Small RNA sequencing identifies miRNA roles in ovule and fibre development

Plant Biotechnology Journal

Volumn 13, Issue 3, 2015, Pages 355-369

  Xie, Fuliang ^a   Jones, Don C ^b   Wang, Qinglian ^c   Sun, Runrun ^a,c   Zhang, Baohong ^a,c  

^a EAST CAROLINA UNIVERSITY   (United States)

^b Agricultural and Environmental Research Division   (United States)

^c HENAN INSTITUTE OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Cotton; Gene regulation; MiRNA; Ovule and fibre development; Transcription factor

Indexed keywords

GOSSYPIUM HIRSUTUM;

MICRORNA; PLANT RNA; SMALL INTERFERING RNA;

COTTON; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; GOSSYPIUM; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OVULE; PLANT LEAF; SEQUENCE ANALYSIS;

BASE SEQUENCE; COTTON FIBER; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GOSSYPIUM; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MOLECULAR SEQUENCE DATA; OVULE; PLANT LEAVES; RNA, PLANT; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA;

EID: 84926419766     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12296     Document Type: Article

References (63)

1. Adams, K.L., Cronn, R., Percifield, R. and Wendel, J.F. (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl Acad. Sci. USA, 100, 4649-4654.
2. Allen, E. and Howell, M.D. (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin. Cell Dev. Biol. 21, 798-804.
3. Bartel, D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
4. Burklew, C.E., Xie, F.L., Ashlock, J. and Zhang, B.H. (2014) Expression of microRNAs and their targets regulates floral development in tobacco (Nicotiana tabacum). Funct. Integr. Genomics, 14, 299-306.
5. Chen, Z.J., Scheffler, B.E., Dennis, E., Triplett, B.A., Zhang, T., Guo, W., Chen, X., Stelly, D.M., Rabinowicz, P.D., Town, C.D., Arioli, T., Brubaker, C., Cantrell, R.G., Lacape, J.M., Ulloa, M., Chee, P., Gingle, A.R., Haigler, C.H., Percy, R., Saha, S., Wilkins, T., Wright, R.J., Van Deynze, A., Zhu, Y., Yu, S., Abdurakhmonov, I., Katageri, I., Kumar, P.A., Mehboob Ur, R., Zafar, Y., Yu, J.Z., Kohel, R.J., Wendel, J.F. and Paterson, A.H. (2007) Toward sequencing cotton (Gossypium) genomes. Plant Physiol. 145, 1303-1310.
6. Dai, X. and Zhao, P.X. (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res. 39(Web Server Issue), W155-W159.
7. Eden, E., Navon, R., Steinfeld, I., Lipson, D. and Yakhini, Z. (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics, 10, 48.
8. Eldem, V., Okay, S. and Unver, T. (2013) Plant microRNAs: new players in functional genomics. Turk. J. Agric. For. 37, 1-21.
9. Fei, Q., Xia, R. and Meyers, B.C. (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell, 25, 2400-2415.
10. Gardner, P.P., Daub, J., Tate, J., Moore, B.L., Osuch, I.H., Griffiths-Jones, S., Finn, R.D., Nawrocki, E.P., Kolbe, D.L., Eddy, S.R. and Bateman, A. (2011) Rfam: Wikipedia, clans and the "decimal" release. Nucleic Acids Res. 39(Database Issue), D141-D145.
11. German, M.A., Pillay, M., Jeong, D.H., Hetawal, A., Luo, S., Janardhanan, P., Kannan, V., Rymarquis, L.A., Nobuta, K., German, R., De Paoli, E., Lu, C., Schroth, G., Meyers, B.C. and Green, P.J. (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26, 941-946.
