Skip to main content
SpringerLink
Log in

High throughput sequencing of herbaceous peony small RNAs to screen thermo-tolerance related microRNAs

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Herbaceous peony (Paeonia lactiflora Pall.) is an ornamental flower with wide applications for landscape. However, its application potential is greatly restricted because it is prone to heat stress injury. Although there are some studies about thermo-tolerance of P. lactiflora which focused on physiological and transcriptional level, the information on post-transcriptional level is lacked. Here, we chose a thermo-tolerant cultivar ‘Zifengyu’ and a moderately thermo-tolerant cultivar ‘Hongyanzhenghui’ under the natural long summer heat to investigate heat responsive miRNAs by miRNA sequencing. A total of 24,008,974 and 21,981,360 raw reads were generated from ‘Zifengyu’ and ‘Hongyanzhenghui’, respectively, as well as 45,016,796 total sRNAs and 6,297,111 unique sRNAs were obtained. Then 271 conserved and 9 novel miRNAs were identified in ‘Zifengyu’, while 236 conserved and 11 novel miRNAs were identified in ‘Hongyanzhenghui’. Among them, 71 known miRNAs with 272 potential target genes and 3 novel miRNAs with 4 potential target genes were significantly differentially expressed. Expression analysis of the 7 candidate miRNAs previously reported to be regulated by heat stress and their target genes were performed. It showed that miR172c-3p, miR395a, miR397a, miR408-5p and miR827 were up-regulated by heat stress, and expressed much higher in thermo-tolerant cultivar ‘Zifengyu’, suggesting that they might be involved in heat stress response at the post-transcriptional level. These results could provide a better understanding about the thermos-tolerant mechanism of P. lactiflora on post-transcriptional level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221. doi:10.1016/j.cell.2005.04.004

    Article  CAS  PubMed  Google Scholar 

  • Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355. doi:10.1038/nature02871

    Article  CAS  PubMed  Google Scholar 

  • An FM, Chan T (2012) Transcriptome-wide characterization of miRNA-directed and non-miRNA-directed endonucleolytic cleavage using degradome analysis under low ambient temperature in Phalaenopsis aphrodite subsp. formosana. Plant Cell Physiol 53:1737–1750. doi:10.1093/pcp/pcs118

    Article  CAS  PubMed  Google Scholar 

  • Baev V, Milev I, Naydenov M, Vachev T, Apostolova E, Mehterov N, Gozmanva M, Minkov G, Sablok G, Yahubyan G (2014) Insight into small RNA abundance and expression in high- and low-temperature stress response using deep sequencing in Arabidopsis. Plant Physiol Biochem 84:105–114. doi:10.1016/j.plaphy.2014.09.007

    Article  CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5

    Article  CAS  PubMed  Google Scholar 

  • Bottino MC, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L, Hemerly AS, Ferreira, PCG (2013) High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8:e59423. doi:10.1371/journal.pone.0059423

    Article  Google Scholar 

  • Chen L, Ren YY, Zhang VL, Xu VL, Sun FS, Zhang ZY, Wang YW (2012) Genome-wide identification and expression analysis of heatresponsive and novel microRNAs in Populus tomentosa. Gene 504:160–165. doi:10.1016/j.gene.2012.05.034

    Article  CAS  PubMed  Google Scholar 

  • Chen JH, Song YP, Zhang H, Zhang DQ (2013) Genome-wide analysis of gene expression in response to drought stress in Populus simonii. Plant Mol Biol Rep 31(4):946–962

    Article  CAS  Google Scholar 

  • Chen J, Huang P, McCarl BA, Shiva L (2014) Climate change, society, and agriculture: an economic and policy perspective. In: Alfen NKV (ed) Encyclopedia of agriculture and food systems. Academic Press Oxford, Oxford, pp 294–306. doi:10.1016/B978-0-444-52512-3.00001-2

    Chapter  Google Scholar 

  • Chiba Y, Mineta K, Hirai MY, Suzuki Y, Kanaya S, Takahashi H, Onouchi H, Yamaguchi J, Naito S (2013) Changes in mRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol 54:180–194. doi:10.1093/pcp/pcs164

