RESUMO
Many developmental processes associated with fruit development occur at the floral meristem (FM). Age-regulated microRNA156 (miR156) and gibberellins (GAs) interact to control flowering time, but their interplay in subsequent stages of reproductive development is poorly understood. Here, in tomato (Solanum lycopersicum), we show that GA and miR156-targeted SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL or SBP) genes interact in the tomato FM and ovary patterning. High GA responses or overexpression of miR156 (156OE), which leads to low expression levels of miR156-silenced SBP genes, resulted in enlarged FMs, ovary indeterminacy and fruits with increased locule number. Conversely, low GA responses reduced indeterminacy and locule number, and overexpression of a S. lycopersicum (Sl)SBP15 allele that is miR156 resistant (rSBP15) reduced FM size and locule number. GA responses were partially required for the defects observed in 156OE and rSBP15 fruits. Transcriptome analysis and genetic interactions revealed shared and divergent functions of miR156-targeted SlSBP genes, PROCERA/DELLA and the classical WUSCHEL/CLAVATA pathway, which has been previously associated with meristem size and determinacy. Our findings reveal that the miR156/SlSBP/GA regulatory module is deployed differently depending on developmental stage and create novel opportunities to fine-tune aspects of fruit development that have been important for tomato domestication.
Assuntos
MicroRNAs , Solanum lycopersicum , Giberelinas/metabolismo , Solanum lycopersicum/genética , Flores , Meristema/metabolismo , Ovário/metabolismo , Regulação da Expressão Gênica de Plantas/genética , Proteínas de Plantas/metabolismo , MicroRNAs/genética , MicroRNAs/metabolismoRESUMO
The miRNA156 (miR156)/SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL/SBP) regulatory hub is highly conserved among phylogenetically distinct species, but how it interconnects multiple pathways to converge to common integrators controlling shoot architecture is still unclear. Here, we demonstrated that the miR156/SlSBP15 node modulates tomato shoot branching by connecting multiple phytohormones with classical genetic pathways regulating both axillary bud development and outgrowth. miR156-overexpressing plants (156-OE) displayed high shoot branching, whereas plants overexpressing a miR156-resistant SlSBP15 allele (rSBP15) showed arrested shoot branching. Importantly, the rSBP15 allele was able to partially restore the wild-type shoot branching phenotype in the 156-OE background. rSBP15 plants have tiny axillary buds, and their activation is dependent on shoot apex-derived auxin transport inhibition. Hormonal measurements revealed that indole-3-acetic acid (IAA) and abscisic acid (ABA) concentrations were lower in 156-OE and higher in rSBP15 axillary buds, respectively. Genetic and molecular data indicated that SlSBP15 regulates axillary bud development and outgrowth by inhibiting auxin transport and GOBLET (GOB) activity, and by interacting with tomato BRANCHED1b (SlBRC1b) to control ABA levels within axillary buds. Collectively, our data provide a new mechanism by which the miR156/SPL/SBP hub regulates shoot branching, and suggest that modulating SlSBP15 activity might have potential applications in shaping tomato shoot architecture.
Assuntos
MicroRNAs , Proteínas de Plantas , Solanum lycopersicum , Regulação da Expressão Gênica de Plantas , Hormônios , MicroRNAs/genética , MicroRNAs/metabolismo , Brotos de Planta/metabolismo , Plantas Geneticamente Modificadas/genética , Regiões Promotoras Genéticas , Solanum lycopersicum/genética , Proteínas de Plantas/metabolismoRESUMO
Age-regulated microRNA156 (miR156) and targets similarly control the competence to flower in diverse species. By contrast, the diterpene hormone gibberellin (GA) and the microRNA319-regulated TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factors promote flowering in the facultative long-day Arabidopsis thaliana, but suppress it in the day-neutral tomato (Solanum lycopersicum). We combined genetic and molecular studies and described a new interplay between GA and two unrelated miRNA-associated pathways that modulates tomato transition to flowering. Tomato PROCERA/DELLA activity is required to promote flowering along with the miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE (SPL/SBP) transcription factors by activating SINGLE FLOWER TRUSS (SFT) in the leaves and the MADS-Box gene APETALA1(AP1)/MC at the shoot apex. Conversely, miR319-targeted LANCEOLATE represses floral transition by increasing GA concentrations and inactivating SFT in the leaves and AP1/MC at the shoot apex. Importantly, the combination of high GA concentrations/responses with the loss of SPL/SPB function impaired canonical meristem maturation and flower initiation in tomato. Our results reveal a cooperative regulation of tomato floral induction and flower development, integrating age cues (miR156 module) with GA responses and miR319-controlled pathways. Importantly, this study contributes to elucidate the mechanisms underlying the effects of GA in controlling flowering time in a day-neutral species.
