Small RNA and PARE sequencing in flower bud reveal the involvement of sRNAs in endodormancy release of Japanese pear (Pyrus pyrifolia 'Kosui')
Tóm tắt
In woody perennial plants, including deciduous fruit trees, such as pear, endodormancy is a strategy for surviving the cold winter. A better understanding of the mechanism underlying the endodormancy phase transition is necessary for developing countermeasures against the effects of global warming. In this study, we analyzed the sRNAome of Japanese pear flower buds in endodormant and ecodormant stages over two seasons by implementing of RNA-seq and degradome-sequencing. We identified 137 conserved or less conserved miRNAs and 50 pear-specific miRNAs. However, none of the conserved microRNAs or pear-specific miRNAs was differentially expressed between endodormancy and ecodormancy stages. On the contrast, 1540 of 218,050 loci that produced sRNAs were differentially expressed between endodormancy and ecodormancy, suggesting their potential roles on the phase transition from endodormancy to ecodomancy. We also characterized a multifunctional miRNA precursor MIR168, which produces two functional miR168 transcripts, namely miR168.1 and miR168.2; cleavage events were predominantly mediated by the non-conserved variant miR168.2 rather than the conserved variant miR168.1. Finally, we showed that a TAS3 trans-acting siRNA triggered phased siRNA within the ORF of one of its target genes, AUXIN RESPONSE FACTOR 4, via the analysis of phased siRNA loci, indicating that siRNAs are able to trigger phased siRNAs in pear. We analyzed the sRNAome of pear flower bud during dormant phase transition. Our work described the sRNA profiles of pear winter buds during dormant phase transition, showing that dormancy release is a highly coordinated physiological process involving the regulation of sRNAs.
Tài liệu tham khảo
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–97.
Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33.
Axtell M, Merchant S. Classification and comparison of small RNAs from plants. Annu Rev Plant Biol. 2013;64:137–59.
Fei Q, Xia R, Meyers B. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell. 2013;25(7):2400–15.
Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell. 2009;136(4):669–87.
Matzke M, Kanno T, Claxinger L, Huettel B, Matzke A. RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol. 2009;21(3):367–76.
Law J, Jacobsen S. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11(3):204–20.
Lee T, Gurazada S, Zhai J, Li S, Simon S, Matzke M, Chen X, Meyers B. RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics. 2012;7(7):781–95.
Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory A, Hilbert J, Bartel D, Crete P. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell. 2004;16(1):69–79.
Wu L, Mao L, Qi Y. Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 2012;160(2):990–9.
Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. DNA methylation mediated by a microRNA pathway. Mol Cell. 2010;38(3):465–75.
Wu G, Poethig R. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development. 2006;133(18):3539–47.
Aukerman M, Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell. 2003;15(11):2730–41.
Wu G, Park M, Conway S, Wang J, Weigel D, Poethig R. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell. 2009;138(4):750–9.
Mallory A, Bartel D, Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell. 2005;17(5):1360–75.
Wu M, Tian Q, Reed J. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 2006;133(21):4211–8.
Kutter C, Schob H, Stadler M, Meins F, Si-Ammour A. MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell. 2007;19(8):2417–29.
Wang Y, Itaya A, Zhong X, Wu Y, Zhang J, van der Knaap E, Olmstead R, Qi Y, Ding B. Function and evolution of a microRNA that regulates a Ca2 + −ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. Plant Cell. 2011;23(9):3185–203.
Wu L, Liu D, Wu J, Zhang R, Qin Z, Liu D, Li A, Fu D, Zhai W, Mao L. Regulation of FLOWERING LOCUS T by a microRNA in Brachypodium distachyon. Plant Cell. 2013;25(11):4363–77.
Hu J, Zhou Y, He F, Dong X, Liu L, Coupland G, Turck F, de Meaux J. miR824-regulated AGAMOUS-LIKE16 contributes to flowering time repression in Arabidopsis. Plant Cell. 2014;26(5):2024–37.
Qin Z, Li C, Mao L, Wu L. Novel insights from non-conserved microRNAs in plants. Front Plant Sci. 2014;5:586.
Xia R, Zhu H, An Y, Beers E, Liu Z. Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol. 2012;13(6):R47.
Visser M, van der Walt A, Maree H, Rees D, Burger J. Extending the sRNAome of apple by next-generation sequencing. PLoS One. 2014;9(4):e95782.
