Genome-wide discovery and differential regulation of conserved and novel microRNAs in chickpea via deep sequencing

Journal of Experimental Botany

Volumn 65, Issue 20, 2014, Pages 5945-5958

  Jain, Mukesh ^a   Chevala, V V S Narayana ^a   Garg, Rohini ^a  

^a NATIONAL INSTITUTE OF PLANT GENOME RESEARCH   (India)

Author keywords

Chickpea (Cicer arietinum); deep sequencing; differential expression; microRNA; miRNA targets; tissue specificity

Indexed keywords

CICER ARIETINUM;

MICRORNA; PLANT RNA;

ANTIBODY SPECIFICITY; CHEMISTRY; CICER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; NUCLEOTIDE SEQUENCE; PLANT; PLANT ROOT; SEQUENCE ANALYSIS;

BASE SEQUENCE; CICER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; ORGAN SPECIFICITY; PLANT COMPONENTS, AERIAL; PLANT ROOTS; RNA, PLANT; SEQUENCE ANALYSIS, RNA;

EID: 84913593601     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru333     Document Type: Article

References (82)

1. Adai A, Johnson C, Mlotshwa S, Archer-Evans S, Manocha V, Vance V, Sundaresan V. 2005. Computational prediction of miRNAs in Arabidopsis thaliana. Genome Research 15, 78-91.
2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11, R106.
3. Axtell MJ, Bowman JL. 2008. Evolution of plant microRNAs and their targets. Trends in Plant Science 13, 343-349.
4. Bartel B Bartel DP. 2003 MicroRNAs: at the root of plant developmentfi Plant Physiology 132 709-717.
5. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
6. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
7. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. 1998. AGO1 defines a novel locus of Arabidopsis controlling leaf development. The EMBO Journal 17, 170-180.
8. Bonnet E, Wuyts J, Rouze P, Van de Peer Y. 2004. Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics 20, 2911-2917.
9. Breakfield NW, Corcoran DL, Petricka JJ, Shen J, Sae-Seaw J, Rubio-Somoza I, Weigel D, Ohler U, Benfey PN. 2012. High-resolution experimental and computational profiling of tissue-specific known and nov el miRNAs in Arabidopsis. Genome Research 22, 163-176.
10. Brown JW, Marshall DF, Echeverria M. 2008. Intronic noncoding RNAs and splicing. Trends in Plant Science 13, 335-342.
11. Carri ngton JC, Ambros V. 2003. Role of microRNAs in plant and animal development. Science 301, 336-338.
12. Chen HM, Chen LT, Patel K, Li YH, Baulcombe DC, Wu SH. 2010. 22-Nucleotide RNAs trigger secondary s iRNA biogenesis in plants. Proceedings of the National Academy of Sciences, USA 107, 15269-15274.
13. Chen X. 2004. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022-2025.
14. Chuck G, Candela H, Hake S. 2009. Big impacts by small RNAs in plant development. Current Opinion in Plant Biology 12, 81-86.
15. Chuck G, O?Connor D. 2010. Small RNAs going the distance during plant development. Current Opinion in Plant Biology 13, 40-45.
16. Cui X, Xu SM, Mu DS, Yang ZM. 2009. Genomic analysis of rice microRNA promoters and clusters. Gene 431, 61-66.
17. Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT, Takeda A, Sullivan CM, Gilbert SD, Montgomery TA, Carrington JC. 2010. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural and Molecular Biology 17, 997-1003.
18. Cuperus JT, Fahlgren N, Carrington JC. 2011. Evolution and functional diversification of MIRNA genes. The Plant Cell 23, 431-442.
19. Dai X, Zhao PX. 2011. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research 39, W155-159.
20. De Luis A, Markmann K, Cog nat V, Holt DB, Charpentier M, Parniske M, Stougaard J, Voinnet O. 2012. Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiology 160, 2137-2154.
21. Ebhardt HA, Fedynak A, Fahlman RP. 2010. Naturally occurring variations in sequence length creates microRNA isoforms that differ in argonaute effector complex specificity. Silence 1, 12.
22. Finnegan EJ, Matzke M.A. 2003. The small RNA world. Journal of Cell Science 116, 4689-4693.
