Identification and Expression Analysis of microRNAs in Response to Dormancy Release During Cold Storage of Lilium pumilum Bulbs

Abstract

MicroRNAs (miRNAs) play important roles in post-transcriptional regulation as well as in various biological and metabolic processes. Lilium pumilum originated from northern China with a high ornamental value, and is important for Lilium resistance breeding. The dormancy of the bulbs has a serious effect on flowering quality. In this study, the miRNAs from samples at 0 days (S1 stage), 30 days (S2 stage), 60 days (S3 stage) and 90 days (S4 stage) of cold storage were sequenced to reveal the dormancy mechanism of Lilium pumilum. Through ultrastructural observation and physiological index measurement, we found that Lilium pumilum bulbs were released from dormancy during low-temperature storage. We further conducted miRNAs sequencing; a total of 17 conserved miRNAs were identified from 12 families, two nonconserved miRNAs were found that belonged to two families, and 38 novel miRNAs were predicted. MiRNA-target pairs analysis showed that some biological processes, including antioxidant reactions, epigenetic modification and abiotic stress, were induced in response to low-temperature conditions. Some transcription factors, plant hormone signalling pathways, and enzymes involved in plant growth and development were also activated to break the bulb dormancy. The study initially revealed the complex regulatory mechanisms of miRNAs for dormancy release during low-temperature storage. Comprehensive sequence information and target gene data were obtained by miRNAs sequencing, which determined that miRNAs regulation of bulb dormancy release in low temperature.

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Availability of Data and Material

All the data supporting our findings are contained within the manuscript.

Abbreviations

ABA:

Abscisic acid

GA:

Gibberellin

ETH:

Ethylene

IAA:

Auxin

BR:

Brassinolide

ROS:

Reactive oxygen species

TPM:

Transcripts Per Million

AGO1:

ARGONAUTE1

SPL:

Squamosa promoter-binding-like protein

References

  1. Bai S, Saito T, Ito A, Tuan PA, Xu Y, Teng Y, Moriguchi T (2016) Small RNA and PARE sequencing in flower bud reveal the involvement of sRNAs in endodormancy release of Japanese pear (Pyrus pyrifolia 'Kosui'). BMC Genomics 17:230. https://doi.org/10.1186/s12864-016-2514-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Damodharan S, Zhao D, Arazi T (2016) A common miRNA160-based mechanism regulates ovary patterning, floral organ abscission and lamina outgrowth in tomato. Plant J 86:458–471. https://doi.org/10.1111/tpj.13127

    CAS  Article  PubMed  Google Scholar 

  3. Debernardi JM et al (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79:413–426. https://doi.org/10.1111/tpj.12567

    CAS  Article  PubMed  Google Scholar 

  4. Eremina M, Rozhon W, Poppenberger B (2016) Hormonal control of cold stress responses in plants. Cell Mol Life Sci 73:797–810. https://doi.org/10.1007/s00018-015-2089-6

    CAS  Article  PubMed  Google Scholar 

  5. Fang L, Jiayan W, Xiaoli W, Yunwei Z (2013) The apical bud cell ultra-structure changes of lilium pumilum bulbs during breaking dormancy under refrigerated condition. Acta Hortic Sin 40:1110–1118

    Google Scholar 

  6. Gai S, Zhang Y, Liu C, Zhang Y, Zheng G (2013) Transcript profiling of paoenia ostii during artificial chilling induced dormancy release identifies activation of ga pathway and carbohydrate metabolism. PLoS ONE 8:e55297. https://doi.org/10.1371/journal.pone.0055297

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Hamilton A, Voinnet O, Chappell L, Baulcombe D (2015) Two classes of short interfering RNA in RNA silencing. Embo J 34:2590. https://doi.org/10.15252/embj.201570050

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. He D, Wang Q, Wang K, Yang P (2015) Genome-wide dissection of the microRNA expression profile in rice embryo during early stages of seed germination. PLoS ONE 10:e0145424. https://doi.org/10.1371/journal.pone.0145424

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Higashi Y, Takechi K, Takano H, Takio S (2013) Involvement of microRNA in copper deficiency-induced repression of chloroplastic CuZn-superoxide dismutase genes in the moss Physcomitrella patens. Plant Cell Physiol 54:1345–1355. https://doi.org/10.1093/pcp/pct084

