Advertisement

Genes & Genomics

, Volume 40, Issue 8, pp 801–817 | Cite as

In silico identification and computational characterization of endogenous small interfering RNAs from diverse grapevine tissues and stages

  • Xudong Zhu
  • Songtao Jiu
  • Xiaopeng Li
  • Kekun Zhang
  • Mengqi Wang
  • Chen Wang
  • Jinggui Fang
Research Article

Abstract

Small interfering RNAs (siRNAs) are effectors of regulatory pathways underlying plant development, metabolism, and stress- and nutrient-signaling regulatory networks. The endogenous siRNAs are generally not conserved between plants; consequently, it is necessary and important to identify and characterize siRNAs from various plants. To address the nature and functions of siRNAs, and understand the biological roles of the huge siRNA population in grapevine (Vitis vinifera L.). The high-throughput sequencing technology was used to identify a large set of putative endogenous siRNAs from six grapevine tissues/organs. Subsequently, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis was performed to classify the target genes of siRNA. In total, 520,519 candidate siRNAs were identified and their expression profiles exhibited typical temporal characters during grapevine development. In addition, we identified two grapevine trans-acting siRNA (TAS) gene homologs (VvTAS3 and VvTAS4) and the derived trans-acting siRNAs (tasiRNAs) that could target grapevine auxin response factor (ARF) and myeloblastosis (MYB) genes. Furthermore, the GO and KEGG analysis of target genes showed that most of them covered a broad range of functional categories, especially involving in disease-resistance process. The large-scale and completely genome-wide level identification and characterization of grapevine endogenous siRNAs from the diverse tissues by high throughput technology revealed the nature and functions of siRNAs in grapevine.

Keywords

Grapevine Endogenous siRNA High-throughput Target genes 

Notes

Acknowledgements

This research was supported by Project Funded by the Natural Science Foundation of China (NSFC) (Nos. 31672131, 31401846 and 31301759), China Postdoctoral Science Foundation Funded Project (2016M590465). Opening Project of State Key Laboratory of Crop Genetics and Germplasm Enhancement (ZW2014009).

Compliance with ethical standards

Conflict of interest

Xudong Zhu declares that he has no conflict of interest. Songtao Jiu declares that he has no conflict of interest. Xiaopeng Li declares that he has no conflict of interest. Kekun Zhang declares that he has no conflict of interest. Mengqi Wang declares that he has no conflict of interest. Chen Wang declares that he has no conflict of interest. Jinggui Fang declares that he has no conflict of interest.