12. Gong, L., Kakrana, A., Arikit, S., Meyers, B.C. and Wendel, J.F. (2013) Composition and expression of conserved microRNA genes in diploid cotton (Gossypium) species. Genome Biol. Evol. 5, 2449-2459.
13. Guan, X., Pang, M., Nah, G., Shi, X., Ye, W., Stelly, D.M. and Chen, Z.J. (2014) miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050.
14. Hinz, M., Wilson, I.W., Yang, J., Buerstenbinder, K., Llewellyn, D., Dennis, E.S., Sauter, M. and Dolferus, R. (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol. 153, 757-772.
15. Kozomara, A. and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39(Database Issue), D152-D157.
16. Kwak, P.B., Wang, Q.Q., Chen, X.S., Qiu, C.X. and Yang, Z.M. (2009) Enrichment of a set of microRNAs during the cotton fiber development. BMC Genomics, 10, 457.
17. Larkin, J.C., Brown, M.L. and Schiefelbein, J. (2003) How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu. Rev. Plant Biol. 54, 403-430.
18. Latchman, D.S. (1997) Transcription factors: an overview. Int. J. Biochem. Cell Biol. 29, 1305-1312.
19. Lee, J.J., Woodward, A.W. and Chen, Z.J. (2007) Gene expression changes and early events in cotton fibre development. Ann. Bot. 100, 1391-1401.
20. Lelandais-Briere, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., Gouzy, J. and Crespi, M. (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell, 21, 2780-2796.
21. Li, F., Orban, R. and Baker, B. (2012) SoMART: a web server for plant miRNA, tasiRNA and target gene analysis. Plant J. 70, 891-901.
22. Lu, S., Li, Q., Wei, H., Chang, M.J., Tunlaya-Anukit, S., Kim, H., Liu, J., Song, J., Sun, Y.H., Yuan, L., Yeh, T.F., Peszlen, I., Ralph, J., Sederoff, R.R. and Chiang, V.L. (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc. Natl Acad. Sci. USA, 110, 10848-10853.
23. Machado, A., Wu, Y., Yang, Y., Llewellyn, D.J. and Dennis, E.S. (2009) The MYB transcription factor GhMYB25 regulates early fibre and trichome development. Plant J. 59, 52-62.
24. Marsit, C.J., Eddy, K. and Kelsey, K.T. (2006) MicroRNA responses to cellular stress. Cancer Res. 66, 10843-10848.
25. Meyers, B.C., Axtell, M.J., Bartel, B., Bartel, D.P., Baulcombe, D., Bowman, J.L., Cao, X., Carrington, J.C., Chen, X., Green, P.J., Griffiths-Jones, S., Jacobsen, S.E., Mallory, A.C., Martienssen, R.A., Poethig, R.S., Qi, Y., Vaucheret, H., Voinnet, O., Watanabe, Y., Weigel, D. and Zhu, J.K. (2008) Criteria for annotation of plant MicroRNAs. Plant Cell, 20, 3186-3190.
26. Mi, H., Muruganujan, A., Casagrande, J.T. and Thomas, P.D. (2013) Large-scale gene function analysis with the PANTHER classification system. Nat. Protoc. 8, 1551-1566.
27. Murakami, Y., Yasuda, T., Saigo, K., Urashima, T., Toyoda, H., Okanoue, T. and Shimotohno, K. (2006) Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene, 25, 2537-2545.
28. Nag, A., King, S. and Jack, T. (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 22534-22539.
29. Palatnik, J.F., Wollmann, H., Schommer, C., Schwab, R., Boisbouvier, J., Rodriguez, R., Warthmann, N., Allen, E., Dezulian, T., Huson, D., Carrington, J.C. and Weigel, D. (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev. Cell, 13, 115-125.
30. Pang, M., Woodward, A.W., Agarwal, V., Guan, X., Ha, M., Ramachandran, V., Chen, X., Triplett, B.A., Stelly, D.M. and Chen, Z.J. (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, R122.
