Differentially expressed microRNA cohorts in seed development may contribute to poor grain filling of inferior spikelets in rice

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Peng, Ting ^a   Sun, Hongzheng ^a   Qiao, Mengmeng ^b   Zhao, Yafan ^a   Du, Yanxiu ^a   Zhang, Jing ^a   Li, Junzhou ^a   Tang, Guiliang ^a,b   Zhao, Quanzhi ^a  

^a HENAN AGRICULTURAL UNIVERSITY   (China)

^b MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

Author keywords

Differential expression; Grain filling; Inferior spikelets; microRNA; miRNA dynamics; Rice (Oryza sativa); Superior spikelets

Indexed keywords

ORYZA SATIVA;

MICRORNA;

GENE EXPRESSION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; PHENOTYPE; PLANT SEED; SEQUENCE ANALYSIS;

GENE EXPRESSION; MICRORNAS; ORYZA; PHENOTYPE; SEEDS; SEQUENCE ANALYSIS, RNA;

EID: 84904522512     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0196-4     Document Type: Article

References (62)

1. Fitzgerald MA, McCouch SR, Hall RD. Not just a grain of rice: the quest for quality. Trends Plant Sci 2009, 14(3):133-139. 10.1016/j.tplants.2008.12.004, 19230745.
2. Sakamoto T, Matsuoka M. Identifying and exploiting grain yield genes in rice. Curr Opin Plant Biol 2008, 11(2):209-214. 10.1016/j.pbi.2008.01.009, 18343712.
3. Yang J, Zhang J. Grain-filling problem in 'super' rice. J Exp Bot 2010, 61(1):1-5. 10.1093/jxb/erp348, 19959608.
4. Peng T, Lv Q, Zhang J, Li J, Du Y, Zhao Q. Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). J Exp Bot 2011, 62(14):4943-4954. 10.1093/jxb/err205, 21791435.
5. Zhang H, Li H, Yuan L, Wang Z, Yang J, Zhang J. Post-anthesis alternate wetting and moderate soil drying enhances activities of key enzymes in sucrose-to-starch conversion in inferior spikelets of rice. J Exp Bot 2012, 63(1):215-227. 10.1093/jxb/err263, 21926094.
6. Tsutomu T. Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling. Funct Plant Biol 2003, 30:1139-1149. 10.1071/FP03122.
7. Mohapatra P, Patel R, Sahu S. Time of flowering affects grain quality and spikelet partitioning within the rice panicle. Funct Plant Biol 1993, 20(2):231-241.
8. Khan GA, Declerck M, Sorin C, Hartmann C, Crespi M, Lelandais-Briere C. MicroRNAs as regulators of root development and architecture. Plant Mol Biol 2011, 77(1-2):47-58. 10.1007/s11103-011-9793-x, 21607657.
9. Kidner CA. The many roles of small RNAs in leaf development. J Genet Genomics 2010, 37(1):13-21. 10.1016/S1673-8527(09)60021-7, 20171574.
10. Khraiwesh B, Zhu JK, Zhu J. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 2012, 1819(2):137-148. 10.1016/j.bbagrm.2011.05.001, 21605713.
11. Sunkar R, Li YF, Jagadeeswaran G. Functions of microRNAs in plant stress responses. Trends Plant Sci 2012, 17(4):196-203. 10.1016/j.tplants.2012.01.010, 22365280.
12. Wang JW, Czech B, Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 2009, 138(4):738-749. 10.1016/j.cell.2009.06.014, 19703399.
13. Zhou CM, Zhang TQ, Wang X, Yu S, Lian H, Tang H, Feng ZY, Zozomova-Lihova J, Wang JW. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 2013, 340(6136):1097-1100. 10.1126/science.1234340, 23723237.
14. Liu Q, Chen Y-Q. Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochem Biophys Res Commun 2009, 384:1-5. 10.1016/j.bbrc.2009.04.028, 19366618.
15. Sanan-Mishra N, Varanasi SP, Mukherjee SK. Micro-regulators of auxin action. Plant Cell Rep 2013, 32(6):733-740. 10.1007/s00299-013-1425-2, 23543387.
16. Peng T, Sun H, Du Y, Zhang J, Li J, Liu Y, Zhao Y, Zhao Q. Characterization and expression patterns of microRNAs involved in rice grain filling. PLoS One 2013, 8(1):e54148. 10.1371/journal.pone.0054148, 23365650.
17. 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. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 2013, 31(9):848-852. 10.1038/nbt.2646, 23873084.
