Genome-wide identification and evolutionary analysis of positively selected miRNA genes in domesticated rice

Molecular Genetics and Genomics

Volumn 290, Issue 2, 2015, Pages 593-602

  Liu, Qingpo ^a   Wang, Hong ^a   Hu, Haichao ^a   Zhang, Hengmu ^b  

^a ZHEJIANG A F UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

Author keywords

Domestication; Evolution; miRNA; Positive selection; Rice

Indexed keywords

MESSENGER RNA; MICRORNA; PLANT RNA; TRANSCRIPTOME;

ARTICLE; CONTROLLED STUDY; DOMESTICATED PLANT; GENE LOCUS; GENE SEQUENCE; GENETIC IDENTIFICATION; GENETIC VARIABILITY; GENOTYPE; MUTATION RATE; NONHUMAN; PLANT GENE; POPULATION GENETICS; PRIORITY JOURNAL; RICE; GENETIC SELECTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENOME;

BASE SEQUENCE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENOME, PLANT; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; ORYZA SATIVA; RNA, PLANT; SELECTION, GENETIC; TRANSCRIPTOME;

EID: 84925538119     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-014-0943-0     Document Type: Article

References (67)

1. Allaby RG, Fuller DQ, Brown TA (2008) The genetic expectations of a protracted model for the origins of domesticated crops. Proc Natl Acad Sci USA 105:13982–13986
2. Asano K, Yamasaki M, Takuno S, Miura K, Katagiri S, Ito T, Doi K, Wu J, Ebana K, Matsumoto T, Innan H, Kitano H, Ashikari M, Matsuoka M (2011) Artificial selection for a green revolution gene during japonica rice domestication. Proc Natl Acad Sci USA 108:11034–11039
3. Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Fledel-Alon A, York TL, Polato NR, Olsen KM, Nielsen R, McCouch SR, Bustamante CD, Purugganan MD (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3:e163
4. Chen XM (2005) MicroRNA biogenesis and functions in plants. FEBS Lett 579:5923–5931
5. Chen Z, Li F, Yang S, Dong Y, Yuan Q, Wang F, Li W, Jiang Y, Jia S, Pei X (2013) Identification and functional analysis of flowering related microRNAs in common wild rice (Oryza rufipogon Griff.). PLoS ONE 8:e82844
6. Cui X, Wang Q, Yin W, Xu H, Wilson ZA, Wei C, Pan S, Zhang D (2012) PMRD: a curated database for genes and mutants involved in plant male reproduction. BMC Plant Biol 12:215
7. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442
8. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159
9. de Meaux J, Hu JY, Tartler U, Goebel U (2008) Structurally different alleles of the ath-MIR824 microRNA precursor are maintained at high frequency in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:8994–8999
10. Droc G, Périn C, Fromentin S, Larmande P (2009) OryGenesDB 2008 update: database interoperability for functional genomics of rice. Nucleic Acids Res 37:D992–D995
11. Ehrenreich IM, Purugganan MD (2008) Sequence variation of microRNAs and their binding sites in Arabidopsis. Plant Physiol 146:1974–1982
12. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413
13. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
14. Gielen H, Remans T, Vangronsveld J, Cuypers A (2012) MicroRNAs in metal stress: specific roles or secondary responses? Int J Mol Sci 13:15826–15847
15. Gong J, Tong Y, Zhang HM, Wang K, Hu T, Shan G, Sun J, Guo AY (2012) Genome-wide identification of SNPs in microRNA genes and the SNP effects on microRNA target binding and biogenesis. Hum Mutat 33:254–263
16. Guo X, Gui Y, Wang Y, Zhu QH, Helliwell C, Fan L (2008) Selection and mutation on microRNA target sequences during rice evolution. BMC Genom 9:454
17. Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z, Min J, Guo X, Murat F, Ham BK, Zhang Z, Gao S, Huang M, Xu Y, Zhong S, Bombarely A, Mueller LA, Zhao H, He H, Zhang Y, Zhang Z, Huang S, Tan T, Pang E, Lin K, Hu Q, Kuang H, Ni P, Wang B, Liu J, Kou Q, Hou W, Zou X, Jiang J, Gong G, Klee K, Schoof H, Huang Y, Hu X, Dong S, Liang D, Wang J, Wu K, Xia Y, Zhao X, Zheng Z, Xing M, Liang X, Huang B, Lv T, Wang J, Yin Y, Yi H, Li R, Wu M, Levi A, Zhang X, Giovannoni JJ, Wang J, Li Y, Fei Z, Xu Y (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58
18. Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614
19. He Z, Zhai W, Wen H, Tang T, Wang Y, Lu X, Greenberg AJ, Hudson RR, Wu CI, Shi S (2011) Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet 7:e1002100
20. Henry RJ (2012) Next-generation sequencing for understanding and accelerating crop domestication. Brief Funct Genomics 11:51–56
21. Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967
22. Huang X, Kurata N, Wei X, Wang Z, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X, Xu Q, Dong G, Zhan Q, Li C, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J, Han B (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501
23. Huerta-Cepas J, Capella-Gutierrez S, Pryszcz LP, Denisov I, Kormes D, Marcet-Houben M, Gabaldón T (2011) PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucleic Acids Res 39:D556–D560
24. Hufford MB, Xu X, van Heerwaarden J, Pyhäjärvi T, Chia JM, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, Lai J, Morrell PL, Shannon LM, Song C, Springer NM, Swanson-Wagner RA, Tiffin P, Wang J, Zhang G, Doebley J, McMullen MD, Ware D, Buckler ES, Yang S, Ross-Ibarra J (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811
25. Izawa T, Konishi S, Shomura A, Yano M (2009) DNA changes tell us about rice domestication. Curr Opin Plant Biol 12:185–192
26. Jia G, Huang X, Zhi H, Zhao Y, Zhao Q, Li W, Chai Y, Yang L, Liu K, Lu H, Zhu C, Lu Y, Zhou C, Fan D, Weng Q, Guo Y, Huang T, Zhang L, Lu T, Feng Q, Hao H, Liu H, Lu P, Zhang N, Li Y, Guo E, Wang S, Wang S, Liu J, Zhang W, Chen G, Zhang B, Li W, Wang Y, Li H, Zhao B, Li J, Diao X, Han B (2013) A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat Genet 45:957–961
27. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544
28. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
29. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34
30. Kovach MJ, Sweeney MT, McCouch SR (2007) New insights into the history of rice domestication. Trends Genet 23:578–587
31. Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73
32. Li C (2008) Automating dChip: toward reproducible sharing of microarray data analysis. BMC Bioinformatics 9:231
33. Li M, Xu W, Yang W, Kong Z, Xue Y (2007) Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice. Plant Physiol 144:1797–1812
34. Li Y, Zhou G, Ma J, Jiang W, Jin L, Zhang Z, Guo Y, Zhang J, Sui Y, Zheng L, Zhang S, Zuo Q, Shi X, Li Y, Zhang W, Hu Y, Kong G, Hong H, Tan B, Song J, Liu Z, Wang Y, Ruan H, Yeung CKL, Liu J, Wang H, Zhang L, Guan R, Wang K, Li W, Chen S, Chang R, Jiang Z, Jackson SA, Li R, Qiu L (2014) De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol. doi:10.1038/nbt.2979
35. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
36. Liu Q, Wang H, Zhu L, Hu H, Sun Y (2013) Genome-wide identification and analysis of miRNA-related single nucleotide polymorphisms (SNPs) in rice. Rice 6:10
37. Lu HY, Liu ZX, Wu NQ, Berné S, Saito Y, Liu B, Wang L (2002) Rice domestication and climatic change: phytolith evidence from East China. Boreas 31:378–385
38. Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun YH, Yuan L, Yeh TF, Peszlen I, Ralph J, Sederoff RR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110:10848–10853
39. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
40. Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239
41. Pashkovskiy PP, Ryazansky SS (2013) Biogenesis, evolution, and functions of plant microRNAs. Biochemistry 78:627–637
