VAL genes regulate vegetative phase change via miR156-dependent and independent mechanisms.
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ABSTRACT:
SUBMITTER: Fouracre JP
PROVIDER: S-EPMC8270478 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Vegetative phase change is regulated by a decrease in the abundance of the miRNAs, miR156 and miR157, and the resulting increase in the expression of their targets, SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcription factors. To determine how miR156/miR157 specify the quantitative and qualitative changes in leaf morphology that occur during vegetative phase change, we measured their abundance in successive leaves and characterized the phenotype of mutations in different MIR156 and MIR157 genes. miR156/miR157 decline rapidly between leaf 1&2 and leaf 3 and decrease more slowly after this point. The amount of miR156/miR157 in leaves 1&2 greatly exceeds the threshold required to specify their identity. Subsequent leaves have relatively low levels of miR156/miR157 and are sensitive to small changes in their abundance. In these later-formed leaves, the amount of miR156/miR157 is close to the threshold required to specify juvenile vs. adult identity; a relatively small decrease in the abundance of miR156/157 in these leaves produces a disproportionately large increase in SPL proteins and a significant change in leaf morphology. miR157 is more abundant than miR156 but has a smaller effect on shoot morphology and SPL gene expression than miR156. This may be attributable to the inefficiency with which miR157 is loaded onto AGO1, as well as to the presence of an extra nucleotide at the 5' end of miR157 that is mis-paired in the miR157:SPL13 duplex. miR156 represses different targets by different mechanisms: it regulates SPL9 by a combination of transcript cleavage and translational repression and regulates SPL13 primarily by translational repression. Our results offer a molecular explanation for the changes in leaf morphology that occur during shoot development in Arabidopsis and provide new insights into the mechanism by which miR156 and miR157 regulate gene expression.
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Project description:In higher plants, miR156 regulates the vegetative phase change via the target SBP/SPL genes. The regulation of miR156 during ontogenetic processes is not fully understood. In the apple genome, of 31 putative MdMIR156 genes that encode pre-miR156, seven were dominantly expressed. However, the transcript levels of only MdMIR156a5 and MdMIR156a12 decreased significantly during the vegetative phase change, which was consistent with the mature miR156 level, indicating that miR156 is under transcriptional regulation. Leaf H2O2 content was higher in the adult phase than in the juvenile phase because of excess H2O2 accumulation in chloroplasts. When in vitro shoots were treated with menadione, diphenyleneiodonium, L-2-oxothiazolidine-4-carboxylic acid or buthionine sulphoximine, the expressions of MdMIR156a5, MdMIR156a12, and as well miR156 were coordinated with reduced glutathione (GSH) contents and glutathione/glutathione disulfide ratio but not H2O2 contents. Alteration of miR156 expression level by MdMIR156a6-overexpressing or miR156-mimetic transgenic Nicotiana benthamiana did not cause a corresponding change in reactive oxygen species or GSH status. Collectively, the results indicate that the vegetative phase change in apple is controlled by the MdMIR156a5 and MdMIR156a12 transcriptional regulatory network in response to the plastid-nucleus redox signals, such as GSH.
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Project description:Vegetative phase change in Arabidopsis is regulated by miR156, a microRNA that promotes the expression of the juvenile phase and represses the expression of the adult phase. miR156 is expressed at a very high level early in shoot development and then decreases, leading to the onset of the adult phase. To determine the source of the factors that regulate vegetative phase change, we examined the effect of root and leaf ablation on the timing of this transition. Ablation of the root system or cotyledons had no effect on the timing of vegetative phase change, but ablation of leaf primordia delayed this transition in a miR156-dependent fashion. This treatment produced an increase in the overall abundance of miR156, which was attributable to an increase in the transcription of some, but not all, of the miR156 genes in Arabidopsis, and decreased the expression of SPL genes regulated by miR156. miR156 levels were also elevated by leaf ablation in Nicotiana benthamiana and in rejuvenating shoot apices of maize cultured in vitro. We conclude that vegetative phase change is initiated by a signal(s) produced by leaf primordia, which acts by repressing the transcription of specific members of the miR156 gene family.
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Project description:The vegetative phase transition is a prerequisite for flowering in angiosperm plants. Mulberry miR156 has been confirmed to be a crucial factor in the vegetative phase transition in Arabidopsis thaliana. The over-expression of miR156 in transgenic Populus × canadensis dramatically prolongs the juvenile phase. Here, we find that the expression of mno-miR156 decreases with age in all tissues in mulberry, which led us to study the hierarchical action of miR156 in mulberry. Utilizing degradome sequencing and dual-luciferase reporter assays, nine MnSPLs were shown to be directly regulated by miR156. The results of yeast one-hybrid and dual-luciferase reporter assays also revealed that six MnSPLs could recognize the promoter sequences of mno-miR172 and activate its expression. Our results demonstrate that mno-miR156 performs its role by repressing MnSPL/mno-miR172 pathway expression in mulberry. This work uncovered a miR156/SPLs/miR172 regulation pathway in the development of mulberry and fills a gap in our knowledge about the molecular mechanism of vegetative phase transition in perennial woody plants.
