A Regulatory Network for miR156-SPL Module in Arabidopsis thaliana

Abstract

Vegetative phase changes in plants describes the transition between juvenile and adult phases of vegetative growth before flowering. It is one of the most fundamental mechanisms for plants to sense developmental signals, presenting a complex process involving many still-unknown determinants. Several studies in annual and perennial plants have identified the conservative roles of miR156 and its targets, SBP/SPL genes, in guiding the switch of plant growth from juvenile to adult phases. Here, we review recent progress in understanding the regulation of miR156 expression and how miR156-SPLs mediated plant age affect other processes in Arabidopsis. Powerful high-throughput sequencing techniques have provided rich data to systematically study the regulatory mechanisms of miR156 regulation network. From this data, we draw an expanded miR156-regulated network that links plant developmental transition and other fundamental biological processes, gaining novel and broad insight into the molecular mechanisms of plant-age-related processes in Arabidopsis.

Keywords: flowering plant; gene regulatory network; miR156; next-generation sequencing; phase change.

Figure 1

Regulation pathway of MIR156 gene expression in Arabidopsis. (a) GCT/CCT regulate expression of MIR156 genes through competitive interactive with unknown transcript factor, inactivating RNA polymerase II. (b) Under low sugar conditions (left), HXK1 transcript complex bind into promoter of MIR156A/MIR156C. Then glucose incorporate with HXK1 (right), inhibiting MIR156 gene expression. (c) The decreases in the expression of MIR156A/MIR156C are regulated by the levels of histone H3 lysine 27 methylation (H3K27me3). PKL reduces the amount of H3K27ac continuously with a histone deacetylase (X). PRC2 binds to the promoter of MIR156 gene then methylates H3K27 when the levels of H3K27ac no longer inhibiting PRC2 binding. (d) BRM activates MIR156A/MIR156C expression by decreasing levels of H3K27me. Then SWN bind to BRM, releasing BRM from the promoter of MIR156A/MIR156C to increase H3K27me abundance leading to repression of miR156 expression. (e) At the initial juvenile phase, ARP6 interacts with SEF, exchanging H2A to H2A.Z, which is the deposition of H3K4me3 at the promoter region of MIR156 locus with the help of ATXR7.

Figure 2

miR156 regulates multiple development traits in Arabidopsis. (a) When plants age, the amount of miR156 decreases, while its targets’ SPL increases, directly promoting miR172 expression. Then, the AP2-like transcript factor no longer inhibits the FT gene and plant flowering. (b) miR156-SPL module active trichome distribution at inflorescence stem by direct bind to TCL/TRY gene. (c) After flowering, miR156-targeted SPLs and non-targeted SPL8 secure male fertility by interacting with SPL/NZZ or independently regulating cell division and differentiation to proper cell type (Tapetum/PMC). X indicates an unknown regulator acts as a direct downstream target. (d) With plant age, miR156-SPL-miR172 targets TOE1 to break its interaction with KAN1, leading to abaxial leaf hair initiation. (e) In the juvenile phase, TCP4, which is the target of miR319, suppresses the dimerization of CUC3 and CUC2, which is the target of miR164. Then, SPL competes with CUCs for SPL interaction, thus allows CUC2–CUC3 dimerization and increase leaf serration and complexity. (f) miR156-SPLs repress lateral root development with plant age. The direct downstream target of SPLs remains unknown.

Figure 3

miR156-SPLs modulate response to abiotic/biotic stress. (a) miR156-SPL module regulates the response to abiotic stress through their effect on anthocyanin biosynthesis. When plants encounter exogenous stress, miR156 is induced to repress SPL, preventing its interaction with PAP1 so that PAP1 bind to TTT8 and TTG1 to form MYB-bHLH-WD40 complex, which activates anthocyanin biosynthesis genes (ABGs) expression. When environment conditions recover, miR156 abundance decreases to activate SPLs, which break the MYB-bHLH-WD40 complex by competent binding to PAP1 with TTT8. (b) miR156-SPLs regulate infect and pathogen defense by regulation JA response. SPLs bind to the ZIM-domain of JAZ protein to prevent it from COI1 mediated 26s protease degradation to repress expression of JA-responsive genes (JRGs). Meanwhile, several defense components accumulate with plant age to increase insect and pathogen defense for old plants.

Figure 4

Diagram of miR156-miRNAs regulation network. The illustration of this network is based on both molecular experiments and HTS data described in the text. The asterisk indicates a verified connection between miR156 and other miRNAs.