The role of small RNAs in vegetative shoot development

Current Opinion in Plant Biology

Volumn 29, Issue , 2016, Pages 64-72

  Fouracre, Jim P ^a   Poethig, R Scott ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; PLANT RNA;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SHOOT;

ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; PLANT SHOOTS; RNA, PLANT;

EID: 84952673589     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2015.11.006     Document Type: Review

References (122)

1. Rogers K., Chen X. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 2013, 25:2383-2399.
2. Bologna N.G., Voinnet O. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 2014, 65:473-503.
3. Benkovics A.H., Timmermans M.C. Developmental patterning by gradients of mobile small RNAs. Curr Opin Genet Dev 2014, 27:83-91.
4. Rubio-Somoza I., Weigel D. MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 2011, 16:258-264.
5. Axtell M.J. Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 2013, 64:137-159.
6. Li J., Reichel M., Li Y., Millar A.A. The functional scope of plant microRNA-mediated silencing. Trends Plant Sci 2014, 19:750-756.
7. Hisanaga T., Miyashima S., Nakajima K. Small RNAs as positional signal for pattern formation. Curr Opin Plant Biol 2014, 21:37-42.
8. Barton M.K. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 2010, 341:95-113.
9. Barton M.K., Poethig R.S. Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of develoment in the wild type and in the shoot meristemless mutant. Development 1993, 119:823-831.
10. McConnell J.R., Barton M.K. Leaf polarity and meristem formation in Arabidopsis. Development 1998, 125:2935-2942.
11. 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.
12. Mallory A.C., Reinhart B.J., Jones-Rhoades M.W., Tang G.L., Zamore P.D., Barton M.K., Bartel D.P. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J 2004, 23:3356-3364.
13. Rhoades M.W., Reinhart B.J., Lim L.P., Burge C.B., Bartel B., Bartel D.P. Prediction of plant microRNA targets. Cell 2002, 110:513-520.
14. 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.
15. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17:61-76.
16. McConnell J.R., Barton M.K. Effect of mutations in the PINHEAD gene of Arabidopsis on the formation of shoot apical meristems. Dev Genet 1995, 16:358-366.
17. Ji L., Liu X., Yan J., Wang W., Yumul R.E., Kim Y.J., Dinh T.T., Liu J., Cui X., Zheng B., et al. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 2011, 7:e1001358.
18. 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.
19. 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.
20. Zhou Y., Honda M., Zhu H., Zhang Z., Guo X., Li T., Li Z., Peng X., Nakajima K., Duan L., et al. Spatiotemporal sequestration of miR165/166 by Arabidopsis ARGONAUTE10 promotes shoot apical meristem maintenance. Cell Rep 2015, 10:1819-1827.
21. Aida M., Ishida T., Tasaka M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOTMERISTEMLESS genes. Development 1999, 126:1563-1570.
22. Aida M., Ishida T., Fukaki H., Fujisawa H., Tasaka M. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 1997, 9:841-857.
23. Laufs P., Peaucelle A., Morin H., Traas J. MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 2004, 131:4311-4322.
24. Mallory A.C., Dugas D.V., Bartel D.P., 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, 14:1035-1046.
25. 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.
26. Knauer S., Holt A.L., Rubio-Somoza I., Tucker E.J., Hinze A., Pisch M., Javelle M., Timmermans M.C., Tucker M.R., Laux T. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 2013, 24:125-132.
27. Schoof H., Lenhard M., Haecker A., Mayer K.F.X., Jurgens G., Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100:635-644.
28. Zhou Y., Liu X., Engstrom E.M., Nimchuk Z.L., Pruneda-Paz J.L., Tarr P.T., Yan A., Kay S.A., Meyerowitz E.M. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 2015, 517:377-380.
29. Huijser P., Schmid M. The control of developmental phase transitions in plants. Development 2011, 138:4117-4129.
30. Poethig R.S. Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 2013, 105:125-152.
31. Wang J.W., Park M.Y., Wang L.J., Koo Y., Chen X.Y., Weigel D., Poethig R.S. miRNA control of vegetative phase change in trees. PLoS Genet 2011, 7:e1002012.
32. Wang Y., Wu F., Bai J., He Y. BrpSPL9 (Brassica rapa ssp. pekinensis SPL9) controls the earliness of heading time in Chinese cabbage. Plant Biotechnol J 2014, 12:312-321.
