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Regulation of synchronism by abscisic-acid-responsive small noncoding RNAs during somatic embryogenesis in larch (Larix leptolepis)

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Abstract

Low levels of abscisic acid (ABA) are associated with embryo asynchronism during somatic embryogenesis. Small non-coding RNAs (sncRNAs) are emerging as key regulators of embryogenesis. To investigate the roles of sncRNAs in regulating the synchronism of somatic embryogenesis in Larix leptolepis, we examined the endogenous “sncRNAome” in synchronous and asynchronous embryos. Non-redundant sRNAs 24 nt in length were overrepresented in both synchronous and asynchronous embryos, while the majority of redundant sRNAs were 24 nt long in synchronous embryos and 21 nt long in asynchronous embryos. Many more non-redundant unknown sRNAs were expressed in synchronous embryos than in asynchronous embryos, indicating that many sRNAs might participate in the regulation of synchronism during larch somatic embryogenesis. However, the proportion of sRNAs that were miRNAs was higher in asynchronous embryos than in synchronous embryos, and their expression was much higher in asynchronous embryos. Although the proportion of sRNAs that matched repeat regions (ra-siRNA) was higher in asynchronous embryos than in synchronous embryos, the ratio of 24-nt ra-siRNAs to total sRNAs was much lower in asynchronous embryos than in synchronous embryos. Further analysis suggested that miRNAs exemplified by miR156 might participate in the regulation of embryo synchronism in larch, which causes a large number of transcripts encoding differentiation-promoting factors to be down regulated. Therefore, we speculate that sncRNAs induced by ABA inhibit the precocious expression of differentiation-promoting factors, thereby regulating the synchronism of somatic embryogenesis.

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References

  • Ammirato P (1974) The effects of abscisic acid on the development of somatic embryos from cells of caraway (Carum carvi L.). Botanical Gazette 59(4):328–337

    Google Scholar 

  • Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123(7):1279–1291

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen W, Gai Y, Liu S, Wang R, Jiang X (2010) Quantitative analysis of cytokinins in plants by high performance liquid chromatography: electronspray ionization ion trap mass spectrometry. J Integr Plant Biol 52(10):925–932

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421(6924):740–743

    Article  CAS  PubMed  Google Scholar 

  • Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10(2):94–108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gutmann M, Von Aderkas P, Label P, Lelu MA (1996) Effects of abscisic acid on somatic embryo maturation of hybrid larch. J Exp Bot 47(12):1905–1917

    Article  CAS  Google Scholar 

  • Hakman I, Hallberg H, Palovaara J (2009) The polar auxin transport inhibitor NPA impairs embryo morphology and increases the expression of an auxin efflux facilitator protein PIN during Picea abies somatic embryo development. Tree Physiol 29(4):483–496

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39(1):152–157

    Article  Google Scholar 

  • Label P, Lelu MA (1994) Influence of exogenous abscisic acid on germination and plantlet conversion frequencies of hybrid larch somatic embryos (Larix × leptoeuropaea). Plant Growth Regul 15(2):175–182

    Article  CAS  Google Scholar 

  • Label P, Lelu MA (2000) Exogenous abscisic acid fate during maturation of hybrid larch (Larix × leptoeuropaea) somatic embryos. Physiol Plant 109(4):456–462

    Article  CAS  Google Scholar 

  • Lelu M, Bastien C, Klimaszewska K, Ward C, Charest P (1994) An improved method for somatic plantlet production in hybrid larch (Larix × leptoeuropaea): part 1. Somatic embryo maturation. Plant Cell, Tissue Organ Cult 36(1):107–115

    Article  CAS  Google Scholar 

  • Li W-F, Zhang S-G, Han S-Y, Wu T, Zhang J-H, Qi L-W (2013) Regulation of LaMYB33 by miR159 during maintenance of embryogenic potential and somatic embryo maturation in Larix kaempferi (Lamb.) Carr. Plant Cell, Tissue Organ Cult 113(1):131–136

    Google Scholar 

  • Liu S, Chen W, Qu L, Gai Y, Jiang X (2013) Simultaneous determination of 24 or more acidic and alkaline phytohormones in femtomole quantities of plant tissues by high-performance liquid chromatography–electrospray ionization–ion trap mass spectrometry. Anal Bioanal Chem 405(4):1257–1266