Ma C, Lu Y, Bai S, Zhang W, Duan X, Meng D, Wang Z, Wang A, Zhou Z, Li T. Cloning and characterization of miRNAs and their targets, including a novel miRNA-targeted NBS-LRR protein class gene in apple (Golden Delicious). Mol Plant. 2014;7(1):218–30.
Niu Q, Qian M, Liu G, Yang F, Teng Y. A genome-wide identification and characterization of mircoRNAs and their targets in ‘Suli’ pear (Pyrus pyrifolia white pear group). Planta. 2013;238(6):1095–112.
Tamura F, Tanabe K, Itai A. Effect of interruption of chilling on bud break in Japanese pear. Acta Horticult. 1995;395:135–40.
Bai S, Saito T, Sakamoto D, Ito A, Fujii H, Moriguchi T. Transcriptome analysis of Japanese pear (Pyrus pyrifolia Nakai) flower buds trransitioning through endodormancy. Plant Cell Physiol. 2013;54(7):1132–51.
Sugiura T, Honjo H. A dynamic model for predicting the flowering date developed using an endodormancy break model and a flower bud development model in Japanese pear. J Agric Meteorol. 1997;54(5):897–900.
Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 2005;33:D121–4.
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan M, Tao S, Korban S, Wang H, et al. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res. 2013;23(2):396–408.
Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
Axtell M. ShortStack: Comprehensive annotation and quantification of small RNA genes. RNA. 2013;19(6):740–51.
Folkes L, Moxon S, Woolfenden H, Stocks M, Szittya G, Dalmay T, Moulton V. PAREsnip: a tool for rapid genome-wide discovery of small RNA/target interactions evidenced through degradome sequencing. Nucleic Acids Res. 2012;40(13):e103.
Stocks M, Moxon S, Mapleson D, Woolfenden H, Mohorianu I, Folkes L, Schwach F, Dalmay T, Moulton V. The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets. Bioinformatics. 2012;28(15):2059–61.
Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014;42(D1):D68–73.
Robinson M, McCarthy D, Smyth G. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40.
Vaucheret H, Vazquez F, Crete P, Bartel DP. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev. 2004;18(10):1187–97.
Dunoyer P, Brosnan C, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O. An endogenous, systemic RNAi pathway in plants. EMBO J. 2010;29(10):1699–712.
Slotkin R, Freeling M, Lisch D. Mu killer causes the heritable inactivation of the Mutator family of transposable elements in Zea mays. Genetics. 2003;165(2):781–97.
Arikit S, Xia R, Kakrana A, Huang K, Zhai J, Yan Z, Valdés-López O, Prince S, Musket TA, Nguyen HT, et al. An atlas of soybean small RNAs identifies phased siRNAs from hundreds of coding genes. Plant Cell. 2014;26(12):4584–601.
Lopez JA, Sun Y, Blair PB, Mukhtar MS. TCP three-way handshake: linking developmental processes with plant immunity. Trends Plant Sci. 2015;20(4):238–45.
Jones-Rhoades M, Bartel D, Bartel B. MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol. 2006;57:19–53.
Liu G, Li W, Zheng P, Xu T, Chen L, Liu D, Hussain S, Teng Y. Transcriptomic analysis of ‘Suli’ pear (Pyrus pyrifolia white pear group) buds during the dormancy by RNA-Seq. BMC Genomics. 2013;13(1):700.
McCormick KP, Willmann MR, Meyers BC. Experimental design, preprocessing, normalization and differential expression analysis of small RNA sequencing experiments. Silence. 2011;2(1):2.
Niu Q, Li J, Cai D, Qian M, Jia H, Bai S, Hussain S, Liu G, Teng Y, Zheng X. Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. J Exp Bot. 2015;67(1):239–57.
Meyers B, Axtell M, Bartel B, Bartel D, Baulcombe D, Bowman J, Cao X, Carrington J, Chen X, Green P, et al. Criteria for annotation of plant microRNAs. Plant Cell. 2008;20(12):3186–90.
Allen E, Xie Z, Gustafson A, Sung G, Spatafora J, Carrington J. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet. 2004;36(12):1282–90.
German M, Luo S, Schroth G, Meyers B, Green P. Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc. 2009;4(3):356–62.
Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics. 2005;21(16):3448–9.