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Plant Growth Regulation

, Volume 85, Issue 3, pp 351–361 | Cite as

Functional characterization of OsmiR396a in rice (Oryza sativa L.)

  • Zhijuan Diao
  • Minxiang Yu
  • Suhong Bu
  • Yuanlin Duan
  • Licong Zhang
  • Weiren Wu
Review paper

Abstract

miR396 is a conservative microRNA family, which has been shown to be important for plant growth and development. To investigate the functions of miR396 in rice (Oryza sativa L.), we carried out a study on OsmiR396a. We found that OsmiR396a was expressed in various tissues with highest transcriptional level in leaves. Bioinformatic prediction suggested that OsmiR396a targets nine Growth Regulating Factor(GRF) genes, of which four (OsGRF1/2/6/8) were significantly down regulated by overexpression of OsmiR396a (aOE). aOE severely suppressed cell proliferation, leading to dwarf plants with smaller leaves. aOE also resulted in abnormal panicles and spikelets, especially a large proportion of rare conjoined-twin florets. Consistent with these defects, some related genes, including H4-2 and OsRAN2 (involved in cell division), FZP and LAX1 (controlling inflorescence architecture) and various floral organ identity genes (involved in floral development), exhibited significantly altered expressional levels in the aOE plants. Our findings further demonstrated the functional conservation of miR396 across dicot and monocot plants and suggested that OsmiR396a functions mainly by targeting OsGRF genes and indirectly regulating many downstream genes in rice.

Keywords

Rice OsmiR396a Overexpression Functional characterization 

Notes

Acknowledgements

We thank Dr. Tao Lan, Dr. Mo Wang, Dr. Xiaofang Xie, Junjie Lin, Chunfen Lai, Binqing Lin, Qin Lin, Huan Chen and Owie Swithin Omosuwa for their help in the experiments. This work was supported by National Natural Science Foundation of China (Project No.: 31301003).

Author contributions

ZD: Conceived and designed the experiments, performed the experiments, analyzed the data, contributed regents/materials/analysis tools and wrote the paper. WW: Conceived and designed the experiments, analyzed the data, contributed regents/materials/analysis tools and wrote the paper. MY: Performed the experiments, analyzed the data and wrote the paper. SB: Analyzed the data. YD: Contributed regents/materials/analysis tools. LZ: Performed the experiments.

Compliance with ethical standards

Conflict of interest

The authors declare no potential competing interests.

Supplementary material

10725_2018_406_MOESM1_ESM.doc (8 mb)
Supplementary material 1 (DOC 8195 KB)

