Developmental patterning by gradients of mobile small RNAs

Current Opinion in Genetics and Development

Volumn 27, Issue , 2014, Pages 83-91

  Benkovics, Anna H ^a,b   Timmermans, Marja CP ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MIR 166; MIR 394; RNA; SMALL RNA; TASIR ARF; UNCLASSIFIED DRUG; COMPLEMENTARY RNA;

BIOGENESIS; CELL FATE; DEVELOPMENTAL BIOLOGY; EVOLUTION; FEEDBACK SYSTEM; GENE EXPRESSION; MORPHOGENESIS; NONHUMAN; PLANT DEVELOPMENT; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RNA DEGRADATION; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; STEM CELL; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BODY PATTERNING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; RNA, ANTISENSE; STEM CELLS;

EID: 84902504018     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2014.04.004     Document Type: Review

References (63)

1. Murphy E., Smith S., De Smet I. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 2012, 24:3198-3217.
2. Wu S., Gallagher K.L. Transcription factors are on the move. Curr Opin Plant Biol 2012, 15:645-651.
3. Chitwood D.H., Nogueira F.T., Howell M.D., Montgomery T.A., Carrington J.C., Timmermans M.C. Pattern formation via small RNA mobility. Genes Dev 2009, 23:549-554.
4. Carlsbecker A., et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465:316-321.
5. Miyashima S., Koi S., Hashimoto T., Nakajima K. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 2011, 138:2303-2313.
6. Skopelitis D.S., Husbands A.Y., Timmermans M.C. Plant small RNAs as morphogens. Curr Opin Cell Biol 2012, 24:217-224.
7. Husbands A.Y., Chitwood D.H., Plavskin Y., Timmermans M.C. Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 2009, 23:1986-1997.
8. Garcia D., Collier S.A., Byrne M.E., Martienssen R.A. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 2006, 16:933-938.
9. Nagasaki H., et al. The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci U S A 2007, 104:14867-14871.
10. Nogueira F.T., Madi S., Chitwood D.H., Juarez M.T., Timmermans M.C. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 2007, 21:750-755.
11. Yifhar T., et al. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 2012, 24:3575-3589.
12. Hunter C., Willmann M.R., Wu G., Yoshikawa M., de la Luz Gutierrez-Nava M., Poethig S.R. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 2006, 133:2973-2981.
13. Fahlgren N., Montgomery T.A., Howell M.D., Allen E., Dvorak S.K., Alexander A.L., Carrington J.C. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 2006, 16:939-944.
14. Nogueira F.T., Chitwood D.H., Madi S., Ohtsu K., Schnable P.S., Scanlon M.J., Timmermans M.C. Regulation of small RNA accumulation in the maize shoot apex. PLoS Genet 2009, 5:e1000320.
15. Miyashima S., Honda M., Hashimoto K., Tatematsu K., Hashimoto T., Sato-Nara K., Okada K., Nakajima K. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol 2013, 54:375-384.
16. Juarez M.T., Kui J.S., Thomas J., Heller B.A., Timmermans M.C. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428:84-88.
17. Yao X., Wang H., Li H., Yuan Z., Li F., Yang L., Huang H. Two types of cis-acting elements control the abaxial epidermis-specific transcription of the MIR165a and MIR166a genes. FEBS Lett 2009, 583:3711-3717.
18. Emery J.F., Floyd S.K., Alvarez J., Eshed Y., Hawker N.P., Izhaki A., Baum S.F., Bowman J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 2003, 13:1768-1774.
19. McConnell J.R., Emery J., Eshed Y., Bao N., Bowman J., Barton M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411:709-713.
20. Knauer S., et al. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 2013, 24:125-132.
21. Yadav R.K., Perales M., Gruel J., Girke T., Jonsson H., Reddy G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 2011, 25:2025-2030.
22. Song J.B., Huang S.Q., Dalmay T., Yang Z.M. Regulation of leaf morphology by microRNA394 and its target LEAF CURLING RESPONSIVENESS. Plant Cell Physiol 2012, 53:1283-1294.
23. Levine E., McHale P., Levine H. Small regulatory RNAs may sharpen spatial expression patterns. PLoS Comput Biol 2007, 3:e233.
24. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136:669-687.
25. Cartolano M., Castillo R., Efremova N., Kuckenberg M., Zethof J., Gerats T., Schwarz-Sommer Z., Vandenbussche M. A conserved microRNA module exerts homeotic control over Petunia hybrida and Antirrhinum majus floral organ identity. Nat Genet 2007, 39:901-905.
26. Nikovics K., Blein T., Peaucelle A., Ishida T., Morin H., Aida M., Laufs P. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 2006, 18:2929-2945.
27. Sieber P., Wellmer F., Gheyselinck J., Riechmann J.L., Meyerowitz E.M. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 2007, 134:1051-1060.