33. Zhang T., Wang J., Zhou C. The role of miR156 in developmental transitions in Nicotiana tabacum. Sci China Life Sci 2015, 58:253-260.
34. Zhang X., Zou Z., Zhang J., Zhang Y., Han Q., Hu T., Xu X., Liu H., Li H., Ye Z. Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett 2011, 585:435-439.
35. Chuck G., Cigan A.M., Saeteurn K., Hake S. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 2007, 39:544-549.
36. Xie K.B., Wu C.Q., Xiong L.Z. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 2006, 142:280-293.
37. Schwab R., Palatnik J.F., Riester M., Schommer C., Schmid M., Weigel D. Specific effects of microRNAs on the plant transcriptome. Dev Cell 2005, 8:517-527.
38. Aukerman M.J., Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 2003, 15:2730-2741.
39. Chen X.M. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004, 303:2022-2025.
40. Yu N., Cai W.J., Wang S., Shan C.M., Wang L.J., Chen X.Y. Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 2010, 22:2322-2335.
41. Shikata M., Koyama T., Mitsuda N., Ohme-Takagi M. Arabidopsis SBP-box genes SPL10 SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 2009, 50:2133-2145.
42. Yamaguchi A., Wu M.F., Yang L., Wu G., Poethig R.S., Wagner D. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY FRUITFULL, and APETALA1. Dev Cell 2009, 17:268-278.
43. Wang J.W., Czech B., Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 2009, 138:738-749.
44. Yu Z.X., Wang L.J., Zhao B., Shan C.M., Zhang Y.H., Chen D.F., Chen X.Y. Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and Patchouli (Pogostemon cablin) by the miR156-targeted SPL transcription factors. Mol Plant 2015, 8:98-110.
45. Gou J.Y., Felippes F.F., Liu C.J., Weigel D., Wang J.W. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 2011, 23:1512-1522.
46. Stief A., Altmann S., Hoffmann K., Pant B.D., Scheible W.R., Baurle I. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 2014, 26:1792-1807.
47. Cui L.G., Shan J.X., Shi M., Gao J.P., Lin H.X. The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 2014, 80:1108-1117.
48. Bergonzi S., Albani M.C., Ver Loren van Themaat E., Nordstrom K.J., Wang R., Schneeberger K., Moerland P.D., Coupland G. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 2013, 340:1094-1097.
49. Zhou C.M., Zhang T.Q., Wang X., Yu S., Lian H., Tang H., Feng Z.Y., Zozomova-Lihova J., Wang J.W. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 2013, 340:1097-1100.
50. Schwarz S., Grande A.V., Bujdoso N., Saedler H., Huijser P. The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 2008, 67:183-195.
51. Wu G., Park M.Y., Conway S.R., Wang J.W., Weigel D., Poethig R.S. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 2009, 138:750-759.
52. Rubio-Somoza I., Zhou C.M., Confraria A., Martinho C., von Born P., Baena-Gonzalez E., Wang J.W., Weigel D. Temporal control of leaf complexity by miRNA-regulated licensing of protein complexes. Curr Biol 2014, 24:2714-2719.
53. Zhang T.Q., Lian H., Tang H., Dolezal K., Zhou C.M., Yu S., Chen J.H., Chen Q., Liu H., Ljung K., et al. An intrinsic microRNA timer regulates progressive decline in shoot regenerative capacity in plants. Plant Cell 2015, 27:349-360.
54. Yu S., Galvao V.C., Zhang Y.C., Horrer D., Zhang T.Q., Hao Y.H., Feng Y.Q., Wang S., Schmid M., Wang J.W. Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell 2012, 24:3320-3332.
55. Xue X.Y., Zhao B., Chao L.M., Chen D.Y., Cui W.R., Mao Y.B., Wang L.J., Chen X.Y. Interaction between two timing microRNAs controls trichome distribution in Arabidopsis. PLoS Genet 2014, 10:e1004266.
56. Yang L., Conway S.R., Poethig R.S. Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 2011, 138:245-249.
57. Yang L., Xu M., Koo Y., He J., Poethig R.S. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2013, 2:e00260.
58. Yu S., Cao L., Zhou C.M., Zhang T.Q., Lian H., Sun Y., Wu J.Q., Huang J.R., Wang G.D., Wang J.W. Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. eLife 2013, 2:e00269.
59. Wang J.W., Schwab R., Czech B., Mica E., Weigel D. Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 2008, 20:1231-1243.
60. Wang F., Perry S.E. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 2013, 161:1251-1264.
61. Serivichyaswat P., Ryu H.S., Kim W., Kim S., Chung K.S., Kim J.J., Ahn J.H. Expression of the floral repressor miRNA156 is positively regulated by the AGAMOUS-like proteins AGL15 and AGL18. Mol Cells 2015, 38:259-266.
62. Lumba S., Tsuchiya Y., Delmas F., Hezky J., Provart N.J., Shi Lu Q., McCourt P., Gazzarrini S. The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 2012, 10:8.