18. Lan Y, Su N, Shen Y, Zhang R, Wu F, Cheng Z, Wang J, Zhang X, Guo X, Lei C. Identification of novel MiRNAs and MiRNA expression profiling during grain development in indica rice. BMC Genomics 2012, 13(1):264. 10.1186/1471-2164-13-264, 22721355.
19. Yi R, Zhu Z, Hu J, Qian Q, Dai J, Ding Y. Identification and expression analysis of microRNAs at the grain filling stage in rice (Oryza sativa L.) via deep sequencing. PLoS One 2013, 8(3):e57863. 10.1371/journal.pone.0057863, 23469249.
20. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genom Res 2008, 18(9):1456-1465. 10.1101/gr.075572.107.
21. Xue LJ, Zhang JJ, Xue HW. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 2009, 37(3):916-930. 10.1093/nar/gkn998, 19103661.
22. Liu H, Jia S, Shen D, Liu J, Li J, Zhao H, Han S, Wang Y. Four AUXIN RESPONSE FACTORs down-regulated by microRNA167 are associated with growth and development in Oryza sativa. Funct Plant Biol 2012, 39(9):736-744. 10.1071/FP12106.
23. Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 2010, 42(6):541-544. 10.1038/ng.591, 20495565.
24. Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 2010, 42(6):545-549. 10.1038/ng.592, 20495564.
25. Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X, Zhang G, Fu X. Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 2012, 44(8):950-954. 10.1038/ng.2327, 22729225.
26. Bian H, Xie Y, Guo F, Han N, Ma S, Zeng Z, Wang J, Yang Y, Zhu M. Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol 2012, 196(1):149-161. 10.1111/j.1469-8137.2012.04248.x, 22846038.
27. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics (Oxford, England) 2008, 24(5):713-714. 10.1093/bioinformatics/btn025.
28. Wei LQ, Yan LF, Wang T. Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 2011, 12(6):R53. 10.1186/gb-2011-12-6-r53, 21679406.
29. Chen X. Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 2009, 25:21-44. 10.1146/annurev.cellbio.042308.113417, 19575669.
30. Wu L, Zhang Q, Zhou H, Ni F, Wu X, Qi Y. Rice MicroRNA effector complexes and targets. Plant Cell 2009, 21(11):3421-3435. 10.1105/tpc.109.070938, 19903869.
31. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. Transcriptome-wide identification of microRNA targets in rice. Plant J 2010, 62(5):742-759. 10.1111/j.1365-313X.2010.04187.x, 20202174.
32. Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X. Degradome sequencing reveals endogenous small RNA targets in rice (oryza sativa L. ssp. indica). Front Biol 2010, 5(1):67-90. 10.1007/s11515-010-0007-8.
33. Zheng Y, Li YF, Sunkar R, Zhang W. SeqTar: an effective method for identifying microRNA guided cleavage sites from degradome of polyadenylated transcripts in plants. Nucleic Acids Res 2012, 40(4):e28. 10.1093/nar/gkr1092, 22140118.
34. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38:64-70. 10.1093/nar/gkq310.
35. Guo H-S, Xie Q, Fei J-F, Chua N-H. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell Online 2005, 17(5):1376-1386. 10.1105/tpc.105.030841.
36. Yang JH, Han SJ, Yoon EK, Lee WS. Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 2006, 34(6):1892. 10.1093/nar/gkl118, 16598073.
37. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK. Criteria for annotation of plant MicroRNAs. Plant Cell 2008, 20(12):3186-3190. 10.1105/tpc.108.064311, 19074682.
38. Dai X, Zhao PX. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 2011, 39(Web Server issue):W155-W159. 10.1093/nar/gkr319, 21622958.
39. Wu HJ, Ma YK, Chen T, Wang M, Wang XJ. PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 2012, 40(Web Server issue):W22-W28. 10.1093/nar/gks554, 22693224.
40. Yang JH, Li JH, Shao P, Zhou H, Chen YQ, Qu LH. starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 2011, 39(Database issue):D202-D209. 10.1093/nar/gkq1056, 21037263.
41. Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 2012, 69(3):462-474. 10.1111/j.1365-313X.2011.04805.x, 21973320.
42. Zhao YT, Wang M, Fu SX, Yang WC, Qi CK, Wang XJ. Small RNA profiling in two Brassica napus cultivars identifies MicroRNAs with oil production-and development-correlated expression and new small RNA classes. Plant Physiol 2012, 158(2):813-823. 10.1104/pp.111.187666, 22138974.