    Article  CAS  PubMed  Google Scholar 

  • Giacomelli JI, Weigel D, Chan RL, Manavella PA (2012) Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol 195:766–773. doi:10.1111/j.1469-8137.2012.04259.x

    Article  CAS  PubMed  Google Scholar 

  • Hackenberg M, Gustafso P, Langridge P, Shi BJ (2015) Differential expression of microRNAs and other small RNAs in barley between water and drought conditions. Plant Biotechnol J 13:2–13. doi:10.1111/pbi.12220

    Article  CAS  PubMed  Google Scholar 

  • Hajdarpašić A, Ruggenthaler P (2012) Analysis of miRNA expression under stress in Arabidopsis thaliana. Bosn J Basic Med Sci 12:169–176

    PubMed  PubMed Central  Google Scholar 

  • Hao ZJ, Wei MR, Gong SJ, Zhao DQ, Tao J (2016) Transcriptome and digital gene expression analysis of herbaceous peony (Paeonia lactiflorapall.) to screen thermo-tolerant related differently expressed genes. Genes Genom 38(12):1201–1215. doi:10.1007/s13258-016-0465-8

    Article  CAS  Google Scholar 

  • Hivrale V, Yun Z, COR P, Jagadeeswaran G, Gowdu K, Kakani VG, Barakat A, Sunkar R (2016) Characterization of drought- and heat-responsive microRNAs in switchgrass. Int J Plant Sci 242:214–223. doi:10.1016/j.plantsci.2015.07.018

    CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207. doi:10.1105/tpc.111.089045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang H, Peng SM, Zhang S, Li XG, Korpelainen H, Li CY (2012) Transcriptional profiling analysis in populus yunnanensis provides insights into molecular mechanisms of sexual differences in salinity tolerance. J Exp Bot 63(10):3709–3726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Q, Wang F, Tan HW, Li MY, Xu ZS, Tan GF, Xiong AS (2015) De novo transcriptome assembly, gene annotation, marker development, and miRNA potential target genes validation under abiotic stresses in Oenanthe javanica. Mol Genet Genom 290:671–683. doi:10.1007/s00438-014-0953-y

    Article  CAS  Google Scholar 

  • Jin WB, Wu FL (2015) Characterization of miRNAs associated with Botrytis cinerea infection of tomato leaves. BMC Plant Biol 15:1. doi:10.1186/s12870-014-0410-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones JD, Henstrand JM, Handa AK, Herrmann KM, Weller SC (1995) Impaired wound induction of 3-deoxy-d-arabino-heptulosonate-7-phosphate (DAHP) synthase and altered stem development in transgenic potato plants expressing a dahp synthase antisense construct. Plant Physiol 108(4):1413–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5:57. doi:10.1371/journal.pbio.0050057

    Article  Google Scholar 

  • Khaksefidi RE, Mirlohi S, Khalaji F, Fakhari Z, Shiran B, Fallahi H, Rafiei F, Budak H, Ebrahimie E (2015) Differential expression of seven conserved microRNAs in response to abiotic stress and their regulatory network in Helianthus annuus. Front. Plant Sci 6:741. doi:10.3389/fpls.2015.00741

    Google Scholar 

  • Koc I, Filiz E, Tombuloglu H (2015) Assessment of miRNA expression profile and differential expression pattern of target genes in cold-tolerant and cold-sensitive tomato cultivars. Biotechnol Biotechnol Equip 29:851–860. doi:10.1080/13102818.2015.1061447

    Article  CAS  Google Scholar 

  • Lai EC (2015) Two decades of miRNA biology: lessons and challenges. RNA 21:675–677. doi:10.1261/rna.051193.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Re. 38:3081–3093

    Article  CAS  Google Scholar 

  • Li RQ, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinform 25:1966–1967. doi:10.1093/bioinformatics/btp336

    Article  CAS  Google Scholar 

  • Li SX, Liu JX, Liu ZY, Li XR, Wu FJ, He YK (2014a) Heat induced tas1 target1 mediates thermotolerance via heat stress transcription factor A1a-directed pathways in Arabidopsis. Plant Cell 26:1764–1780. doi:10.1105/tpc.114.124883