31. Pang, C.Y., Wang, H., Pang, Y., Xu, C., Jiao, Y., Qin, Y.M., Western, T.L., Yu, S.X. and Zhu, Y.X. (2010) Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol. Cell Proteomics, 9, 2019-2033.
32. Paterson, A.H., Wendel, J.F., Gundlach, H., Guo, H., Jenkins, J., Jin, D., Llewellyn, D., Showmaker, K.C., Shu, S., Udall, J., Yoo, M.J., Byers, R., Chen, W., Doron-Faigenboim, A., Duke, M.V., Gong, L., Grimwood, J., Grover, C., Grupp, K., Hu, G., Lee, T.H., Li, J., Lin, L., Liu, T., Marler, B.S., Page, J.T., Roberts, A.W., Romanel, E., Sanders, W.S., Szadkowski, E., Tan, X., Tang, H., Xu, C., Wang, J., Wang, Z., Zhang, D., Zhang, L., Ashrafi, H., Bedon, F., Bowers, J.E., Brubaker, C.L., Chee, P.W., Das, S., Gingle, A.R., Haigler, C.H., Harker, D., Hoffmann, L.V., Hovav, R., Jones, D.C., Lemke, C., Mansoor, S., Ur Rahman, M., Rainville, L.N., Rambani, A., Reddy, U.K., Rong, J.K., Saranga, Y., Scheffler, B.E., Scheffler, J.A., Stelly, D.M., Triplett, B.A., Van Deynze, A., Vaslin, M.F., Waghmare, V.N., Walford, S.A., Wright, R.J., Zaki, E.A., Zhang, T., Dennis, E.S., Mayer, K.F., Peterson, D.G., Rokhsar, D.S., Wang, X. and Schmutz, J. (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature, 492, 423-427.
33. Pesch, M. and Hulskamp, M. (2009) One, two, three... models for trichome patterning in Arabidopsis? Curr. Opin. Plant Biol. 12, 587-592.
34. Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N. and Clark, S.E. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell, 17, 61-76.
35. Pu, L., Li, Q., Fan, X., Yang, W. and Xue, Y. (2008) The R2R3 MYB transcription factor GhMYB109 is required for cotton fiber development. Genetics, 180, 811-820.
36. Qin, Y.M. and Zhu, Y.X. (2011) How cotton fibers elongate: a tale of linear cell-growth mode. Curr. Opin. Plant Biol. 14, 106-111.
37. Qin, Y.M., Hu, C.Y., Pang, Y., Kastaniotis, A.J., Hiltunen, J.K. and Zhu, Y.X. (2007) Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell, 19, 3692-3704.
38. Qiu, C., Zuo, K., Qin, J., Zhao, J., Ling, H. and Tang, K. (2006) Isolation and characterization of a class III homeodomain-leucine zipper-like gene from Gossypium barbadense. DNA Seq. 17, 334-341.
39. Qiu, C.X., Xie, F.L., Zhu, Y.Y., Guo, K., Huang, S.Q., Nie, L. and Yang, Z.M. (2007) Computational identification of microRNAs and their targets in Gossypium hirsutum expressed sequence tags. Gene, 395, 49-61.
40. Quintero, A., Perez-Quintero, A.L. and Lopez, C. (2013) Identification of ta-siRNAs and cis-nat-siRNAs in cassava and their roles in response to cassava bacterial blight. Genomics Proteomics Bioinformatics, 11, 172-181.
41. Sunkar, R., Zhou, X., Zheng, Y., Zhang, W. and Zhu, J.K. (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol. 8, 25.
42. Suo, J., Liang, X., Pu, L., Zhang, Y. and Xue, Y. (2003) Identification of GhMYB109 encoding a R2R3 MYB transcription factor that expressed specifically in fiber initials and elongating fibers of cotton (Gossypium hirsutum L.). Biochim. Biophys. Acta, 1630, 25-34.
43. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.L., Bartel, D.P. and Crete, P. (2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell, 16, 69-79.
44. Wang, S., Wang, J.W., Yu, N., Li, C.H., Luo, B., Gou, J.Y., Wang, L.J. and Chen, X.Y. (2004) Control of plant trichome development by a cotton fiber MYB gene. Plant Cell, 16, 2323-2334.
