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

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• 作者：Ting Peng (1) (2)
  Hongzheng Sun (1) (2)
  Mengmeng Qiao (3)
  Yafan Zhao (1) (2)
  Yanxiu Du (1) (2)
  Jing Zhang (1) (2)
  Junzhou Li (1) (2)
  Guiliang Tang (1) (3)
  Quanzhi Zhao (1) (2)
  
  1. Collaborative Innovation Center of Henan Grain Crops ; Henan Agricultural University ; Zhengzhou ; 450002 ; China
  2. Research Center for Rice Engineering in Henan Province ; Henan Agricultural University ; Zhengzhou ; 450002 ; China
  3. Department of Biological Sciences ; Michigan Technological University ; Houghton ; Michigan ; 49931 ; USA
  
• 关键词：Rice (Oryza sativa) ; microRNA ; Differential expression ; miRNA dynamics ; Inferior spikelets ; Superior spikelets ; Grain filling
• 刊名：BMC Plant Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：1,775 KB
• 参考文献：1. Fitzgerald, MA, McCouch, SR, Hall, RD (2009) Not just a grain of rice: the quest for quality. Trends Plant Sci 14: pp. 133-139 CrossRef
  2. Sakamoto, T, Matsuoka, M (2008) Identifying and exploiting grain yield genes in rice. Curr Opin Plant Biol 11: pp. 209-214 CrossRef
  3. Yang, J, Zhang, J (2010) Grain-filling problem in 'super' rice. J Exp Bot 61: pp. 1-5 CrossRef
  4. Peng, T, Lv, Q, Zhang, J, Li, J, Du, Y, Zhao, Q (2011) Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). J Exp Bot 62: pp. 4943-4954 CrossRef
  5. Zhang, H, Li, H, Yuan, L, Wang, Z, Yang, J, Zhang, J (2012) 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 63: pp. 215-227 CrossRef
  6. Tsutomu, T (2003) Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling. Funct Plant Biol 30: pp. 1139-1149 CrossRef
  7. Mohapatra, P, Patel, R, Sahu, S (1993) Time of flowering affects grain quality and spikelet partitioning within the rice panicle. Funct Plant Biol 20: pp. 231-241
  8. Khan, GA, Declerck, M, Sorin, C, Hartmann, C, Crespi, M, Lelandais-Briere, C (2011) MicroRNAs as regulators of root development and architecture. Plant Mol Biol 77: pp. 47-58 CrossRef
  9. Kidner, CA (2010) The many roles of small RNAs in leaf development. J Genet Genomics 37: pp. 13-21 CrossRef
  10. Khraiwesh, B, Zhu, JK, Zhu, J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819: pp. 137-148 CrossRef
  11. Sunkar, R, Li, YF, Jagadeeswaran, G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17: pp. 196-203 CrossRef
  12. Wang, JW, Czech, B, Weigel, D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: pp. 738-749 CrossRef
  13. Zhou, CM, Zhang, TQ, Wang, X, Yu, S, Lian, H, Tang, H, Feng, ZY, Zozomova-Lihova, J, Wang, JW (2013) Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340: pp. 1097-1100 CrossRef
  14. Liu, Q, Chen, Y-Q (2009) Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochem Biophys Res Commun 384: pp. 1-5 CrossRef
  15. Sanan-Mishra, N, Varanasi, SP, Mukherjee, SK (2013) Micro-regulators of auxin action. Plant Cell Rep 32: pp. 733-740 CrossRef
  16. Peng, T, Sun, H, Du, Y, Zhang, J, Li, J, Liu, Y, Zhao, Y, Zhao, Q (2013) Characterization and expression patterns of microRNAs involved in rice grain filling. PLoS One 8: pp. e54148 CrossRef
  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 (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31: pp. 848-852 CrossRef
  18. Lan, Y, Su, N, Shen, Y, Zhang, R, Wu, F, Cheng, Z, Wang, J, Zhang, X, Guo, X, Lei, C (2012) Identification of novel MiRNAs and MiRNA expression profiling during grain development in indica rice. BMC Genomics 13: pp. 264 CrossRef
  19. Yi, R, Zhu, Z, Hu, J, Qian, Q, Dai, J, Ding, Y (2013) Identification and expression analysis of microRNAs at the grain filling stage in rice (Oryza sativa L.) via deep sequencing. PLoS One 8: pp. e57863 CrossRef
  20. 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. Genom Res 18: pp. 1456-1465 CrossRef
  21. Xue, LJ, Zhang, JJ, Xue, HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37: pp. 916-930 CrossRef
  22. Liu, H, Jia, S, Shen, D, Liu, J, Li, J, Zhao, H, Han, S, Wang, Y (2012) Four AUXIN RESPONSE FACTORs down-regulated by microRNA167 are associated with growth and development in Oryza sativa. Funct Plant Biol 39: pp. 736-744 CrossRef