63. Gillmor C.S., Silva-Ortega C.O., Willmann M.R., Buendia-Monreal M., Poethig R.S. The Arabidopsis Mediator CDK8 module genes CCT (MED12) and GCT (MED13) are global regulators of developmental phase transitions. Development 2014, 141:4580-4589.
64. Pico S., Ortiz-Marchena M.I., Merini W., Calonje M. Deciphering the role of Polycomb Repressive Complex 1 (PRC1) variants in regulating the acquisition of flowering competence in Arabidopsis. Plant Physiol 2015, 168:1286-1297.
65. Yant L., Mathieu J., Dinh T.T., Ott F., Lanz C., Wollmann H., Chen X.M., Schmid M. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 2010, 22:2156-2170.
66. Steeves T.A., Sussex I.M. Patterns in Plant Development 1989, Cambridge University Press. edn 2.
67. Juarez M.T., Kui J.S., Thomas J., Heller B.A., Timmermans M.C.P. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428:84-88.
68. Kidner C.A., Martienssen R.A. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 2004, 428:81-84.
69. 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.
70. 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.
71. Schwab R., Maizel A., Ruiz-Ferrer V., Garcia D., Bayer M., Crespi M., Voinnet O., Martienssen R.A. Endogenous TasiRNAs mediate non-cell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS One 2009, 4:e5980.
72. Li H., Xu L., Wang H., Yuan Z., Cao X., Yang Z., Zhang D., Xu Y., Huang H. The putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 2005, 17:2157-2171.
73. 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.
74. Ilegems M., Douet V., Meylan-Bettex M., Uyttewaal M., Brand L., Bowman J.L., Stieger P.A. Interplay of auxin KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 2010, 137:975-984.
75. Yu L., Yu X., Shen R., He Y. HYL1 gene maintains venation and polarity of leaves. Planta 2005, 221:231-242.
76. Jover-Gil S., Candela H., Robles P., Aguilera V., Barrero J.M., Micol J.L., Ponce M.R. The microRNA pathway genes AGO1 HEN1 and HYL1 participate in leaf proximal-distal, venation and stomatal patterning in Arabidopsis. Plant Cell Physiol 2012, 53:1322-1333.
77. Liu Z., Jia L., Wang H., He Y. HYL1 regulates the balance between adaxial and abaxial identity for leaf flattening via miRNA-mediated pathways. J Exp Bot 2011, 62:4367-4381.
78. Alonso-Peral M.M., Li J., Li Y., Allen R.S., Schnippenkoetter W., Ohms S., White R.G., Millar A.A. The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 2010, 154:757-771.
79. Nath U., Crawford B.C.W., Carpenter R., Coen E. Genetic control of surface curvature. Science 2003, 299:1404-1407.
80. Efroni I., Blum E., Goldshmidt A., Eshed Y. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 2008, 20:2293-2306.
81. Palatnik J.F., Allen E., Wu X.L., Schommer C., Schwab R., Carrington J.C., Weigel D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425:257-263.
82. Shleizer-Burko S., Burko Y., Ben-Herzel O., Ori N. Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development 2011, 138:695-704.
83. Zhou M., Li D., Li Z., Hu Q., Yang C., Zhu L., Luo H. Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol 2013, 161:1375-1380.
84. Mao Y., Wu F., Yu X., Bai J., Zhong W., He Y. MicroRNA319a-targeted Brassica rapa ssp. pekinensis TCP genes modulate head shape in chinese cabbage by differential cell division arrest in leaf regions. Plant Physiol 2014, 164:710-720.
85. Ori N., Cohen A.R., Etzioni A., Brand A., Yanai O., Shleizer S., Menda N., Amsellem Z., Efroni I., Pekker I., et al. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 2007, 39:787-791.
86. Koyama T., Mitsuda N., Seki M., Shinozaki K., Ohme-Takagi M. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 2010, 22:3574-3588.
87. Schommer C., Debernardi J.M., Bresso E.G., Rodriguez R.E., Palatnik J.F. Repression of cell proliferation by miR319-regulated TCP4. Mol Plant 2014, 7:1533-1544.
88. Efroni I., Han S.K., Kim H.J., Wu M.F., Steiner E., Birnbaum K.D., Hong J.C., Eshed Y., Wagner D. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev Cell 2013, 24:438-445.
89. Yanai O., Shani E., Russ D., Ori N. Gibberellin partly mediates LANCEOLATE activity in tomato. Plant J 2011, 68:571-582.
90. Rodriguez R.E., Mecchia M.A., Debernardi J.M., Schommer C., Weigel D., Palatnik J.F. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 2010, 137:103-112.
91. Koyama T., Furutani M., Tasaka M., Ohme-Takagi M. TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 2007, 19:473-484.