45. Wang, K., Wang, Z., Li, F., Ye, W., Wang, J., Song, G., Yue, Z., Cong, L., Shang, H., Zhu, S., Zou, C., Li, Q., Yuan, Y., Lu, C., Wei, H., Gou, C., Zheng, Z., Yin, Y., Zhang, X., Liu, K., Wang, B., Song, C., Shi, N., Kohel, R.J., Percy, R.G., Yu, J.Z., Zhu, Y.X. and Yu, S. (2012a) The draft genome of a diploid cotton Gossypium raimondii. Nat. Genet. 44, 1098-1103.
46. Wang, Z.M., Xue, W., Dong, C.J., Jin, L.G., Bian, S.M., Wang, C., Wu, X.Y. and Liu, J.Y. (2012b) A comparative miRNAome analysis reveals seven fiber initiation-related and 36 novel miRNAs in developing cotton ovules. Mol. Plant, 5, 889-900.
47. Wang, M., Wang, Q.L. and Zhang, B.H. (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene, 530, 26-32.
48. Wendel, J.F. (1989) New World tetraploid cottons contain Old World cytoplasm. Proc. Natl Acad. Sci. USA, 86, 4132-4136.
49. Williams, L., Carles, C.C., Osmont, K.S. and Fletcher, J.C. (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. USA, 102, 9703-9708.
50. Xie, F., Frazier, T.P. and Zhang, B. (2010) Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). Planta, 232, 417-434.
51. Xie, F., Sun, G., Stiller, J.W. and Zhang, B. (2011) Genome-wide functional analysis of the cotton transcriptome by creating an integrated EST database. PLoS ONE, 6, e26980.
52. Xie, F., Xiao, P., Chen, D., Xu, L. and Zhang, B. (2012a) miRDeepFinder: a miRNA analysis tool for deep sequencing of plant small RNAs. Plant Mol. Biol. 80, 75-84. doi: 10.1007/s11103-012-9885-2.
53. Xie, K., Shen, J., Hou, X., Yao, J., Li, X., Xiao, J. and Xiong, L. (2012b) Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol. 158, 1382-1394.
54. Xie, F.L., Stewart, C.N., Taki, F.A., He, Q.L., Liu, H.W. and Zhang, B.H. (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol. J. 12, 354-366.
55. Xie, F.L., Wang, Q.L. and Zhang, B.H. (2015) Global microRNA modification in cotton (Gossypium hirsutum L).. Plant Biotechnol. J. 13 (in press). doi: 10.1111/pbi.12271.
56. Xing, S., Salinas, M., Hohmann, S., Berndtgen, R. and Huijser, P. (2010) miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell, 22, 3935-3950.
57. Xue, W., Wang, Z., Du, M., Liu, Y. and Liu, J.Y. (2013) Genome-wide analysis of small RNAs reveals eight fiber elongation-related and 257 novel microRNAs in elongating cotton fiber cells. BMC Genomics, 14, 629.
58. Yoshikawa, M., Peragine, A., Park, M.Y. and Poethig, R.S. (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19, 2164-2175.
59. Zhang, B. and Wang, Q. (2015) MicroRNA-based biotechnology for plant improvement. J. Cell. Physiol. 230, 1-15. doi: 10.1002/jcp.24685.
60. Zhang, Z. and Zhang, X. (2012) Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr. Opin. Plant Biol. 15, 652-658.
61. Zhang, F., Liu, X., Zuo, K., Sun, X. and Tang, K. (2011) Molecular cloning and expression analysis of a novel SANT/MYB gene from Gossypium barbadense. Mol. Biol. Rep. 38, 2329-2336.
62. Zhang, H., Wan, Q., Ye, W., Lv, Y., Wu, H. and Zhang, T. (2013) Genome-wide analysis of small RNA and novel microRNA discovery during fiber and seed initial development in Gossypium hirsutum L. PLoS ONE, 8, e69743.
63. Zhang, C., Li, G., Zhu, S., Zhang, S. and Fang, J. (2014) tasiRNAdb: a database of ta-siRNA regulatory pathways. Bioinformatics, 30, 1045-1046. doi: 10.1093/bioinformatics/btt746.