43. Peng T, Du Y, Zhang J, Li J, Liu Y, Zhao Y, Sun H, Zhao Q. Genome-Wide Analysis of 24-nt siRNAs Dynamic Variations during Rice Superior and Inferior Grain Filling. PLoS One 2013, 8(4):e61029. 10.1371/journal.pone.0061029, 23593380.
44. Zhu G, Ye N, Yang J, Peng X, Zhang J. Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. J Exp Bot 2011, 62(11):3907-3916. 10.1093/jxb/err088, 21459770.
45. Xie K, Wu C, Xiong L. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 2006, 142(1):280-293. 10.1104/pp.106.084475, 16861571.
46. Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, Fujioka S, Feldmann KA, Pennell RI. Brassinosteroids regulate grain filling in rice. Plant Cell 2008, 20(8):2130-2145. 10.1105/tpc.107.055087, 18708477.
47. Reyes JL, Chua NH. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 2007, 49(4):592-606. 10.1111/j.1365-313X.2006.02980.x, 17217461.
48. Yang J, Zhang J, Wang Z, Liu K, Wang P. Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J Exp Bot 2006, 57(1):149-160. 10.1093/jxb/erj018, 16330527.
49. Tang T, Xie H, Wang Y, Lu B, Liang J. The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.). J Exp Bot 2009, 60(9):2641-2652. 10.1093/jxb/erp114, 19401410.
50. Zhang Z, Chen J, Lin S, Li Z, Cheng R, Fang C, Chen H, Lin W. Proteomic and phosphoproteomic determination of ABA's effects on grain-filling of Oryza sativa L. inferior spikelets. Plant Sci 2012, 185-186:259-273. 10.1016/j.plantsci.2011.11.012, 22325889.
51. Allen RS, Li J, Stahle MI, Dubroue A, Gubler F, Millar AA. Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci U S A 2007, 104(41):16371-16376. 10.1073/pnas.0707653104, 17916625.
52. Mallory AC, Bartel DP, Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 2005, 17(5):1360-1375. 10.1105/tpc.105.031716, 15829600.
53. Kinoshita N, Wang H, Kasahara H, Liu J, Macpherson C, Machida Y, Kamiya Y, Hannah MA, Chua NH. IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell 2012, 24(9):3590-3602. 10.1105/tpc.112.097006, 22960911.
54. Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 2009, 21(10):3119-3132. 10.1105/tpc.108.064758, 19820192.
55. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A. miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 2010, 22(4):1104-1117. 10.1105/tpc.109.072553, 20363771.
56. Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS. Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 2010, 38(4):1382. 10.1093/nar/gkp1128, 19969544.
57. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutie´rrez RA. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci 2010, 107(9):4477-4482. 10.1073/pnas.0909571107, 20142497.
58. Si-Ammour A, Windels D, Arn-Bouldoires E, Kutter C, Ailhas J, Meins F, Vazquez F. miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol 2011, 157(2):683-691. 10.1104/pp.111.180083, 21828251.
59. Abu-Zaitoon YM, Bennett K, Normanly J, Nonhebel HM. A large increase in IAA during development of rice grains correlates with the expression of tryptophan aminotransferase OsTAR1 and a grain-specific YUCCA. Physiol Plant 2012, 146(4):487-499. 10.1111/j.1399-3054.2012.01649.x, 22582989.
60. Zhang H, Tan G, Yang L, Yang J, Zhang J, Zhao B. Hormones in the grains and roots in relation to post-anthesis development of inferior and superior spikelets in japonica/indica hybrid rice. Plant Physiol Biochem 2009, 47(3):195-204. 19117763.
61. Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M. OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 2012, 7(1):e30039. 10.1371/journal.pone.0030039, 22253868.
62. Gardner PP, Daub J, Tate JG, Nawrocki EP, Kolbe DL, Lindgreen S, Wilkinson AC, Finn RD, Griffiths-Jones S, Eddy SR. Rfam: updates to the RNA families database. Nucleic Acids Res 2009, 37(suppl 1):D136-D140. 10.1093/nar/gkn766, 18953034.