92. Liu D.M., Song Y., Chen Z.X., Yu D.Q. Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 2009, 136:223-236.
93. Wang L., Gu X.L., Xu D.Y., Wang W., Wang H., Zeng M.H., Chang Z.Y., Huang H., Cui X.F. miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 2011, 62:761-773.
94. 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.
95. Bilsborough G.D., Runions A., Barkoulas M., Jenkins H.W., Hasson A., Galinha C., Laufs P., Hay A., Prusinkiewicz P., Tsiantis M. Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci USA 2011, 108:3424-3429.
96. Hasson A., Plessis A., Blein T., Adroher B., Grigg S., Tsiantis M., Boudaoud A., Damerval C., Laufs P. Evolution and diverse roles of the CUP-SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell 2011, 23:54-68.
97. Larue C.T., Wen J., Walker J.C. A microRNA-transcription factor module regulates lateral organ size and patterning in Arabidopsis. Plant J 2009, 58:450-463.
98. Blein T., Pulido A., Vialette-Guiraud A., Nikovics K., Morin H., Hay A., Johansen I.E., Tsiantis M., Laufs P. A conserved molecular framework for compound leaf development. Science 2008, 322:1835-1839.
99. Berger Y., Harpaz-Saad S., Brand A., Melnik H., Sirding N., Alvarez J.P., Zinder M., Samach A., Eshed Y., Ori N. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 2009, 136:823-832.
100. Mallory A.C., Bartel D.P., 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, 17:1360-1375.
101. Liu P.P., Montgomery T.A., Fahlgren N., Kasschau K.D., Nonogaki H., Carrington J.C. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 2007, 52:133-146.
102. Wang J.J., Guo H.S. Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by microRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell 2015, 27:574-590.
103. 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, 157:683-691.
104. 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:e30039.
105. 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, 196:149-161.
106. Debernardi J.M., Mecchia M.A., Vercruyssen L., Smaczniak C., Kaufmann K., Inze D., Rodriguez R.E., Palatnik J.F. Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 2014, 79:413-426.
107. Oh S.A., Park J.H., Lee G.I., Paek K.H., Park S.K., Nam H.G. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 1997, 12:527-535.
108. Kim J.H., Woo H.R., Kim J., Lim P.O., Lee I.C., Choi S.H., Hwang D., Nam H.G. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 2009, 323:1053-1057.
109. Li Z., Peng J., Wen X., Guo H. ETHYLENE-INSENSITIVE3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 2013, 25:3311-3328.
110. Schommer C., Palatnik J.F., Aggarwal P., Chetelat A., Cubas P., Farmer E.E., Nath U., Weigel D. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 2008, 6:e230.
111. Sarvepalli K., Nath U. Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 2011, 67:595-607.
112. Ellis C.M., Nagpal P., Young J.C., Hagen G., Guilfoyle T.J., Reed J.W. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 2005, 132:4563-4574.
113. Lim P.O., Lee I.C., Kim J., Kim H.J., Ryu J.S., Woo H.R., Nam H.G. AUXIN RESPONSE FACTOR2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 2010, 61:1419-1430.
114. Alonso-Peral M.M., Sun C., Millar A.A. MicroRNA159 can act as a switch or tuning microRNA independently of its abundance in Arabidopsis. PLoS One 2012, 7:e34751.
115. Carlsbecker A., Lee J.Y., Roberts C.J., Dettmer J., Lehesranta S., Zhou J., Lindgren O., Moreno-Risueno M.A., Vaten A., Thitamadee S., et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465:316-321.
116. Li J., Reichel M., Millar A.A. Determinants beyond both complementarity and cleavage govern microR159 efficacy in Arabidopsis. PLoS Genet 2014, 10:e1004232.
117. Brodersen P., Sakvarelidze-Achard L., Bruun-Rasmussen M., Dunoyer P., Yamamoto Y.Y., Sieburth L., Voinnet O. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320:1185-1190.
118. Gandikota M., Birkenbihl R.P., Hohmann S., Cardon G.H., 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, 49:683-693.
119. Yang L., Wu G., Poethig R.S. Mutations in the GW-repeat protein SUO reveal a developmental function for microRNA-mediated translational repression in Arabidopsis. Proc Natl Acad Sci USA 2012, 109:315-320.
120. Li S., Liu L., Zhuang X., Yu Y., Liu X., Cui X., Ji L., Pan Z., Cao X., Mo B., et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 2013, 153:562-574.
121. 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.
122. Allen R.S., Li J., Alonso-Peral M.M., White R.G., Gubler F., Millar A.A. MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 2010, 1:18.