Ethical approval

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

References

  1. Allen E, Xie ZX, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221CrossRefPubMedGoogle Scholar
  2. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297CrossRefPubMedGoogle Scholar
  3. Bentley DR (2006) Whole-genome re-sequencing. Curr Opin Genet Dev 16:545–552CrossRefPubMedGoogle Scholar
  4. Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143:1347–1361CrossRefPubMedPubMedCentralGoogle Scholar
  5. Carra A, Mica E, Gambino G, Pindo M, Moser C, Pè ME, Schubert A (2009) Cloning and characterization of small non-coding RNAs from grapevine. Plant J 59:750–763CrossRefPubMedGoogle Scholar
  6. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen HM, Li HY, Wu SH (2007) Bioinformatic prediction and experimental validation of a microRNA-directed tandem trans-acting siRNA cascade in Arabidopsis. Proc Natl Acad Sci 104:3318–3323CrossRefPubMedGoogle Scholar
  8. Cutanda-Perez MC, Ageorges A, Gomez C, Vialet S, Terrier N, Romieu C, Torregrosa L (2009) Ectopic expression of VlmybA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport. Plant Mol Biol 69:633–648CrossRefPubMedGoogle Scholar
  9. Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J (2009) The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiol 151:1513–1530CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXINRESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16:939–944CrossRefPubMedGoogle Scholar
  11. Gambino G, Perrone I, Carra A, Chitarra W, Boccacci P, Marinoni DT, Barberis M, Maghuly F, Laimer M, Gribaudo I (2010) Transgene silencing in grapevines transformed with GFLV resistance genes: analysis of variable expression of transgene, siRNAs production and cytosine methylation. Transgenic Res 19(1):17–27CrossRefPubMedGoogle Scholar
  12. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C et al (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32(Database issue):D258–D261Google Scholar
  13. Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, de Menezes RX, Boer JM, van Ommen GJ, den Dunnen JT (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36:e141CrossRefPubMedPubMedCentralGoogle Scholar
  14. Howell MD, Fahlgren N, Chapman EJ, Cumbie JS, Sullivan CM, Givan SA, Kasschau KD, Carrington JC (2007) Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA-and tasiRNA-directed targeting. Plant Cell 19:926–942CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132CrossRefPubMedPubMedCentralGoogle Scholar
  16. Jagadeeswaran G, Nimmakayala P, Zheng Y, Gowdu K, Reddy UK, Sunkar R (2012) Characterization of the small RNA component of leaves and fruits from four different cucurbit species. BMC Genom 13(1):329CrossRefGoogle Scholar
  17. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53CrossRefPubMedGoogle Scholar
  18. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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(3):e57CrossRefPubMedPubMedCentralGoogle Scholar
  20. Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246CrossRefPubMedPubMedCentralGoogle Scholar
  21. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci 103:18002–18007CrossRefPubMedGoogle Scholar
  22. Li D, Wang L, Liu X, Cui D, Chen T, Zhang H, Jiang C, Xu C, Li P, Li S et al (2013) Deep sequencing of maize small RNAs reveals a diverse set of MicroRNA in dry and imbibed seeds. PLoS ONE 8(1):e55107CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lu C, Tej SS, Luo S, Handenschild CD, Meyers BC, Green PJ (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569CrossRefPubMedGoogle Scholar
  24. Luo QJ, Mittal A, Jia F, Rock CD (2012) An autoregulatory feedback loop involving PAP1 and TAS4in response to sugars in Arabidopsis. Plant Mol Biol 80:117–129CrossRefPubMedGoogle Scholar
  25. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C et al (2008) Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mica E, Piccolo V, Delledonne M, Ferrarini A, Pezzotti M, Casati C, Fabbro CD, Valle G, Policriti A, Morgante M et al (2010) Correction: high throughput approaches reveal splicing of primarymicroRNA transcripts and tissue specific expression of mature microRNAs in Vitis vinifera. BMC Genom 11:109CrossRefGoogle Scholar
  27. Miozzi L, Gambino L, Burgyan J, Pantaleo V (2013) Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol Plant Pathol 14(1):30–43CrossRefPubMedGoogle Scholar
  28. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133(1):128–141CrossRefPubMedGoogle Scholar
  29. Morin RD, Aksay G, Dolgosheina E, Ebhardt HA, Magrini V, Mardis ER, Sahinalp SC, Unrau PJ (2008) Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18(4):571–584CrossRefPubMedPubMedCentralGoogle Scholar