23. Garg R, Patel RK, Jhanwar S, Priya P, Bhattacharjee A, Yadav G, Bhatia S, Chattopa dhyay D, Tyagi AK, Jain M. 2011. Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiology 156, 1661-1678.
24. Griff iths-Jones S, Saini HK, van Dongen S, Enright AJ. 2008. miRBase: tools for microRNA genomics. Nucleic Acids Research 36, D154-D158.
25. Ho MS, Ou C, Chan YR, Chien CT, Pi H. 2008. The utility F-box for protein destruction. Cellular and Molecular Life Sciences 65, 1977-2000.
26. Hofacker IL. 2003 Vienna RNA secondary structure server Nucleic Acids Research 31 3429-3431.
27. Hunter C, Poethig RS. 2003. miSSING LINKS: miRNAs and plant development. Current Opinion in Genetics and Development 13, 372-378.
28. Hwang DG, Park JH, Lim JY et al. 2013. The hot pepper Capsicum annuum microRNA transcriptome reveals novel and conserved targets: a foundation for understanding MicroRNA functional roles in hot pepper. PLoS One 8, e64238.
29. Jacobsen SE, Running MP, Meyerowitz EM. 1999. Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126, 5231-5243.
30. Jain M, Misra G, Patel RK et al. 2013. A draft genome sequence of the pulse crop chickpea Cicer arietinum L.. The Plant Journal 74, 715-729.
31. Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ. 2011. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. The Plant Cell 23, 4185-4207.
32. Jones-Rh oades MW, Bartel DP. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell 14, 787-799.
33. Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAS and their regulatory roles in plants. Annual Review of Plant Biology 57, 19-53.
34. Joshi T, Yan Z, Libault M, et al. 2010. Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 11 Suppl. 1, S14.
35. Kidner CA, Martienssen RA. 2005. The developmental role of microRNA in plants. Current Opinion in Plant Biology 8, 38-44.
36. Kim VN. 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews: Molecular Cell Biology 6, 376-385.
37. Kim VN, Nam JW. 2006. Genomics of microRNA. Trends in Genetics 22, 165-173.
38. Kliebenstein DJ, Monde RA, Last RL. 1998. Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiology 118, 637-650 .
39. Kramer MF. 2011. Stem-loop RT-qPCR for miRNAs. Current Protocols in Molecular Biology 15.10.1-15.10.15.
40. Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P. 2006. Fbox proteins everywhere. Current Opinion in Plant Biology 9, 631-638.
41. Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M. 2009. Genome-wide Medicago truncatula small RNA a nalysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell 21, 2780-2796.
42. Li A, Mao L. 2007. Evolution of plant microRNA gene families. Cell Research 17, 212-218.
43. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
44. Li S, Liu L, Zhuang X et al. 2013. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153, 562-574.
45. Llave C, Xie Z, Kasschau KD, Carrington JC. 2002. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056.
46. Lu C, Fedoroff N. 2000. A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. The Plant Cell 12, 2351-2366.
47. Maher C Stein L Ware D. 2006 Evolution of Arabidopsis microRNA families through duplication events Genome Research 16 510-519.
48. Mallory AC, Vaucheret H. 2006. Functions of microRNAs and related small RNAs in plants. Nature Genetics 38 Suppl., S31-S36.
49. Manavella PA, Koenig D, Weigel D. 2012. Plant secondary siRNA production determined by microRNA-duplex structure. Proceedings of the National Academy of Sciences, USA 109, 2461-2466.
50. Mantri N, Basker N, Ford R, Pang E, Pardeshi V. 2013. The role of micro-ribonucleic acids in legumes with a focus on abiotic stress response. Plant Genome 6, 1-14.
51. Meyers BC, Axtell MJ, Bartel B et al. 2008. Criteria for annotation of plant microRNAs. The Plant Cell 20, 3186-3190.
52. Mi S, Cai T, Hu Y et al. 2008. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5? terminal nucleotide. Cell 133, 116-127.
53. Mishra AK, Agarwal S, Jain CK, Rani V. 2009. High GC content: critical parameter for predicting stress regulated miRNAs in Arabidopsis thaliana. Bioinformation 4, 151-154.