  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 (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42: pp. 541-544 CrossRef
  24. Miura, K, Ikeda, M, Matsubara, A, Song, XJ, Ito, M, Asano, K, Matsuoka, M, Kitano, H, Ashikari, M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42: pp. 545-549 CrossRef
  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 (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44: pp. 950-954 CrossRef
  26. Bian, H, Xie, Y, Guo, F, Han, N, Ma, S, Zeng, Z, Wang, J, Yang, Y, Zhu, M (2012) 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 196: pp. 149-161 CrossRef
  27. Li, R, Li, Y, Kristiansen, K, Wang, J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics (Oxford, England) 24: pp. 713-714 CrossRef
  28. Wei, LQ, Yan, LF, Wang, T (2011) Deep sequencing on genome-wide scale reveals the unique composition and expression patterns of microRNAs in developing pollen of Oryza sativa. Genome Biol 12: pp. R53 CrossRef
  29. Chen, X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: pp. 21-44 CrossRef
  30. Wu, L, Zhang, Q, Zhou, H, Ni, F, Wu, X, Qi, Y (2009) Rice MicroRNA effector complexes and targets. Plant Cell 21: pp. 3421-3435 CrossRef
  31. Li, YF, Zheng, Y, Addo-Quaye, C, Zhang, L, Saini, A, Jagadeeswaran, G, Axtell, MJ, Zhang, W, Sunkar, R (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62: pp. 742-759 CrossRef
  32. Zhou, M, Gu, L, Li, P, Song, X, Wei, L, Chen, Z, Cao, X (2010) Degradome sequencing reveals endogenous small RNA targets in rice (oryza sativa L. ssp. indica). Front Biol 5: pp. 67-90 CrossRef
  33. Zheng, Y, Li, YF, Sunkar, R, Zhang, W (2012) SeqTar: an effective method for identifying microRNA guided cleavage sites from degradome of polyadenylated transcripts in plants. Nucleic Acids Res 40: pp. e28 CrossRef
  34. Du, Z, Zhou, X, Ling, Y, Zhang, Z, Su, Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: pp. 64-70 CrossRef
  35. Guo, H-S, Xie, Q, Fei, J-F, Chua, N-H (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell Online 17: pp. 1376-1386 CrossRef
  36. Yang, JH, Han, SJ, Yoon, EK, Lee, WS (2006) Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells. Nucleic Acids Res 34: pp. 1892 CrossRef
  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 (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20: pp. 3186-3190 CrossRef
  38. Dai, X, Zhao, PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39: pp. W155-W159 CrossRef
  39. Wu, HJ, Ma, YK, Chen, T, Wang, M, Wang, XJ (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 40: pp. W22-W28 CrossRef
  40. Yang, JH, Li, JH, Shao, P, Zhou, H, Chen, YQ, Qu, LH (2011) starBase: a database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res 39: pp. D202-D209 CrossRef
  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 (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69: pp. 462-474 CrossRef
  42. Zhao, YT, Wang, M, Fu, SX, Yang, WC, Qi, CK, Wang, XJ (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: pp. 813-823 CrossRef
  43. Peng, T, Du, Y, Zhang, J, Li, J, Liu, Y, Zhao, Y, Sun, H, Zhao, Q (2013) Genome-Wide Analysis of 24-nt siRNAs Dynamic Variations during Rice Superior and Inferior Grain Filling. PLoS One 8: pp. e61029 CrossRef
  44. Zhu, G, Ye, N, Yang, J, Peng, X, Zhang, J (2011) 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 62: pp. 3907-3916 CrossRef
  45. Xie, K, Wu, C, Xiong, L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142: pp. 280-293 CrossRef
  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 (2008) Brassinosteroids regulate grain filling in rice. Plant Cell 20: pp. 2130-2145 CrossRef
  47. Reyes, JL, Chua, NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49: pp. 592-606 CrossRef
  48. Yang, J, Zhang, J, Wang, Z, Liu, K, Wang, P (2006) Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J Exp Bot 57: pp. 149-160 CrossRef
  49. Tang, T, Xie, H, Wang, Y, Lu, B, Liang, J (2009) 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 60: pp. 2641-2652 CrossRef