42. Pryszcz LP, Huerta-Cepas J, Gabaldón T (2011) MetaPhOrs: orthology and paralogy predictions from multiple phylogenetics evidence using a consistency-based confidence score. Nucleic Acids Res 39:e32
43. Qi J, Liu X, Shen D, Miao H, Xie B, Li X, Zeng P, Wang S, Shang Y, Gu X, Du Y, Li Y, Lin T, Yuan J, Yang X, Chen J, Chen H, Xiong X, Huang K, Fei Z, Mao L, Tian L, Städler T, Renner SS, Kamoun S, Lucas WJ, Zhang Z, Huang S (2013) A genome variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45:1510–1515
44. Quach H, Barreiro LB, Laval G, Zidane N, Patin E, Kidd KK, Kidd JR, Bouchier C, Veuille M, Antoniewski C, Quintana-Murci L (2009) Signatures of purifying and local positive selection in human miRNAs. Am J Hum Genet 84:316–327
45. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionary fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425
46. Sang T, Ge S (2013) Understanding rice domestication and implications for cultivar improvement. Curr Opin Plant Biol 16:139–146
47. Sun J, Zhou M, Mao Z, Li C (2012) Characterization and evolution of microRNA genes derived from repetitive elements and duplication events in plants. PLoS ONE 7:e34092
48. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
49. Todesco M, Balasubramanian S, Cao J, Ott F, Sureshkumar S, Schneeberger K, Meyer RC, Altmann T, Weigel D (2012) Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol 22:166–170
50. Wang S, Zhu QH, Guo X, Gui Y, Bao J, Helliwell C, Fan L (2007) Molecular evolution and selection of a gene encoding two tandem microRNAs in rice. FEBS Lett 581:4789–4793
51. Wang Y, Shen D, Bo S, Chen H, Zheng J, Zhu QH, Cai D, Helliwell C, Fan L (2010) Sequence variation and selection of small RNAs in domesticated rice. BMC Evol Biol 10:119
52. Wang Y, Bai X, Yan C, Gui Y, Wei X, Zhu QH, Guo L, Fan L (2012) Genomic dissection of small RNAs in wild rice (Oryza rufipogon): lessons for rice domestication. New Phytol 196:914–925
53. Watterson GA (1975) On the number of segregating sites in genetical models without recombinations. Theor Popul Biol 7:256–276
54. Wei FJ, Droc G, Guiderdoni E, Hsing YC (2013) International consortium of rice mutagenesis: resources and beyond. Rice 6:39
55. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111
56. Yamasaki M, Tenaillon MI, Bi IV, Schroeder SG, Sanchez-Villeda H, Doebley JF, Gaut BS, McMullen MD (2005) A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17:2859–2872
57. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
58. Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43
59. Yang C, Kawahara Y, Mizuno H, Wu J, Matsumoto T, Itoh T (2012) Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol Biol Evol 29:1471–1479
60. Yonemaru J, Yamamoto T, Ebana K, Yamamoto E, Nagasaki H, Shibaya T, Yano M (2012) Genome-wide haplotype changes produced by artificial selection during modern rice breeding in Japan. PLoS ONE 7:e32982
61. Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5:e1000716
62. Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, Liao JY, Wang XJ, Qu LH, Chen F, Xin P, Yan C, Chu J, Li HQ, Chen YQ (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–852
63. Zhao ZJ (1998) The middle Yangtze region in China is one place where rice was domesticated: phytolith evidence from the Diaotonghuan cave, northern Jiangxi. Antiquity 72:885–897
64. Zhu Q, Zheng X, Luo J, Gaut BS, Ge S (2007) Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Mol Biol Evol 24:875–888
65. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 18:1456–1465
66. Zhu Z, Tan L, Fu Y, Liu F, Cai H, Xie D, Wu F, Wu J, Matsumoto T, Sun C (2013) Genetic control of inflorescence architecture during rice domestication. Nat Commun 4:2200
67. Zhuo Y, Gao G, Shi J, Zhou X, Wang X (2013) miRNAs: biogenesis, origin and evolution, functions on virus-host interaction. Cell Physiol Biochem 32:499–510