To Bloom or Not to Bloom: Role of MicroRNAs in Plant Flowering Sachin Teotia, Guiliang Tang  Molecular Plant  Volume 8, Issue 3, Pages 359-377 (March 2015) DOI: 10.1016/j.molp.2014.12.018 Copyright © 2015 The Author Terms and Conditions

Figure 1 Five Major Pathways for Flowering Time Control in Arabidopsis: Autonomous, Vernalization, Photoperiod, Aging, and Gibberellin (GA) Pathways. Autonomous and vernalization pathways repress the activity of FLOWERING LOCUS C (FLC), a repressor of flowering. FLC represses floral pathway integrators, FLOWERING LOCUS T (FT) and SUPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1). Photoperiod pathway (long day) positively regulates FT in the leaves through the sequential activation of GIGANTEA (GI) and CONSTANS (CO), which are regulated by antagonistic control of the photoreceptors, phytochrome A (PHYA) and B (PHYB). FT protein is transported to shoot apical meristem (SAM) through phloem, where together with FD and SOC1 it channelizes the signals to induce expression of meristem identity regulators to stimulate flowering. The GA pathway mainly regulates LEAFY (LFY) expression and also crosstalks with the miR156-SPL pathway. The age pathway, through differential expression of miR156 and miR172 with plant age, represses the activity of flowering repressors and induces the expression of floral integrators, enabling the plant to respond to environmental and genetic signals to induce flowering. Autonomous pathway genes: FCA, FY, FPA, FVE; vernalization pathway genes: VERNALIZATION INSENSITIVE 3 (VIN3), VERNALIZATION 1 (VRN1), VRN2; age-pathway genes: APETALA2 (AP2), SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL). Molecular Plant 2015 8, 359-377DOI: (10.1016/j.molp.2014.12.018) Copyright © 2015 The Author Terms and Conditions

Figure 2 miRNA-Regulated Pathways in the Control of Plant Flowering Time. The miR156 pathway is shown on the left and the miR172 pathway on the right. miR156 downregulates its target genes, SPL family TFs, while miR172 downregulates the target genes of the AP2-like family. miR156 is regulated not only by the age of the plant but also by factors such as ambient temperature (AT), CO2, AGL15/18, sugar (through HXK1), and T6P (through TPS1). SPL family genes, independent of miR156, are also regulated by photoperiod in an FT-SOC1-dependent manner and putatively by TCP4 and ARF3/4. GA induces flowering by upregulating expression of SPL3, SPL4, and SPL5 genes. SPL4 expression is activated by FUL. SPL3 regulates the expression of LFY, AP1, FT, and FUL, and SPL9 directly regulates the expression of AP1, SOC1, and FUL. miR172 is regulated by AT (through FCA), SPL family genes, photoperiod (long day [LD] through GI), and GA (through SPL9). TOE1 and TOE3 repress flowering by downregulating FT. SMZ negatively regulates the expression of AP1, SOC1, and FT, the latter through FLM. miR159 is regulated by the GA pathway. The DELLA protein represses SPL9, miR159, and the expression of SPL3/4/5. miR319-TCP4 module and miR390-ARF3/4 module induce flowering through putative control over SPL3 expression. Stress-induced miR169-NF-Y module and miR399-PHO2 module regulate flowering time by regulating expression of FLC/SOC1 and TSF, respectively. miR171 controls the expression of miR156 through LOM genes while miR393 regulates flowering through control over the expression of auxin-responsive genes. miR824-AGL16 controls flowering time by altering FT expression through FRI, FLC, and SVP pathways. miR5200 represses FT-like genes under short-day conditions in Brachypodium. Broken arrow represents weak activation in comparison with a solid arrow. Arrows represent activation; line with a bar represents repression. The specific colors of arrows and bars represent the activation and/or repression activities with respect to the specific genes bearing the same color. miRNAs are shown in bold colored boxes and their respective targets are shown by boxes of the same colors. AFB1 (AUXIN SIGNALING F BOX PROTEIN 1); AGL, AGAMOUS-LIKE; AP1/2, APETALA1/2; ARF, AUXIN RESPONSE FACTOR; ARG, auxin-responsive genes; CO, CONSTANS; FLM, FLOWERING LOCUS M; FLC, FLOWERING LOCUS C; FRI, FRIGIDA; FT, FLOWERING LOCUS T; FUL, FRUTIFUL; GA, gibberellic acid; GI, GIGANTEA; HXK1, hexokinase; LFY, LEAFY; LOM, LOST MERISTEM; NF-Y, NUCLEAR FACTOR Y; PHO2, PHOSPHATE 2; PNY, PENNYWISE; PNF, POUND-FOOLISH; RGA, REPRESSOR OF GA1-3; SMZ, SCHLAFMÜTZE; SNZ, SCHNARCHZAPFEN; SOC1, SUPPRESSOR OF CONSTANS1; SPL, SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE; SVP, SHORT VEGETATIVE PHASE; ta-siRNA, trans-acting siRNA; TCP, TEOSINTE BRANCHED/CYCLOIDEA/PCF; TIR1, TRANSPORT INHIBITOR RESPONSE 1; TOE1-3, TARGET OF EAT1-3; T6P, trehalose-6-phosphate; TPS1, TREHALOSE-6-PHOSPHATE SYNTHASE1; TSF, TWIN SISTER OF FT. Molecular Plant 2015 8, 359-377DOI: (10.1016/j.molp.2014.12.018) Copyright © 2015 The Author Terms and Conditions

Figure 3 An Auto-Regulatory Loop between miR156-SPLs and miR172-AP2 Modules. Crosstalks between miR156 and miR172 modules are shown along with the regulatory networks and feedback regulation of the target genes. miR156 is regulated by positive and negative feedback loop of SPL9 and SPL15, respectively; and positively regulated by AP2 and AGL15. miR172 is regulated by the positive feedback loop of TOE1/2 and negatively by AP2 through LUG and SEU. TOE1/2 repress the expression of SPL3/4/5 genes. SPL3 positively regulates the expression of TOE3. AP2 and SMZ repress their own expression and also of other miR172 target genes. AGL15, AGAMOUS-LIKE15; AP2, APETALA2; LUG, LEUNIG; SEU, SEUSS; SMZ, SCHLAFMÜTZE; SNZ, SCHNARCHZAPFEN; SPL, SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE; TOE1-3, TARGET OF EAT1-3. Molecular Plant 2015 8, 359-377DOI: (10.1016/j.molp.2014.12.018) Copyright © 2015 The Author Terms and Conditions