  • Li MY, Wang F, Xu ZS, Jiang Q, Ma J, Tan GF, Xiong AS (2014b) High throughput sequencing of two celery cultivars small RNAs identifies microRNAs involved in temperature stress response. BMC Genom 15:242. doi:10.1186/1471-2164-15-242

  • Lin SI, Santi C, Jobet E, Lacut E, El KN, Karlowski WM, Verdeil JL, Breitler JC, Périn C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (2010) Complex regulation of two target genes encoding spx-mfs proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131. doi:10.1093/pcp/pcq170

    Article  CAS  PubMed  Google Scholar 

  • Liu FL, Wang WJ, Sun XT, Liang ZR, Wang FJ (2014) RNA-Seq revealed complex response to heat stress on transcriptomic level in Saccharina japonica (Laminariales, Phaeophyta). J Appl Phycol 26:1585–1596. doi:10.1007/s10811-013-0188-z

    Article  CAS  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151. doi:10.1111/j.1365-313X.2008.03497.x

    Article  CAS  PubMed  Google Scholar 

  • Lv C, Liu L (2008) Effects of high temperature on physiological and biochemical characteristics of Paeonia lactiflora. J Hunan Agric Univ (Nat Sci) 34:664–667 (in Chinese)

    Google Scholar 

  • Mahale BM, Fakrudin B, Ghosh S, Krishnaraj PU (2013) LNA mediated in situ hybridization of miR171 and miR397a in leaf and ambient root tissues revealed expressional homogeneity in response to shoot heat shock in Arabidopsis thaliana. J Plant Biochem Biotechnol 23:93–103. doi:10.1007/s13562-013-0191-0

    Google Scholar 

  • May P, Liao W, Wu YJ, Shuai B, McCombie WR, Zhang MQ, Liu QA (2013) The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nat Commun 4:405–415. doi:10.1038/ncomms3145

    Article  Google Scholar 

  • Niu L, Fu X, Liu A (2010) Application of herbaceous peony in flower border. North Hortic 4:97–100 (in Chinese)

    Google Scholar 

  • Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen, XM, Triplett BA, Stelly DM, Chen ZJ (2009) Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genom Biol 10:122. doi:10.1186/gb-2009-10-11-r122

    Article  Google Scholar 

  • Pashkovskiy PP, Ryazansky SS (2013) Biogenesis, evolution, and functions of plant microRNAs. Biochem 78:627–637. doi:10.1134/S0006297913060084

    CAS  Google Scholar 

  • Sailaja B, Voleti SR, Subrahmanyam D, Sarla N, Vishnu PV, Bhadana VP, Mangrauthia SK (2014) Prediction and expression analysis of miRNAs associated with heat stress in Oryza sativa. Rice Sci 21:3–12. doi:10.1016/S16726308(13)60164-X

    Article  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 36:1101–1108. doi:10.1038/nprot.2008.73

    Article  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8:517–527. doi:10.1016/j.devcel.2005.01.018

    CAS  Google Scholar 

  • Stief A, Altmann S, Hoffmann K, Pant BD, Scheibl W, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26:1792–1807. doi:10.1105/tpc.114.123851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Ren LP, Cheng Y, Gao JJ, Dong B, Chen SM, Chen FD, Jiang JF (2014) Identification of differentially expressed genes in Chrysanthemum nankingense (Asteraceae) under heat stress by RNA SEq. Gene 552:59–66. doi:10.1016/j.gene.2014.09.013

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Xu L, Wang Y, Yu R, Zhu X, Luo X, Gong Y, Wang R, Limera C, Zhang K, Liu, L (2015) Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genom 16:1. doi:10.1186/s12864-015-1416-5

    Article  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019. doi:10.1105/tpc.104.022830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma SS, Sinha R, Rahman MH, Megha S, Deyholos MK, Kav NN (2014) miRNA-Mediated Posttranscriptional Regulation of Gene Expression in ABR17-Transgenic Arabidopsis thaliana Under Salt Stress. Plant Mol Biol Rep 32:1203–1218. doi:10.1007/s11105-014-0716-2