  50. Zhang, Z, Chen, J, Lin, S, Li, Z, Cheng, R, Fang, C, Chen, H, Lin, W (2012) Proteomic and phosphoproteomic determination of ABA's effects on grain-filling of Oryza sativa L. inferior spikelets. Plant Sci 185鈥?86: pp. 259-273 CrossRef
  51. Allen, RS, Li, J, Stahle, MI, Dubroue, A, Gubler, F, Millar, AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci U S A 104: pp. 16371-16376 CrossRef
  52. Mallory, AC, Bartel, DP, Bartel, B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17: pp. 1360-1375 CrossRef
  53. Kinoshita, N, Wang, H, Kasahara, H, Liu, J, Macpherson, C, Machida, Y, Kamiya, Y, Hannah, MA, Chua, NH (2012) IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell 24: pp. 3590-3602 CrossRef
  54. Gutierrez, L, Bussell, JD, Pacurar, DI, Schwambach, J, Pacurar, M, Bellini, C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21: pp. 3119-3132 CrossRef
  55. Marin, E, Jouannet, V, Herz, A, Lokerse, AS, Weijers, D, Vaucheret, H, Nussaume, L, Crespi, MD, Maizel, A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: pp. 1104-1117 CrossRef
  56. Yoon, EK, Yang, JH, Lim, J, Kim, SH, Kim, SK, Lee, WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38: pp. 1382 CrossRef
  57. Vidal, EA, Araus, V, Lu, C, Parry, G, Green, PJ, Coruzzi, GM, Guti茅rrez, RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci 107: pp. 4477-4482 CrossRef
  58. Si-Ammour, A, Windels, D, Arn-Bouldoires, E, Kutter, C, Ailhas, J, Meins, F, Vazquez, F (2011) miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol 157: pp. 683-691 CrossRef
  59. Abu-Zaitoon, YM, Bennett, K, Normanly, J, Nonhebel, HM (2012) 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 146: pp. 487-499 CrossRef
  60. Zhang, H, Tan, G, Yang, L, Yang, J, Zhang, J, Zhao, B (2009) 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 47: pp. 195-204
  61. Xia, K, Wang, R, Ou, X, Fang, Z, Tian, C, Duan, J, Wang, Y, Zhang, M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7: pp. e30039 CrossRef
  62. Gardner, PP, Daub, J, Tate, JG, Nawrocki, EP, Kolbe, DL, Lindgreen, S, Wilkinson, AC, Finn, RD, Griffiths-Jones, S, Eddy, SR (2009) Rfam: updates to the RNA families database. Nucleic Acids Res 37: pp. D136-D140 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background The inferior spikelets are defined to be those at portions where the grains receive less photosynthetic products during the seed development. The typical inferior spikelets are physically located on the proximal secondary branches in a rice panicle and traditionally characterized by a later flowering time and a slower grain-filling rate, compared to those so-called superior spikelets. Grains produced on the inferior spikelets are consequently under-developed and lighter in weight than those formed on the superior spikelets. MicroRNAs (miRNAs) are recognized as key players in regulating plant development through post-transcriptional gene regulations. We previously presented the evidence that miRNAs may influence grain-filling rate and played a role in determining the grain weight and yield in rice. Results In this study, further analyses of the expressed small RNAs in superior and inferior spikelets were conducted at five distinct developmental stages of grain development. Totally, 457 known miRNAs and 13 novel miRNAs were analyzed, showing a differential expression of 141 known miRNAs between superior and inferior spikelets with higher expression levels of most miRNAs associated with the superior than the inferior spikelets during the early stage of grain filling. Genes targeted by those differentially expressed miRNAs (i.e. miR156, miR164, miR167, miR397, miR1861, and miR1867) were recognized to play roles in multiple developmental and signaling pathways related to plant hormone homeostasis and starch accumulation. Conclusions Our data established a complicated link between miRNA dynamics and the traditional role of hormones in grain filling and development, providing new insights into the widely accepted concepts of the so-called superior and inferior spikelets in rice production.