28. Wollmann H., Mica E., Todesco M., Long J.A., Weigel D. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 2010, 137:3633-3642.
29. Ashe H.L., Briscoe J. The interpretation of morphogen gradients. Development 2006, 133:385-394.
30. Lewis J. From signals to patterns: space, time, and mathematics in developmental biology. Science 2008, 322:399-403.
31. Rogers K.W., Schier A.F. Morphogen gradients: from generation to interpretation. Annu Rev Cell Dev Biol 2011, 27:377-407.
32. Tabata T., Takei Y. Morphogens, their identification and regulation. Development 2004, 131:703-712.
33. Wolpert L. One hundred years of positional information. Trends Genet 1996, 12:359-364.
34. Maule A.J., Benitez-Alfonso Y., Faulkner C. Plasmodesmata - membrane tunnels with attitude. Curr Opin Plant Biol 2011, 14:683-690.
35. Vaten A., et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell 2011, 21:1144-1155.
36. Dunoyer P., Schott G., Himber C., Meyer D., Takeda A., Carrington J.C., Voinnet O. Small RNA duplexes function as mobile silencing signals between plant cells. Science 2010, 328:912-916.
37. Molnar A., Melnyk C.W., Bassett A., Hardcastle T.J., Dunn R., Baulcombe D.C. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 2010, 328:872-875.
38. Yoo B.C., Kragler F., Varkonyi-Gasic E., Haywood V., Archer-Evans S., Lee Y.M., Lough T.J., Lucas W.J. A systemic small RNA signaling system in plants. Plant Cell 2004, 16:1979-1980.
39. Dunoyer P., Himber C., Ruiz-Ferrer V., Alioua A., Voinnet O. Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet 2007, 39:848-856.
40. Dunoyer P., Himber C., Voinnet O. DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat Genet 2005, 37:1356-1360.
41. Smith L.M., Pontes O., Searle I., Yelina N., Yousafzai F.K., Herr A.J., Pikaard C.S., Baulcombe D.C. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 2007, 19:1507-1521.
42. de Felippes F.F., Ott F., Weigel D. Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res 2011, 39:2880-2889.
43. Rogers K., Chen X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 2013, 25:2383-2399.
44. Todesco M., Balasubramanian S., Cao J., Ott F., Sureshkumar S., Schneeberger K., Meyer R.C., Altmann T., Weigel D. Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol 2012, 22:166-170.
45. Park M.Y., Wu G., Gonzalez-Sulser A., Vaucheret H., Poethig R.S. Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 2005, 102:3691-3696.
46. Manavella P.A., Hagmann J., Ott F., Laubinger S., Franz M., Macek B., Weige l.D. Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 2012, 151:859-870.
47. Jouannet V., Moreno A.B., Elmayan T., Vaucheret H., Crespi M.D., Maizel A. Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J 2012, 31:1704-1713.
48. Liu Q., Yao X., Pi L., Wang H., Cui X., Huang H. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 2009, 58:27-40.
49. Zhu H., Hu F., Wang R., Zhou X., Sze S.H., Liou L.W., Barefoot A., Dickman M., Zhang X. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2011, 145:242-256.
50. Mi S., et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell 2008, 133:116-127.
51. Montgomery T.A., et al. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 2008, 133:128-141.
52. Li S., et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 2013, 153:562-574.
53. Stalder L., et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 2013, 32:1115-1127.
54. Lynn K., Fernandez A., Aida M., Sedbrook J., Tasaka M., Masson P., Barton M.K. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 1999, 126:469-481.
55. Kim I., Hempel F.D., Sha K., Pfluger J., Zambryski P.C. Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development 2002, 129:1261-1272.
56. Kim I., Kobayashi K., Cho E., Zambryski P.C. Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 2005, 102:11945-11950.
57. Brunkard J.O., Runkel A.M., Zambryski P.C. Plasmodesmata dynamics are coordinated by intracellular signaling pathways. Curr Opin Plant Biol 2013, 16:614-620.
58. Benitez-Alfonso Y., Cilia M., San Roman A., Thomas C., Maule A., Hearn S., Jackson D. Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 2009, 106:3615-3620.
59. Zhai J., et al. Plant microRNAs display differential 3' truncation and tailing modifications that are ARGONAUTE1 dependent and conserved across species. Plant Cell 2013, 25:2417-2428.
60. Ameres S.L., Horwich M.D., Hung J.H., Xu J., Ghildiyal M., Weng Z., Zamore P.D. Target RNA-directed trimming and tailing of small silencing RNAs. Science 2010, 328:1534-1539.
61. Franco-Zorrilla J.M., et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 2007, 39:1033-1037.
62. Wu H.J., Wang Z.M., Wang M., Wang X.J. Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 2013, 161:1875-1884.
63. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.