54. Nozawa M, Miura S, Nei M. 2012. Origins and evolution of microRNA genes in plant species. Genome Biology and Evolution 4, 230-239.
55. Palatnik JF, Wollmann H, Schom mer C et al. 2007. Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Developmental Cell 13, 115-125.
56. Park W, Li J, Song R, Messing J, Chen X. 2002. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology 12, 1484-1495.
57. Patel RK, Jain M. 2012. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7, e30619.
58. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes and Development 20, 3407-3425.
59. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. 2002. MicroRNAs in plants. Genes and Development 16, 1616-1626.
60. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110, 513-520.
61. Rogers K, Chen X. 2013. Biogenesis, turnover, and mode of action of plant microRNAs. The Plant Cell 25, 2383-2399.
62. Rubio-Somoza I, Weigel D. 2011. MicroRNA networks and developmental plasticity in plants. Trends in Plant Science 16, 258-264.
63. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. 2005. Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8, 517-527.
64. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. 2007. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134, 1051-1060 .
65. Simon SA, Meyers BC, Sherrier DJ. 2009. MicroRNAs in the rhizobia legume symbiosis. Plant Physiology 151, 1002-1008.
66. Singh VK, Garg R, Jain M. 2013. A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnology Journal 11, 691-701.
67. Sunkar R, Girke T. Jain PK, Zhu JK. 2005. Cloning and characterization of microRNAs from rice. The Plant Cell 17, 1397-1411.
68. Telfer A Poethig RS. 1998 HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana Development 125 1889-1898.
69. Thakur V, Wanchana S, Xu M, Bruskiewich R, Quick WP, Mosig A, Zhu XG. 2011. Characterization of statistical features for plant microRNA prediction. BMC Genomics 12, 108.
70. Turner M, Yu O, Subramanian S. 2012. Genome organization and characteristics of soybean microRNAs. BMC Genomics 13, 169.
71. Varshney RK, Song C, Saxena RK et al. 2013. Draft genome sequence of chickpea Cicer arietinum provides a resource for trait improvement. Nature Biotechnology 31, 240-246.
72. Vaucheret H. 2009. AGO1 homeostasis involves differential production of 21-nt and 22-nt miR168 species by MIR168a and MIR168b. PLoS One 4, e6442.
73. Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687.
74. Wang WC, Lin FM, Chang WC, Lin KY, Huang HD, Lin NS. 2009. miRExpress: analyzing high-throughput sequencing data for profiling microRNA expression. BMC Bioinformatics 10, 328.
75. Wu L, Zhou H, Zhang Q, Zhang J, Ni F,Liu C,Qi Y. 2010. DNA methylation mediated by a microRNA pathway. Molecular Cell 38, 465-475.
76. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zi lberman D, Jacobsen SE, Carrington JC. 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biology 2, E104.
77. Yang X, Li L. 2011. miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27, 2614-2615.
78. Yang X, Zhang H, Li L. 2011. Global analysis of gene-level microRNA expression in Arabidopsis using deep sequencing data. Genomics 98, 40-46.
79. Zhai J, Jeong DH, De Paoli E, et al. 2011. MicroRNAs as master regulators of the p lant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes and Devlopment 25, 2540-2553.
80. Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA. 2006. Evidence that miRNAs are different from other RNAs. Cellular and Molecular Life Sciences 63, 246-254.
81. Zhang R, Marshall D, Bryan GJ, Hornyik C. 2013. Identification and characterization of miRNA transcriptome in potato by high-throughput sequencing. PLoS One 8, e57233.
82. Zhu E, Zhao F, Xu G, Hou H, Zhou L, Li X, Sun Z, Wu, J. 2010. mirTools: microRNA profiling and discovery based on high-throughput sequencing. Nucleic A cids Research 38, W392-W397.