    CAS  Article  PubMed  Google Scholar 

  10. Holdsworth MJ, Finchsavage WE, Grappin P, Job D (2008) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13:7–13

    CAS  Article  Google Scholar 

  11. Howe GT, Horvath DP, Dharmawardhana P, Priest HD, Mockler TC, Strauss SH (2015) Extensive transcriptome changes during natural onset and release of vegetative bud dormancy in Populus. Front Plant Sci 6:989. https://doi.org/10.3389/fpls.2015.00989

    Article  PubMed  PubMed Central  Google Scholar 

  12. Huo H, Wei S, Bradford KJ (2016) DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci USA 113:E2199–2206. https://doi.org/10.1073/pnas.1600558113

    CAS  Article  PubMed  Google Scholar 

  13. Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2016) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101. https://doi.org/10.1111/jipb.12513

    CAS  Article  Google Scholar 

  14. Kawashima CG et al (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876. https://doi.org/10.1111/j.1365-313X.2011.04547.x

    CAS  Article  PubMed  Google Scholar 

  15. Kendall SL, Hellwege A, Marriot P, Whalley C, Graham IA, Penfield S (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell 23:2568–2580. https://doi.org/10.1105/tpc.111.087643

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Kim JY, Lee HJ, Jung HJ, Maruyama K, Suzuki N, Kang H (2010) Overexpression of microRNA395c or 395e affects differently the seed germination of Arabidopsis thaliana under stress conditions. Planta 232:1447–1454. https://doi.org/10.1007/s00425-010-1267-x

    CAS  Article  PubMed  Google Scholar 

  17. Li D et al (2013) Deep sequencing of maize small RNAs reveals a diverse set of microRNA in dry and imbibed seeds. PLoS ONE 8:e55107. https://doi.org/10.1371/journal.pone.0055107

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Li J et al (2012) miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220. https://doi.org/10.1186/1471-2229-12-220

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146. https://doi.org/10.1111/j.1365-313X.2007.03218.x

    CAS  Article  PubMed  Google Scholar 

  20. Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen HA, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62:416–428. https://doi.org/10.1111/j.1365-313X.2010.04164.x

    CAS  Article  PubMed  Google Scholar 

  21. Liu X, Wang Q, Gu J, Lu Y (2014) Vernalization of Oriental hybrid lily 'Sorbonne': changes in physiology metabolic activity and molecular mechanism. Mol Biol Rep 41:6619–6634. https://doi.org/10.1007/s11033-014-3545-3

    CAS  Article  PubMed  Google Scholar 

  22. Ma C, Burd S, Lers A (2015) miR408 is involved in abiotic stress responses in Arabidopsis. Plant J 84:169–187. https://doi.org/10.1111/tpj.12999

    CAS  Article  PubMed  Google Scholar 

  23. Ma Z, Marsolais F, Bykova NV, Igamberdiev AU (2016) Nitric oxide and reactive oxygen species mediate metabolic changes in barley seed embryo during germination. Front Plant Sci 7:138. https://doi.org/10.3389/fpls.2016.00138

    Article  PubMed  PubMed Central  Google Scholar 

  24. Maksymiec W, Wianowska D, Dawidowicz AL, Radkiewicz S, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346. https://doi.org/10.1016/j.jplph.2005.01.013

    CAS  Article  PubMed  Google Scholar 

  25. Mazzitelli L et al (2007) Co-ordinated gene expression during phases of dormancy release in raspberry (Rubus idaeus L.) buds. J Exp Bot 58:1035–1045. https://doi.org/10.1093/jxb/erl266

    CAS  Article  PubMed  Google Scholar 

  26. Meng Y, Shuai H, Luo X, Chen F, Zhou W, Yang W, Shu K (2016) Karrikins: regulators involved in phytohormone signaling networks during seed germination and seedling development. Front Plant Sci 7:2021. https://doi.org/10.3389/fpls.2016.02021

