Comprehensive analyses of microRNA gene evolution in paleopolyploid soybean genome

Plant Journal

Volumn 76, Issue 2, 2013, Pages 332-344

  Zhou, Zhengkui ^a   Wang, Zheng ^a   Li, Weiyu ^a   Fang, Chao ^a,b   Shen, Yanting ^a,b   Li, Congcong ^a,b   Wu, Yunshuai ^a   Tian, Zhixi ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

evolution; microRNA; MIRNA like hairpin; soybean; structure divergence

Indexed keywords

BIRTH AND DEATH PROCESS; COMPREHENSIVE ANALYSIS; EVOLUTION; GENETIC RECOMBINATIONS; MICRORNAS; MIRNA-LIKE HAIRPIN; SOYBEAN; TRANSPOSABLE ELEMENTS;

GENES;

RNA;

GLYCINE MAX;

MICRORNA; PLANT RNA; SMALL INTERFERING RNA;

ARTICLE; EVOLUTION; GENE DUPLICATION; GENETIC RECOMBINATION; GENETICS; MIRNA-LIKE HAIRPIN; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PLANT GENOME; POLYPLOIDY; SEQUENCE ANALYSIS; SOYBEAN; STRUCTURE DIVERGENCE; TRANSPOSON;

EVOLUTION; MICRORNA; MIRNA-LIKE HAIRPIN; SOYBEAN; STRUCTURE DIVERGENCE;

CONSERVED SEQUENCE; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; MICRORNAS; POLYPLOIDY; RECOMBINATION, GENETIC; RNA, PLANT; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, RNA; SOYBEANS;

EID: 84885292642     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12293     Document Type: Article

References (71)