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Project description:HYL1 is an important regulator of microRNA (miRNA) biogenesis. A loss-of-function mutation of HYL1 causes the reduced accumulation of some miRNAs but fails to display the miRNA-deficient phenotypes of these miRNAs. In Arabidopsis, miR156 mediates phase transition through repression of SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL) genes. However, it remains unknown whether, and if so how, HYL1 enables phase transition through miR156. This study showed that a loss-of-function mutation of the HYL1 gene caused defects in the timing of the juvenile phase. In the primary leaves of hyl1-2 mutants, abaxial trichomes were generated prematurely, the leaf blades elongated, and the blade base angles enlarged, as is observed for adult leaves. In hyl1-2 p35S::miR156a and hyl1-2 spl9-4 spl15-1 plants, increased accumulation of miR156a and repressed expression of the SPL genes were concomitant with a complete or partial rescue of the hyl1-2 phenotype in phase defects. In contrast, overexpression of the SPL9 gene in hyl1-2 mutants led to total disappearance of the juvenile phase. Moreover, HYL1 prevented the premature accumulation of adult-related transcripts in the primary leaves. Taken together, these results suggest that HYL1 controls the expression levels of miR156-targeted SPL genes and enables plants to undergo the juvenile phase, an important and critical step during plant development to ensure maximum growth and productivity.
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Project description:Plants transition through juvenile and adult phases of vegetative development in a process known as vegetative phase change (VPC). In poplars (genus Populus) the differences between these stages are subtle, making it difficult to determine when this transition occurs. Previous studies of VPC in poplars have relied on plants propagated in vitro, leaving the natural progression of this process unknown. We examined developmental morphology of seed-grown and in vitro derived Populus tremula × alba (clone 717-1B4), and compared the phenotype of these to transgenics with manipulated miR156 expression, the master regulator of VPC. In seed-grown plants, most traits changed from node-to-node during the first 3 months of development but remained constant after node 25. Many traits remained unchanged in clones over-expressing miR156, or were enhanced when miR156 was lowered, demonstrating their natural progression is regulated by the miR156/SPL pathway. The characteristic leaf fluttering of Populus is one of these miR156-regulated traits. Vegetative development in plants grown from culture mirrored that of seed-grown plants, allowing direct comparison between plants often used in research and those found in nature. These results provide a foundation for further research on the role of VPC in the ecology and evolution of this economically important genus.
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Project description:Plants that develop under low light (LL) intensity often display a phenotype known as the "shade tolerance syndrome (STS)". This syndrome is similar to the phenotype of plants in the juvenile phase of shoot development, but the basis for this similarity is unknown. We tested the hypothesis that the STS is regulated by the same mechanism that regulates the juvenile vegetative phase by examining the effect of LL on rosette development in Arabidopsis (Arabidopsis thaliana). We found that LL prolonged the juvenile vegetative phase and that this was associated with an increase in the expression of the master regulators of vegetative phase change, miR156 and miR157, and a decrease in the expression of their SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL) targets. Exogenous sucrose partially corrected the effect of LL on seedling development and miR156 expression. Our results suggest that the response of Arabidopsis to LL is mediated by an increase in miR156/miR157 expression and by factors that repress SPL gene expression independently of miR156/miR157, and is caused in part by a decrease in carbohydrate production. The effect of LL on vegetative phase change does not require the photoreceptors and transcription factors responsible for the shade avoidance syndrome, implying that light intensity and light quality regulate rosette development through different pathways.
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Project description:As sessile organisms, the precise development phase transitions are very important for the success of plant adaptability, survival and reproduction. The transition from juvenile to the adult phase-referred to as the vegetative phase change-is significantly influenced by numbers of endogenous and environmental signals. Here, we showed that brassinosteroid (BR), a major growth-promoting steroid hormone, positively regulates the vegetative phase change in Arabidopsis thaliana. The BR-deficient mutant det2-1 and BR-insensitive mutant bri1-301 displayed the increased ratio of leaf width to length and reduced blade base angle. The plant specific transcription factors SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) are key masters for the vegetative phase transition in plants. The expression levels of SPL9, SPL10 and SPL15 were significantly induced by BR treatment, but reduced in bri1-116 mutant compared to wild-type plants. The gain-of-function pSPL9:rSPL9 transgenic plants displayed the BR hypersensitivity on hypocotyl elongation and partially suppressed the delayed vegetative phase change of det2-1 and bri1-301. Furthermore, we showed that BRASSINAZOLE-RESISTANT 1 (BZR1), the master transcription factor of BR signaling pathway, interacted with SPL9 to cooperatively regulate the expression of downstream genes. Our findings reveal an important role for BRs in promoting vegetative phase transition through regulating the activity of SPL9 at transcriptional and post-transcriptional levels.
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