAs (circRNAs) in plants. Front Plant Sci 10:379. https://doi.org/10.1038/s41598-017-05922-9
Zhou R, Zhu Y, Zhao J, Fang Z, Wang S, Yin J, Chu Z, Ma D (2018) Transcriptome-wide identification and characterization of potato circular RNAs in response to Pectobacterium carotovorum subspecies brasiliense infection. Int J Mol Sci 19:71. https://doi.org/10.3390/ijms19010071
Zhu YX, Jia JH, Yang L, Xia YC, Zhang HL, Jia JB, Zhou R, Nie PY, Yin JL, Ma DF, Liu LC (2019a) Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biol 19:164. https://doi.org/10.1186/s12870-019-1712-3
Zhu Y, Gong H, Yin J (2019b) Role of silicon in mediating salt tolerance in plants: A review. Plants 8:147. https://doi.org/10.3390/plants8060147
Zhu Y, Yang L, Liu N, Yang J, Zhou X, Xia Y, He Y, He Y, Gong H, Ma D, Yin J (2019c) Genome-wide identification, structure characterization, and expression pattern profiling of aquaporin gene family in cucumber. BMC Plant Biol 19:345. https://doi.org/10.1186/s12870-019-1953-1
Acknowledgements
We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Funding
This work was partially supported by the Open Project Program of Hubei Key Laboratory of Food Crop Germplasm and Genetic Improvement (2019lzjj03), the Open Project Program of Key Laboratory of Integrated Pest Management of Crops in Central China, Ministry of Agriculture/Hubei Key Laboratory of Crop Diseases, Insect Pests and Weeds Control (2019ZTSJJ8).
Author information
Authors and Affiliations
Contributions
J.L. Y., Y.K. L., L. L., and J. Z. conceived the study, designed the experiments, and analyzed data. J.L. Y. wrote the first draft, S.Y. C. and B.T. W. finalized the manuscript. All the authors read the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Fei Dai.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10725_2021_772_MOESM1_ESM.xlsx
Supplementary file1 Supplementary Table 1. Genome-wide identification of circRNAs in recipient 93-11 and introgression line 9L136. Supplementary Table 2. Detailed information of identified circRNAs in rice. Supplementary Table 3. Salt induced differentially expressed circRNAs and annotations in 93-11. Supplementary Table 4. Salt induced differentially expressed circRNAs and annotations in 9L136. Supplementary Table 5. Detailed information of miRNA sponged by circRNAs and their mRNA targets in 93-11. Supplementary Table 6. Function annotations of mRNAs targeted by miRNAs in 93-11. Supplementary Table 7. Detailed information of miRNA sponged by circRNAs and their mRNA targets in 9L136. Supplementary Table 8. Function annotations of mRNAs targeted by miRNAs in 9L136. Supplementary Table 9. Primers used for circRNAs sequences validation. (XLSX 153 KB)
Rights and permissions
About this article
Cite this article
Yin, J., Liu, Y., Lu, L. et al. Comparison of tolerant and susceptible cultivars revealed the roles of circular RNAs in rice responding to salt stress. Plant Growth Regul 96, 243–254 (2022). https://doi.org/10.1007/s10725-021-00772-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-021-00772-y