1. Abrouk, M., Zhang, R., Murat, F., Li, A., Pont, C., Mao, L., and, Salse, J., (2012) Grass microRNA gene paleohistory unveils new insights into gene dosage balance in subgenome partitioning after whole-genome duplication. Plant Cell, 24, 1776-1792.
2. Allen, E., Xie, Z., Gustafson, A.M., Sung, G.H., Spatafora, J.W., and, Carrington, J.C., (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282-1290.
3. Ambros, V., (2004) The functions of animal microRNAs. Nature, 431, 350-355.
4. Ambros, V., and, Chen, X., (2007) The regulation of genes and genomes by small RNAs. Development, 134, 1635-1641.
5. Axtell, M.J., and, Bartel, D.P., (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell, 17, 1658-1673.
6. Axtell, M.J., and, Bowman, J.L., (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci. 13, 343-349.
7. Bartel, D.P., (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
8. Bennetzen, J.L., Ma, J., and, Devos, K.M., (2005) Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95, 127-132.
9. Berezikov, E., (2011) Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet. 12, 846-860.
10. Carrington, J.C., and, Ambros, V., (2003) Role of microRNAs in plant and animal development. Science, 301, 336-338.
11. Chan, C., Qi, X., Li, M.W., Wong, F.L., and, Lam, H.M., (2012) Recent developments of genomic research in soybean. J Gene Genomics, 39, 317-324.
12. Chen, X., (2005) MicroRNA biogenesis and function in plants. FEBS Lett. 579, 5923-5931.
13. Chen, X.M., (2009) Small RNAs and Their Roles in Plant Development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
14. Devos, K.M., Brown, J.K., and, Bennetzen, J.L., (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12, 1075-1079.
15. Du, J., Tian, Z., Bowen, N.J., Schmutz, J., Shoemaker, R.C., and, Ma, J., (2010a) Bifurcation and enhancement of autonomous-nonautonomous retrotransposon partnership through LTR Swapping in soybean. Plant Cell, 22, 48-61.
16. Du, J., Tian, Z., Hans, C.S., Laten, H.M., Cannon, S.B., Jackson, S.A., Shoemaker, R.C., and, Ma, J., (2010b) Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J. 63, 584-598.
17. Emberton, J., Ma, J., Yuan, Y., SanMiguel, P., and, Bennetzen, J.L., (2005) Gene enrichment in maize with hypomethylated partial restriction (HMPR) libraries. Genome Res. 15, 1441-1446.
18. Fahlgren, N., Howell, M.D., Kasschau, K.D., et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE, 2, e219.
19. Fahlgren, N., Jogdeo, S., Kasschau, K.D., et al. (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell, 22, 1074-1089.
20. Felippes, F.F., Schneeberger, K., Dezulian, T., Huson, D.H., and, Weigel, D., (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA, 14, 2455-2459.
21. Friedlander, M.R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., and, Rajewsky, N., (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26, 407-415.
22. Gill, N., Findley, S., Walling, J.G., Hans, C., Ma, J., Doyle, J., Stacey, G., and, Jackson, S.A., (2009) Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol. 151, 1167-1174.
23. Griffiths-Jones, S., (2004) The microRNA Registry. Nucleic Acids Res. 32, D109-D111.
24. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A., and, Enright, A.J., (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140-D144.
25. Griffiths-Jones, S., Saini, H.K., van Dongen, S., and, Enright, A.J., (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res. 36, D154-D158.
26. Hamilton, A., Voinnet, O., Chappell, L., and, Baulcombe, D., (2002) Two classes of short interfering RNA in RNA silencing. EMBO J. 21, 4671-4679.
27. Hofacker, I.L., Fontana, W., Stadler, P.F., Bonhoeffer, L.S., Tacker, M., and, Schuster, P., (1994) Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 125, 167-188.
28. Jiang, D.H., Yin, C.S., Yu, A.P., Zhou, X.F., Liang, W.Q., Yuan, Z., Xu, Y., Yu, Q.B., Wen, T.Q., and, Zhang, D.B., (2006) Duplication and expression analysis of multicopy miRNA gene family members in Arabidopsis and rice. Cell Res. 16, 507-518.
29. Jones-Rhoades, M.W., Bartel, D.P., and, Bartel, B., (2006) MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53.
30. Kasschau, K.D., Fahlgren, N., Chapman, E.J., Sullivan, C.M., Cumbie, J.S., Givan, S.A., and, Carrington, J.C., (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 5, e57.
31. Kozomara, A., and, Griffiths-Jones, S., (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157.
32. Lee, R.C., Feinbaum, R.L., and, Ambros, V., (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843-854.
33. Li, H., and, Durbin, R., (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
34. Li, A.L., and, Mao, L., (2007) Evolution of plant microRNA gene families. Cell Res. 17, 212-218.
35. Lippman, Z., Gendrel, A.V., Black, M., et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature, 430, 471-476.
36. Lisch, D., (2009) Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol. 60, 43-66.
37. Lisch, D., (2013) How important are transposons for plant evolution? Nat. Rev. Genet. 14, 49-61.