Assuntos
Flores/crescimento & desenvolvimento , Giberelinas/metabolismo , MicroRNAs/metabolismo , Solanum lycopersicum/crescimento & desenvolvimento , Solanum lycopersicum/genética , Inflorescência/crescimento & desenvolvimento , Meristema/crescimento & desenvolvimento , MicroRNAs/genética , Modelos Biológicos , Mutação/genética , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismoRESUMO
Alterations in the timing of developmental programs during evolution, that lead to changes in the shape, or size of organs, are known as heterochrony. Heterochrony has been widely studied in animals, but has often been neglected in plants. During plant evolution, heterochronic shifts have played a key role in the origin and diversification of leaves, roots, flowers, and fruits. Heterochrony that results in a juvenile or simpler outcome is known as paedomorphosis, while an adult or more complex outcome is called peramorphosis. Mechanisms that alter developmental timing at the cellular level affect cell proliferation or differentiation, while those acting at the tissue or organismal level change endogenous aging pathways, morphogen signaling, and metabolism. We believe that wider consideration of heterochrony in the context of evolution will contribute to a better understanding of plant development.
RESUMO
UV-B is a high-energy component of the solar radiation perceived by the plant and induces a number of modifications in plant growth and development, including changes in flowering time. However, the molecular mechanisms underlying these changes are largely unknown. In the present work, we demonstrate that Arabidopsis plants grown under white light supplemented with UV-B show a delay in flowering time, and this developmental reprogramming is mediated by the UVR8 photoreceptor. Using a combination of gene expression analyses and UV-B irradiation of different flowering mutants, we gained insight into the pathways involved in the observed flowering time delay in UV-B-exposed Arabidopsis plants. We provide evidence that UV-B light downregulates the expression of MSI1 and CLF, two of the components of the polycomb repressive complex 2, which in consequence drives a decrease in H3K27me3 histone methylation of MIR156 and FLC genes. Modification in the expression of several flowering time genes as a consequence of the decrease in the polycomb repressive complex 2 activity was also determined. UV-B exposure of flowering mutants supports the involvement of this complex in the observed delay in flowering time, mostly through the age pathway.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/genética , Arabidopsis/efeitos da radiação , Flores/fisiologia , Flores/efeitos da radiação , MicroRNAs/metabolismo , Proteínas Repressoras/metabolismo , Raios Ultravioleta , Arabidopsis/fisiologia , Proteínas de Arabidopsis/genética , Regulação para Baixo/genética , Flores/genética , Regulação da Expressão Gênica de Plantas/efeitos da radiação , Genes de Plantas , Histonas/metabolismo , Lisina/metabolismo , Metilação , MicroRNAs/genética , Mutação/genética , Complexo Repressor Polycomb 2 , Fatores de TempoRESUMO
In Arabidopsis, leaves produced during the juvenile vegetative phase are simple, while adult leaves are morphologically complex. The juvenile to adult transition is regulated by miR156, a microRNA that promotes juvenility by impeding the function of SPL transcription factors, which specify adult leaf traits. Both leaf derived sugars, as well as the Mediator Cyclin Dependent Kinase 8 (CDK8) module genes CENTER CITY (CCT)/MED12 and GRAND CENTRAL (GCT)/MED13, act upstream of miR156 to promote the juvenile to adult transition. However, it is not known whether sugar, CCT and GCT repress miR156 independently, as part of the same pathway, or in a cooperative manner. Here we show that sugar treatment can repress MIR156 expression in the absence of CCT or GCT. Both cct and the photosynthetic mutant chlorina1 (ch1) (which decreases sugar synthesis) exhibit extended juvenile development and increased MIR156A and MIR156C expression. Compared to ch1 and cct single mutants, the ch1 cct double mutant has a stronger effect on juvenile leaf traits, higher MIR156C levels, and a dramatic increase in MIR156A. Our results show that sugar and the CDK8 module are capable of regulating MIR156 independently, but suggest they normally act together in a synergistic manner.
Assuntos
Proteínas de Arabidopsis/metabolismo , Arabidopsis/genética , Carboidratos/farmacologia , Quinase 8 Dependente de Ciclina/metabolismo , Complexo Mediador/metabolismo , MicroRNAs/metabolismo , Proteínas Repressoras/metabolismo , Arabidopsis/efeitos dos fármacos , Proteínas de Arabidopsis/genética , Flores/efeitos dos fármacos , Flores/fisiologia , Regulação da Expressão Gênica no Desenvolvimento/efeitos dos fármacos , Regulação da Expressão Gênica de Plantas/efeitos dos fármacos , MicroRNAs/genética , Mutação/genética , Característica Quantitativa Herdável , RNA Mensageiro/genética , RNA Mensageiro/metabolismo , Reprodução/efeitos dos fármacosRESUMO
Temporal coordination of developmental programs is necessary for normal ontogeny, but the mechanism by which this is accomplished is still poorly understood. We have previously shown that two components of the Mediator CDK8 module encoded by CENTER CITY (CCT; Arabidopsis MED12) and GRAND CENTRAL (GCT; Arabidopsis MED13) are required for timing of pattern formation during embryogenesis. A morphological, molecular and genomic analysis of the post-embryonic phenotype of gct and cct mutants demonstrated that these genes also promote at least three subsequent developmental transitions: germination, vegetative phase change, and flowering. Genetic and molecular analyses indicate that GCT and CCT operate in parallel to gibberellic acid, a phytohormone known to regulate these same three transitions. We demonstrate that the delay in vegetative phase change in gct and cct is largely due to overexpression of miR156, and that the delay in flowering is due in part to upregulation of FLC. Thus, GCT and CCT coordinate vegetative and floral transitions by repressing the repressors miR156 and FLC. Our results suggest that MED12 and MED13 act as global regulators of developmental timing by fine-tuning the expression of temporal regulatory genes.