  30. Moxon S, Jing R, Szittya G, Schwach F, Rusholme-Pilcher RL, Moulton V, Dalmay T (2008) Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome Res 18:1602–1609CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pang M, Woodward AW, Agarwal V, Guan X, Ha M, Ramachandran V, Chen X, 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.). Genome Biol 10:R122CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high throughput sequencing and degradome analysis. Plant J 62:960–976PubMedGoogle Scholar
  33. Qiu CX, Xie FL, Zhu YY, Guo K, Huang SQ, Li N, Zhi MY (2007) Computational identification of microRNAs and their targets in Gossypium hirsutum expressed sequence tags. Gene 395:49–61CrossRefPubMedGoogle Scholar
  34. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rock CD (2013) Trans-acting small interfering RNA4: key to nutraceutical synthesis in grape development? Trends Plant Sci 18(11):601–610CrossRefPubMedGoogle Scholar
  36. Ron M, Alandete SM, Eshed WL, Fletcher JC, McCormick S (2010) Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24(10):1010–1021CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ronemus M, Vaughn MW, Martienssen RA (2006) MicroRNA-targeted and small interfering RNA-mediated mRNA degradation is regulated by Argonaute, Dicer, and RNA-dependent RNA polymerase in Arabidopsis. Plant Cell 18:1559–1574CrossRefPubMedPubMedCentralGoogle Scholar
  38. Somvanshi P, Singh V, Seth PK (2009) High throughput prediction and analysis of small interfering RNA from the 5′UTR and capsid genes of flavivirus through in silico strategies. Interdiscip Sci 1(4):298–302CrossRefPubMedGoogle Scholar
  39. Song CN, Wang C, Zhang CQ, Nicholas KK, Yu HP, Ma ZQ, Fang JG (2010) Deep sequencing discovery of new and conserved microRNAs in trifoliate orange (Citrus trifoliate). BMC Genom 11:431CrossRefGoogle Scholar
  40. Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Semin Cell Dev Biol 21(8):805–811CrossRefPubMedGoogle Scholar
  41. Sunkar R, Girke T, Zhu JK (2005) Identification and characterization of endogenous small interfering RNAs from rice. Nucleic Acids Res 33(14):4443–4454CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12(7):301–309CrossRefPubMedGoogle Scholar
  43. Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among Argonaute proteins. Plant Cell Physiol 49:493–500CrossRefPubMedGoogle Scholar
  44. Tedder P, Zubko E, Westhead DR, Meyer P (2009) Small RNA analysis in Petunia hybrida identifies unusual tissue-specific expression patterns of conserved miRNAs and of a 24mer RNA. RNA 15:1012–1020CrossRefPubMedPubMedCentralGoogle Scholar
  45. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687CrossRefPubMedGoogle Scholar
  46. Wan L, Wang F, Guo X, Lu S, Qiu Z, Zhao Y, Zhang H, Lin J (2012) Identification and characterization of small non-coding RNAs from Chinese fir by high throughput sequencing. BMC Plant Biol 12:146CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wang C, Wang X, Nicholas KK, Song C, Zhang C, Li X, Han J, Fang J (2011) Deep sequencing of grapevine flower and berry short RNA library for discovery of new microRNAs and validation of precise sequences of grapevine microRNAs deposited in miRBase. Physiol Plant 143:64–81CrossRefPubMedGoogle Scholar
  48. Wang C, Han J, Liu C, Kibet KN, Kayesh E, Shangguan L, Li X, Fang J (2012) Identification of microRNAs from Amur grape (Vitis amurensis Rupr.) by deep sequencing and analysis of microRNA variations with bioinformatics. BMC Genom 13(1):122CrossRefGoogle Scholar
  49. Williams L, Carles CC, Osmont KS, Fletcher JC (2005) A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci 102:9703–9708CrossRefPubMedGoogle Scholar
  50. Wu L, Zhang QQ, Zhou HY, Ni FR, Wu XY, Qi YJ (2009) Rice microRNA effector complexes and targets. Plant Cell 21:3421–3435CrossRefPubMedPubMedCentralGoogle Scholar
  51. Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE4 functions intrans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci 102:12984–12989CrossRefPubMedGoogle Scholar
  52. Xu MY, Dong Y, Zhang QX, Zhang L, Luo YZ, Sun J, Fan YL, Wang L (2012) Identification of miRNAs and their targets from Brassica napus by high-throughput sequencing and degradome analysis. BMC Genom 13:421CrossRefGoogle Scholar
  53. Yoshikawa M, Peragine A, Park MY, Poethig S (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164–2175CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492CrossRefPubMedGoogle Scholar
  55. Zhang C, Li G, Wang J, Fang J (2012) Identification of trans-acting siRNAs and their regulatory cascades in grapevine. Bioinformatics 28(20):2561–2568CrossRefPubMedGoogle Scholar
  56. 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):89–101CrossRefPubMedGoogle Scholar
  57. Zhang C, Li G, Zhu S, Zhang S, Fang J (2014) tasiRNAdb: a database of ta-siRNA regulatory pathways. Bioinformatics 30(7):1045–1046CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of HorticultureNanjing Agricultural UniversityNanjingChina

Personalised recommendations