    Article  CAS  Google Scholar 

  • Wan XL, Zhou Q, Wang YY, Wang WE, Bao MZ, Zhang JW (2015) Identification of heat-responsive genes in carnation (Dianthus caryophyllus L.) by RNA-sEq. Front Plant Sci 6:519. doi:10.3389/fpls.2015.00519

    PubMed  PubMed Central  Google Scholar 

  • Wang Y, Liu W, Shen H, Zhu X, Zhai L, Xu L, Wang R, Gong Y, Limera C, Liu L (2015) Identification of radish (Raphanus sativus L.) miRNAs and their target genes to explore miRNA-mediated regulatory networks in lead (Pb) stress responses by high-throughput sequencing and degradome analysis. Plant Mol Biol Rep 33:358–376. doi:10.1007/s11105-014-0752-y

    Article  CAS  Google Scholar 

  • Wei B, Cai T, Zhang RZ, Li AL, Huo NX, Li S, Gu YQ, Vogel J, Jia JZ, Qi YJ, Mao L (2009) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.). Beauv Funct Integr Genom 9:532–541. doi:10.1007/s10142-009-0128-9

    Google Scholar 

  • Xin MM, Wang Y, Yao YY, Xie CJ, Peng HR, Ni ZF, Sun QX (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123. doi:10.1186/1471-2229-10-123

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin XC, Wang J, Cheng H, Wang XL, Yu DY (2013) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta 237:1213–1225. doi:10.1007/s00425-012-1835-3

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Xu YY, Huan Q, Chong K (2009) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genom 10:1. doi:10.1186/1471-2164-10-449

    Article  CAS  Google Scholar 

  • Zhao T, Li GL, Mi SJ, Li S, Hannon GJ, Wang XJ, Qi YJ (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21:1190–1203. doi:10.1101/gad.1543507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao DQ, Zhou CH, Tao J (2011) Carotenoid accumulation and carotenogenic genes expression during two types of persimmon fruit (Diospyros kaki L.) development. Plant Mol Biol Rep 29:646–654. doi:10.1007/s11105-010-0272-3

    Article  CAS  Google Scholar 

  • Zhao DQ, Gong SJ, Hao ZJ, Tao J (2015a) Identification of miRNAs responsive to Botrytis cinerea in Herbaceous Peony (Paeonia lactiflora Pall.) by high-throughput sequencing. Genes 6:918–934. doi:10.3390/genes6030918

  • Zhao DQ, Han CX, Zhou CH, Tao J (2015b) Shade ameliorates high temperature-induced inhibition of growth in herbaceous peony (Paeonia lactiflora). Int J Agric Biol 17:911–919. doi:10.17957/IJAB/15.0004

Download references

Acknowledgements

This work was supported by the College Natural Science Research of Jiangsu Province (14KJB210011), the Opening Project of Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement (2014014), the Natural Science Foundation of Yangzhou City (YZ2014033), and the Priority Academic Program Development from Jiangsu Government.

Author information

Authors and Affiliations

  1. College of Animal Science and Technology, Yangzhou University, Yangzhou, 225009, People’s Republic of China

    Zhaojun Hao & Ding Liu

  2. Key Laboratory of Crop Genetics and Physiology, College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, 225009, People’s Republic of China

    Zhaojun Hao, Ding Liu, Saijie Gong, Daqiu Zhao & Jun Tao

  3. Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing, 210014, People’s Republic of China

    Daqiu Zhao & Jun Tao

Authors
  1. Zhaojun Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ding Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saijie Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daqiu Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Tao.

Ethics declarations

Conflict of interest

Zhaojun Hao declares that she has no conflict of interest. Ding Liu declares that he has no conflict of interest. Saijie Gong declares that he has no conflict of interest. Daqiu Zhao declares that he has no conflict of interest. Jun Tao declares that he has no conflict of interest.

Research involving animal and human rights

This article does not contain any studies with human subjects or animals performed by any of the authors.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hao, Z., Liu, D., Gong, S. et al. High throughput sequencing of herbaceous peony small RNAs to screen thermo-tolerance related microRNAs. Genes Genom 39, 397–408 (2017). https://doi.org/10.1007/s13258-016-0505-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-016-0505-4

Keywords

Search

Navigation