38. Lu, C., Tej, S.S., Luo, S., Haudenschild, C.D., Meyers, B.C., and, Green, P.J., (2005) Elucidation of the small RNA component of the transcriptome. Science, 309, 1567-1569.
39. Lu, C., Meyers, B.C., and, Green, P.J., (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods, 43, 110-117.
40. Lu, J., Shen, Y., Wu, Q., Kumar, S., He, B., Shi, S., Carthew, R.W., Wang, S.M., and, Wu, C.I., (2008) The birth and death of microRNA genes in Drosophila. Nat. Genet. 40, 351-355.
41. Ma, J., and, Bennetzen, J.L., (2006) Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc. Natl Acad. Sci. USA 103, 383-388.
42. Ma, Z.R., Coruh, C., and, Axtell, M.J., (2010) Arabidopsis lyrata Small RNAs: transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell, 22, 1090-1103.
43. Maher, C., Stein, L., and, Ware, D., (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res. 16, 510-519.
44. Meunier, J., Lemoine, F., Soumillon, M., Liechti, A., Weier, M., Guschanski, K., Hu, H., Khaitovich, P., and, Kaessmann, H., (2013) Birth and expression evolution of mammalian microRNA genes. Genome Res. 23, 34-45.
45. Millar, A.A., and, Waterhouse, P.M., (2005) Plant and animal microRNAs: similarities and differences. Funct. Integr. Genomics 5, 129-135.
46. Nozawa, M., Miura, S., and, Nei, M., (2010) Origins and evolution of microRNA genes in Drosophila species. Genome Biol. Evol. 2, 180-189.
47. Palmer, L.E., Rabinowicz, P.D., O'Shaughnessy, A.L., Balija, V.S., Nascimento, L.U., Dike, S., de la Bastide, M., Martienssen, R.A., and, McCombie, W.R., (2003) Maize genome sequencing by methylation filtration. Science, 302, 2115-2117.
48. Pasquinelli, A.E., Reinhart, B.J., Slack, F., et al. (2000) Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature, 408, 86-89.
49. Piriyapongsa, J., and, Jordan, I.K., (2007) A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS ONE, 2, e203.
50. Piriyapongsa, J., and, Jordan, I.K., (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA, 14, 814-821.
51. Rajagopalan, R., Vaucheret, H., Trejo, J., and, Bartel, D.P., (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407-3425.
52. Roulin, A., Auer, P.L., Libault, M., Schlueter, J., Farmer, A., May, G., Stacey, G., Doerge, R.W., and, Jackson, S.A., (2013) The fate of duplicated genes in a polyploid plant genome. Plant J. 73, 143-153.
53. Schlueter, J.A., Lin, J.Y., Schlueter, S.D., et al. (2007) Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. BMC Genomics, 8, 330.
54. Schmutz, J., Cannon, S.B., Schlueter, J., et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178-183.
55. Severin, A.J., Woody, J.L., Bolon, Y.T., et al. (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 10, 160.
56. Shoemaker, R.C., Schlueter, J., and, Doyle, J.J., (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr. Opin. Plant Biol. 9, 104-109.
57. Smalheiser, N.R., and, Torvik, V.I., (2005) Mammalian microRNAs derived from genomic repeats. Trends Genet. 21, 322-326.
58. Tang, G., (2010) Plant microRNAs: an insight into their gene structures and evolution. Semin. Cell Dev. Biol. 21, 782-789.
59. Tian, Z., Rizzon, C., Du, J., Zhu, L., Bennetzen, J.L., Jackson, S.A., Gaut, B.S., and, Ma, J., (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res. 19, 2221-2230.
60. Trapnell, C., Pachter, L., and, Salzberg, S.L., (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
61. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and, Pachter, L., (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515.
62. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and, Pachter, L., (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578.
63. Voinnet, O., (2009) Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669-687.
64. Washietl, S., Hofacker, I.L., and, Stadler, P.F., (2005) Fast and reliable prediction of noncoding RNAs. Proc. Natl Acad. Sci. USA 102, 2454-2459.
65. Wicker, T., Sabot, F., Hua-Van, A., et al. (2007) A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982.
66. Wright, S.I., Agrawal, N., and, Bureau, T.E., (2003) Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 13, 1897-1903.
67. Yan, J., Gu, Y., Jia, X., Kang, W., Pan, S., Tang, X., Chen, X., and, Tang, G., (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell, 24, 415-427.
68. Zhang, L., and, Gaut, B.S., (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res. 13, 2533-2540.
69. Zhang, B.H., Pan, X.P., Cobb, G.P., and, Anderson, T.A., (2006) Plant microRNA: a small regulatory molecule with big impact. Dev. Biol. 289, 3-16.
70. Zhang, B., Wang, Q., and, Pan, X., (2007) MicroRNAs and their regulatory roles in animals and plants. J. Cell. Physiol. 210, 279-289.
71. Zhao, Y.T., Wang, M., Fu, S.X., Yang, W.C., Qi, C.K., and, Wang, X.J., (2012) Small RNA profiling in two Brassica napus cultivars identifies microRNAs with oil production- and development-correlated expression and new small RNA classes. Plant Physiol. 158, 813-823.