    Article  CAS  PubMed  Google Scholar 

  • Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21(3):367–376

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20(2):55

    Article  CAS  Google Scholar 

  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678–2692

    Article  CAS  PubMed  Google Scholar 

  • Penfield S, Hall A (2009) A role for multiple circadian clock genes in the response to signals that break seed dormancy in Arabidopsis. The Plant Cell Online 21(6):1722–1732

    Article  CAS  Google Scholar 

  • Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18(19):2368–2379

    Article  CAS  PubMed  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49(4):592–606

    Article  CAS  PubMed  Google Scholar 

  • Ross J, O’Neill D (2001) New interactions between classical plant hormones. Trends Plant Sci 6(1):2–4

    Article  CAS  PubMed  Google Scholar 

  • Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54(4):608–620

    Article  CAS  PubMed  Google Scholar 

  • Schwach F, Moxon S, Moulton V, Dalmay T (2009) Deciphering the diversity of small RNAs in plants: the long and short of it. Brief Funct Genomic Proteomic 8(6):472–481

    Article  CAS  PubMed  Google Scholar 

  • Schwarzerova K, Vondrakova Z, Fischer L, Borikova P, Bellinvia E, Eliasova K, Havelkova L, Fiserova J, Vagner M, Opatrny Z (2010) The role of actin isoforms in somatic embryogenesis in Norway spruce. BMC Plant Biol 10:89

    Article  PubMed Central  PubMed  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687

    Article  CAS  PubMed  Google Scholar 

  • Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155(4):1871–1884

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Woodger FJ, Millar A, Murray F, Jacobsen JV, Gubler F (2003) The role of GAMYB transcription factors in GA-regulated gene expression. J Plant Growth Regul 22(2):176–184

    Article  CAS  Google Scholar 

  • Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37(3):916–930

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto A, Kagaya Y, Toyoshima R, Kagaya M, Takeda S, Hattori T (2009) Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. Plant J 58(5):843–856

    Article  CAS  PubMed  Google Scholar 

  • Yang JH, Han SJ, Yoon EK, Lee WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34(6):1892–1899

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang J, Zhang S, Han S, Wu T, Li X, Li W, Qi L (2012) Genome-wide identification of microRNAs in larch and stage-specific modulation of 11 conserved microRNAs and their targets during somatic embryogenesis. Planta 236(2):647–657

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Wu T, Li L, Han S, Li X, Zhang S, Qi L (2013) Dynamic expression of small RNA populations in larch (Larix leptolepis). Planta 237(1):89–101

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31330017; 31300566), and the National High Technology Research and Development Program of China (Grant Nos. 2011AA100203; 2013AA102704).

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Authors and Affiliations

  1. Laboratory of Cell Biology, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

    Jun-Hong Zhang, Shou-Gong Zhang, Shui-Gen Li, Wan-Feng Li, Xin-Min Li & Li-Wang Qi

  2. Nurturing Station for the State Key Laboratory of Subtropical Silviculture, Zhejiang Agriculture and Forestry University, Lin’an, Hangzhou, 311300, Zhejiang, People’s Republic of China

    Jun-Hong Zhang

  3. Key Laboratory of Research Institute of Forest Ecology and Protection, Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

    Su-Ying Han

  4. Department of Pathology and Laboratory Medicine, University of California at Los Angeles, 1000 Veteran Ave, Los Angeles, CA, 90095, USA

    Xin-Min Li

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  1. Jun-Hong Zhang
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  2. Shou-Gong Zhang
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  3. Shui-Gen Li
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  4. Su-Ying Han
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  5. Wan-Feng Li
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Correspondence to Li-Wang Qi.

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Jun-Hong Zhang, Shou-Gong Zhang and Shui-Gen Li have contributed equally to this work.

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Zhang, JH., Zhang, SG., Li, SG. et al. Regulation of synchronism by abscisic-acid-responsive small noncoding RNAs during somatic embryogenesis in larch (Larix leptolepis). Plant Cell Tiss Organ Cult 116, 361–370 (2014). https://doi.org/10.1007/s11240-013-0412-1

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  • DOI: https://doi.org/10.1007/s11240-013-0412-1

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