Gradual Increase of MiR156 Regulates Temporal Expression Changes of Numerous Genes During Leaf Development in Rice

Overview

Journal Plant Physiol

Specialty Physiology

Date 2012 Jan 25

PMID 22271747

Citations 93

Authors

Kabin Xie

Jianqiang Shen

Xin Hou

Jialing Yao

Xianghua Li

Jinghua Xiao

Lizhong Xiong

Affiliations

Soon will be listed here.

Abstract

The highly conserved plant microRNA, miR156, is an essential regulator for plant development. In Arabidopsis (Arabidopsis thaliana), miR156 modulates phase changing through its temporal expression in the shoot. In contrast to the gradual decrease over time in the shoot (or whole plant), we found that the miR156 level in rice (Oryza sativa) gradually increased from young leaf to old leaf after the juvenile stage. However, the miR156-targeted rice SQUAMOSA-promoter binding-like (SPL) transcription factors were either dominantly expressed in young leaves or not changed over the time of leaf growth. A comparison of the transcriptomes of early-emerged old leaves and later-emerged young leaves from wild-type and miR156 overexpression (miR156-OE) rice lines found that expression levels of 3,008 genes were affected in miR156-OE leaves. Analysis of temporal expression changes of these genes suggested that miR156 regulates gene expression in a leaf age-dependent manner, and miR156-OE attenuated the temporal changes of 2,660 genes. Interestingly, seven conserved plant microRNAs also showed temporal changes from young to old leaves, and miR156-OE also attenuated the temporal changes of six microRNAs. Consistent with global gene expression changes, miR156-OE plants resulted in dramatic changes including precocious leaf maturation and rapid leaf/tiller initiation. Our results indicate that another gradient of miR156 is present over time, a gradual increase during leaf growth, in addition to the gradual decrease during shoot growth. Gradually increased miR156 expression in the leaf might be essential for regulating the temporal expression of genes involved in leaf development.

Citing Articles

Non-coding RNAs and their role in plants: prospective omics-tools for improving growth, development and stress tolerance in field crops.

Bashir T, Husaini A Mol Biol Rep. 2025; 52(1):249.

PMID: 39976851 DOI: 10.1007/s11033-025-10305-9.

Transcription Factors and Their Regulatory Roles in the Male Gametophyte Development of Flowering Plants.

Qian Z, Shi D, Zhang H, Li Z, Huang L, Yan X Int J Mol Sci. 2024; 25(1).

PMID: 38203741 PMC: 10778882. DOI: 10.3390/ijms25010566.

Temporal regulation of vegetative phase change in plants.

Poethig R, Fouracre J Dev Cell. 2024; 59(1):4-19.

PMID: 38194910 PMC: 10783531. DOI: 10.1016/j.devcel.2023.11.010.

Shoot Maturation Strengthens FLS2-Mediated Resistance to .

Hu L, Kvitko B, Severns P, Yang L Mol Plant Microbe Interact. 2023; 36(12):796-804.

PMID: 37638673 PMC: 10989731. DOI: 10.1094/MPMI-02-23-0018-R.

Integrating omics reveals that miRNA-guided genetic regulation on plant hormone level and defense response pathways shape resistance to in the tomato gene-carrying line.

Liu G, Liu F, Zhang D, Zhao T, Yang H, Jiang J Front Genet. 2023; 14:1158631.

PMID: 37303956 PMC: 10248068. DOI: 10.3389/fgene.2023.1158631.

References

Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S . A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell. 2003; 15(12):2900-10. PMC: 282825. DOI: 10.1105/tpc.014712. View

Xing S, Salinas M, Hohmann S, Berndtgen R, Huijser P . miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell. 2010; 22(12):3935-50. PMC: 3027167. DOI: 10.1105/tpc.110.079343. View

Miyoshi K, Ahn B, Kawakatsu T, Ito Y, Itoh J, Nagato Y . PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci U S A. 2004; 101(3):875-80. PMC: 321774. DOI: 10.1073/pnas.2636936100. View

Wang J, Czech B, Weigel D . miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell. 2009; 138(4):738-49. DOI: 10.1016/j.cell.2009.06.014. View

Wang J, Park M, Wang L, Koo Y, Chen X, Weigel D . miRNA control of vegetative phase change in trees. PLoS Genet. 2011; 7(2):e1002012. PMC: 3044678. DOI: 10.1371/journal.pgen.1002012. View

Schwab R, Palatnik J, Riester M, Schommer C, Schmid M, Weigel D . Specific effects of microRNAs on the plant transcriptome. Dev Cell. 2005; 8(4):517-27. DOI: 10.1016/j.devcel.2005.01.018. View

Varkonyi-Gasic E, Wu R, Wood M, Walton E, Hellens R . Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007; 3:12. PMC: 2225395. DOI: 10.1186/1746-4811-3-12. View

Efroni I, Blum E, Goldshmidt A, Eshed Y . A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell. 2008; 20(9):2293-306. PMC: 2570723. DOI: 10.1105/tpc.107.057521. View

Nodine M, Bartel D . MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 2010; 24(23):2678-92. PMC: 2994041. DOI: 10.1101/gad.1986710. View

10.

Lauter N, Kampani A, Carlson S, Goebel M, Moose S . microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci U S A. 2005; 102(26):9412-7. PMC: 1166634. DOI: 10.1073/pnas.0503927102. View

11.

Gandikota M, Birkenbihl R, Hohmann S, Cardon G, Saedler H, Huijser P . The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J. 2007; 49(4):683-93. DOI: 10.1111/j.1365-313X.2006.02983.x. View

12.

Yu N, Cai W, Wang S, Shan C, Wang L, Chen X . Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell. 2010; 22(7):2322-35. PMC: 2929091. DOI: 10.1105/tpc.109.072579. View

13.

Tsukaya H . Controlling size in multicellular organs: focus on the leaf. PLoS Biol. 2008; 6(7):e174. PMC: 2459211. DOI: 10.1371/journal.pbio.0060174. View

14.

Voinnet O . Origin, biogenesis, and activity of plant microRNAs. Cell. 2009; 136(4):669-87. DOI: 10.1016/j.cell.2009.01.046. View

15.

Poethig R . Phase change and the regulation of developmental timing in plants. Science. 2003; 301(5631):334-6. DOI: 10.1126/science.1085328. View

16.

Asai K, Satoh N, Sasaki H, Satoh H, Nagato Y . A rice heterochronic mutant, mori1, is defective in the juvenile-adult phase change. Development. 2002; 129(1):265-73. DOI: 10.1242/dev.129.1.265. View

17.

Mallory A, Dugas D, Bartel D, Bartel B . MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol. 2004; 14(12):1035-46. DOI: 10.1016/j.cub.2004.06.022. View

18.

Zhu Q, Upadhyaya N, Gubler F, Helliwell C . Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol. 2009; 9:149. PMC: 2803185. DOI: 10.1186/1471-2229-9-149. View

19.

Ferjani A, Horiguchi G, Yano S, Tsukaya H . Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol. 2007; 144(2):988-99. PMC: 1914195. DOI: 10.1104/pp.107.099325. View

20.

Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C . High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell. 2011; 23(3):873-94. PMC: 3082270. DOI: 10.1105/tpc.111.083345. View