    Article  PubMed  Google Scholar 

  27. Qiao YX, Zhang YP, Chen C, Chen MM (2010) Relationship between breaking of dormancy and antioxidative systems enzymes in low temperature treatment in bulbs of Oriental Lily 'Sorbonne' Southwest China. J Agric Sci 23:161–163. https://doi.org/10.16213/j.cnki.scjas.2010.01.048

    Article  Google Scholar 

  28. Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606. https://doi.org/10.1111/j.1365-313X.2006.02980.x

    CAS  Article  PubMed  Google Scholar 

  29. Su L, Lan Q, Pritchard HW, Xue H, Wang X (2016) Reactive oxygen species induced by cold stratification promote germination of Hedysarum scoparium seeds. Plant Physiol Biochem 109:406–415. https://doi.org/10.1016/j.plaphy.2016.10.025

    CAS  Article  PubMed  Google Scholar 

  30. Sun H, Li T, Li Y (2006) Changes of endogenous hormones in Lilium davidii var. unicolor bulbs during bulb development and storage at low temperature for dormancy release. Bul Bot Res 26:570–576

    CAS  Google Scholar 

  31. Sun HM, Silva JATD, Li YF, Li TL (2007) Effects of Low temperature on dormancy release in lily bulbs floriculture & ornamental. Biotechnology 1:41–45

    Google Scholar 

  32. Tripathi RK, Goel R, Kumari S, Dahuja A (2017) Genomic organization, phylogenetic comparison, and expression profiles of the SPL family genes and their regulation in soybean. Dev Genes Evol 227:101–119. https://doi.org/10.1007/s00427-017-0574-7

    CAS  Article  PubMed  Google Scholar 

  33. Tsuji H et al (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444. https://doi.org/10.1111/j.1365-313X.2006.02795.x

    CAS  Article  PubMed  Google Scholar 

  34. Vaucheret H, Mallory AC, Bartel DP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22:129–136. https://doi.org/10.1016/j.molcel.2006.03.011

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687. https://doi.org/10.1016/j.cell.2009.01.046

    CAS  Article  PubMed  Google Scholar 

  36. Wang W, Su X, Tian Z, Liu Y, Zhou Y, He M (2018) Transcriptome profiling provides insights into dormancy release during cold storage of Lilium pumilum. BMC Genomics 19:196. https://doi.org/10.1186/s12864-018-4536-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Wei LQ, Yan LF, Wang T (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12:R53. https://doi.org/10.1186/gb-2011-12-6-r53

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475. https://doi.org/10.1016/j.molcel.2010.03.008

    CAS  Article  PubMed  Google Scholar 

  39. Xia J, Wang X, Perroud PF, He Y, Quatrano R, Zhang W (2016) Endogenous small-noncoding RNAs and potential functions in desiccation tolerance in physcomitrella patens. Sci Rep 6:30118. https://doi.org/10.1038/srep30118

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Xu R-Y, Niimi Y, Han D-S (2006) Changes in endogenous abscisic acid and soluble sugars levels during dormancy-release in bulbs of Lilium rubellum. Sci Hortic 111:68–72. https://doi.org/10.1016/j.scienta.2006.08.004

    CAS  Article  Google Scholar 

  41. Zhang CH, Zhang BB, Ma RJ, Yu ML, Guo SL, Guo L (2015) Isolation and expression analysis of four HD-ZIP III family genes targeted by microRNA166 in peach. Genet Mol Res 14:14151–14161. https://doi.org/10.4238/2015.October.29.37

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

This study was financially supported by National Natural Science Foundation of China (31470698). We thank Prof. Yunwei Zhou and Miao He for their help and support, we would like to acknowledge Xiaoxia Su for guidance and sincerely thank the editors and reviewers for their patient work.

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WW and LY designed the research and wrote the manuscript. XS provided guidance on the experiment. YZ and MH reviewed and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Miao He.

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Zhou, Y., Wang, W., Yang, L. et al. Identification and Expression Analysis of microRNAs in Response to Dormancy Release During Cold Storage of Lilium pumilum Bulbs. J Plant Growth Regul 40, 388–404 (2021). https://doi.org/10.1007/s00344-020-10108-1

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Keywords

  • Lilium pumilum
  • miRNAs
  • Low temperature
  • Dormancy release