References

  1. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bao M, Bian H, Zha Y, Li F, Sun Y, Bai B, Chen Z, Wang J, Zhu M, Han N (2014) miR396a-Mediated basic helix-loop-helix transcription factor bHLH74 repression acts as a regulator for root growth in Arabidopsis seedlings. Plant Cell Physiol 55:1343–1353CrossRefPubMedGoogle Scholar
  3. Bartel B, Bartel DP (2003) MicroRNAs: at the root of plant development? Plant Physiol 132:709–717CrossRefPubMedPubMedCentralGoogle Scholar
  4. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338CrossRefPubMedGoogle Scholar
  5. Carthew RW, Sontheimer EJ (2009) Origins and Mechanisms of miRNAs and siRNAs. Cell 136:642–655CrossRefPubMedPubMedCentralGoogle Scholar
  6. Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013) Repression of growth regulating factors by the microRNA396 inhibits cell proliferation by UV-B radiation in Arabidopsis leaves. Plant Cell 25:3570–3583CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chen XM (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025CrossRefPubMedGoogle Scholar
  8. Chen X (2005) MicroRNA biogenesis and function in plants. FEBS Lett 579:5923–5931CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen N, Xu Y, Wang X, Du C, Du J, Yuan M, Xu Z, Chong K (2010) OsRAN2, essential for mitosis, enhances cold tolerance in rice by promoting export of intranuclear tubulin and maintaining cell division under cold stress. Plant Cell Environ 34:52–64CrossRefPubMedGoogle Scholar
  10. Debernardi JM, Rodriguez RE, Mecchia MA, Palatnik JF (2012) Functional specialization of the plant miR396 regulatory network through distinct microRNA-target interactions. PLoS Genet 8:e1002419CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dreni L, Jacchia S, Fornara F, Fornari M, Ouwerkerk PBF, An G, Colombo L, Kater MM (2007) The D-lineage MADS-box gene OsMADS13 controls ovule identity in rice. Plant J 52:690–699CrossRefPubMedGoogle Scholar
  12. Duan CG, Wang CH, Guo HS (2006) Regulation of microRNA on plant development and viral infection. Chin Sci Bull 51:269–278CrossRefGoogle Scholar
  13. Duan Y, Xing Z, Diao Z, Xu W, Li S, Du X, Wu G, Wang C, Lan T, Meng Z, Liu H, Wang F, Wu W, Xue Y (2012) Characterization of Osmads6-5, a null allele, reveals that OsMADS6 is a critical regulator for early flower development in rice (Oryza sativa L.). Plant Mol Biol 80(4–5):429–442CrossRefPubMedGoogle Scholar
  14. Fang Y, Xie K, Xiong L (2014) Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. J Exp Bot 65:2119–2135CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gao P, Bai X, Yang L, Lv D, Li Y, Cai H, Ji W, Guo D, Zhu Y (2010) Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta 231:991–1001CrossRefPubMedGoogle Scholar
  16. Gao F, Wang K, Liu Y, Chen Y, Chen P, Shi Z, Luo J, Jiang D, Fan F, Zhu Y, Li S (2015) Blocking miR396 increases rice yield by shaping inflorescence architecture. Nature Plants 2:15196CrossRefPubMedGoogle Scholar
  17. Hewezi T, Baum TJ (2012) Complex feedback regulations govern the expression of miRNA396 and its GRF target genes. Plant Signal Behav 7:749–751CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282CrossRefPubMedGoogle Scholar
  19. Horiguchi G, Kim GT, Tsukaya H (2005) The transcriptionfactor AtGRF5 and the transcription coactivator AN3cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78CrossRefPubMedGoogle Scholar
  20. Ikeda K, Sunohara H, Nagato Y (2004) Developmental course of inflorescence and spikelet in rice. Breed Sci 54:147–156CrossRefGoogle Scholar
  21. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799CrossRefPubMedGoogle Scholar
  22. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53CrossRefPubMedGoogle Scholar
  23. Jung JH, Lee S, Yun J, Lee M, Park CM (2014) The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci 215–216:29–38CrossRefPubMedGoogle Scholar
  24. Kamiuchi Y, Yamamoto K, Furutani M, Tasaka M, Aida M (2014) The CUC1 and CUC2 genes promote carpel margin meristem formation during Arabidopsis gynoeciumdevelopment. Front Plant Sci 5:165CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kater MM, Dreni L, Colombo L (2006) Functional conservation of MADS-box factorscontrolling floral organ identity in rice and Arabidopsis. J Exp Bot 57(13):3433–3444CrossRefPubMedGoogle Scholar
  26. Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl AcadSci USA 101:13374–13379CrossRefGoogle Scholar
  27. Kim JH, Choi DS, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104CrossRefPubMedGoogle Scholar
  28. Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Kim VN, Chua NH, Park CM (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42:84–94CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kim BH, Kwon Y, Lee BH, Nam KH (2014) Overexpression of miR172 suppresses the brassinosteroid signaling defects of bak1 in Arabidopsis. Biochem Biophys Res Commun 447:479–484CrossRefPubMedGoogle Scholar
  30. Komatsu M, Maekawa M, Shimamoto K, Kyozuka J (2001) The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev Biol 231:364–373CrossRefPubMedGoogle Scholar
  31. Komatsu M, Chujo A, Nagato Y, Shimamoto K, Kyozuka J (2003) FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development 130:3841–3850CrossRefPubMedGoogle Scholar
  32. Liang G, He H, Li Y, Wang F, Yu D (2014) Molecular mechanism of microRNA396 mediating pistil development in Arabidopsis. Plant Physiol 164:249–258CrossRefPubMedGoogle Scholar
  33. Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136:223–236CrossRefPubMedGoogle Scholar
  34. Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen HA, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62:416–428CrossRefPubMedGoogle Scholar
  35. Liu H, Guo S, Xu Y, Li C, Zhang Z, Zhang D, Xu S, Zhang C, Chong K (2014) Osa-miR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol 165:160–174CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046CrossRefPubMedGoogle Scholar
  37. Mecchia MA, Debernardi JM, Rodriguez RE, Schommer C, Palatnik JF (2013) MicroRNA miR396 and RDR6 synergistically regulate leaf development. Mech Dev 130:2–13CrossRefPubMedGoogle Scholar
  38. Palatnik JF, Allen E, Wu XL, Schommer C, Schwab R, Carrington JC, Detlef W (2003) Control of leaf morphogenesis by MicroRNAs. Nature 425:257–263CrossRefPubMedGoogle Scholar
  39. Pelucchi N, Fornara F, Favalli C, Msiero S, Lago C, Pe MF, Colombo L, Kater MM (2002) Comparative analysis of rice MADS-box genes expressed during flower development. Sex Plant Reprod 15:113–122CrossRefGoogle Scholar
  40. Qin Y, Duan Z, Xia X, Yin W (2011) Expression profiles of precursor and mature microRNAs under dehydration and high salinity shock in Populus euphratica. Plant Cell Rep 30:1893–1907CrossRefPubMedGoogle Scholar
  41. Ramanjulu S, Guru J (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 8:37CrossRefGoogle Scholar
  42. Ramanjulu S, Thomas G, Pradeep KJ, Jian-Kang Z (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411CrossRefGoogle Scholar
  43. Schommer C, Debernardi JM, Bresso EG, Rodriguez RE, Palatnik JF (2014) Repression of cell proliferation by miR319-regulated TCP4. Mol Plant 7:1533–1544CrossRefPubMedGoogle Scholar
  44. Tobina H, Uozu S, Matsuoka M, Kitano H, Hattori K (2003) Gene expression pattern of cell division/elongation factors in rice dwarf mutants. In: Khush GS, Brar DS, Hardy B (eds) In advances in rice genetics. International Rice Research Institute, Manila, pp 470–472Google Scholar
  45. Tsuzuki M, Takeda A, Watanabe Y (2014) Recovery of dicer-like 1-late flowering phenotype by miR172 expressed by the noncanonical DCL4-dependent biogenesis pathway. RNA 20:1320–1327CrossRefPubMedPubMedCentralGoogle Scholar
  46. Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668CrossRefPubMedGoogle Scholar
  47. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yang C, Li D, Mao D, Liu X, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ 36:2207–2218CrossRefPubMedGoogle Scholar
  49. Zhang B, Wang Q, Pan X (2007) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289CrossRefPubMedGoogle Scholar
  50. Zhou S, Wang Y, Li W, Zhao Z, Ren Y, Wang Y, Gu S, Lin Q, Wang D, Jiang L, Su N, Zhang X, Liu L, Cheng Z, Lei C, Wang J, Guo X, Wu F, Ikehashi H, Wang H, Wan J (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23(1):111–129CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life SciencesFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of EducationFujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.Fujian Key Laboratory of Crop Breeding by DesignFujian Agriculture and Forestry UniversityFuzhouChina

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