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VAL genes regulate vegetative phase change via miR156-dependent and independent mechanisms

['Jim P. Fouracre', 'Biology Department', 'University Of Pennsylvania', 'Philadelphia', 'Pennsylvania', 'United States Of America', 'Jia He', 'Victoria J. Chen', 'Simone Sidoli', 'Department Of Biochemistry']

Date: 2021-08

How organisms control when to transition between different stages of development is a key question in biology. In plants, epigenetic silencing by Polycomb repressive complex 1 (PRC1) and PRC2 plays a crucial role in promoting developmental transitions, including from juvenile-to-adult phases of vegetative growth. PRC1/2 are known to repress the master regulator of vegetative phase change, miR156, leading to the transition to adult growth, but how this process is regulated temporally is unknown. Here we investigate whether transcription factors in the VIVIPAROUS/ABI3-LIKE (VAL) gene family provide the temporal signal for the epigenetic repression of miR156. Exploiting a novel val1 allele, we found that VAL1 and VAL2 redundantly regulate vegetative phase change by controlling the overall level, rather than temporal dynamics, of miR156 expression. Furthermore, we discovered that VAL1 and VAL2 also act independently of miR156 to control this important developmental transition. In combination, our results highlight the complexity of temporal regulation in plants.

During their life-cycles multicellular organisms progress through a series of different developmental phases. The correct timing of the transitions between these phases is essential to ensure that development occurs at an appropriate rate and in the right order. In plants, vegetative phase change—the switch from a juvenile to an adult stage of vegetative growth prior to the onset of reproductive development–is a widely conserved transition associated with a number of phenotypic changes. It is therefore an excellent model to investigate the regulation of developmental timing. The timing of vegetative phase change is determined by a decline in the expression of a regulatory microRNA–miRNA156. However, what controls the temporal decline in miR156 expression is a major unknown in the field. In this study we tested whether members of the VAL gene family, known to be important for coordinating plant developmental transitions, are critical regulators of vegetative phase change. Using a series of genetic and biochemical approaches we found that VAL genes are important determinants of the timing of vegetative phase change. However, we discovered that VAL genes function largely to control the overall level, rather than temporal expression pattern, of miR156.

Funding: This project was funded by National Institutes of Health ( www.nih.gov ) Grant GM051893 to R.S.P. Research in the Sidoli lab is supported by the Umberto Mortari Award from Merck/MSD (2019), the Japan Agency for Medical Research and Development (AMED) and the New York Academy of Sciences (NYAS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. The raw mass spectrometry data files generated in this study are deposited on the freely accessible spectrometry data repository Chorus as part of Project No. 1706 ( https://chorusproject.org/pages/dashboard.html#/projects/all/1706/experiments ). The unprocessed and processed mass spectrometry data is also included in the S1 and S2 Datasets. The data underlying all other findings in this study are included in the S3 Dataset.

In this study we investigated whether VAL genes function as temporal regulators of vegetative phase change. We report that reduced VAL activity significantly delays the timing of vegetative phase change through both miR156-dependent and independent mechanisms. We find that the temporal decline in miR156 expression is remarkably robust and is insensitive to loss of VAL function, inhibition of VAL1-binding and the combined loss of VAL1 and PRC2 components. Finally, we show that the effects of VAL1 on the timing of vegetative phase cannot be explained by temporal changes in its interactions with other proteins.

Although there is good evidence that MIR156A/C are epigenetically silenced during vegetative development, how this mechanism is regulated temporally remains unknown. VIVIPAROUS/ABI3-LIKE (VAL) genes are excellent candidates for temporal effectors in this model. VAL genes encode B3 domain transcription factors that are closely related to the ABI3/FUSCA3 (FUS3)/LEAFY COYTLEDON2 (LEC2) clade of embryogenesis regulators. There are three VAL genes in Arabidopsis, of which VAL1 and VAL2 (also known as HSI2 and HSL2 respectively) are the most functionally important [ 25 ]. VAL proteins repress their targets by binding to 6 base pair RY-sequence motifs (CATGCA) via their B3 domain [ 26 – 32 ].

The findings that H3K27me3 replaces H3K27ac and H3K4me3 at MIR156A/C over time, and that PRC1/PRC2-activity promotes vegetative phase change, led us to propose that the temporal dynamics of miR156 accumulation are coordinated by antagonistic patterns of active (H3K27ac, H3K4me3) and repressive (H3K27me3) histone modifications [ 19 , 21 ]. In this model the stochastic removal of H3K27ac/H3K4me3 facilitates the deposition of H3K27me3 and the gradual epigenetic silencing of miR156. Similar mechanisms have been reported to function at other developmental transitions [ 22 ]. For example, during flowering, H3K27 deacetylation is a pre-requisite for PRC2-mediated H3K27me3 deposition at FLOWERING LOCUS C (FLC) [ 23 ], and during seed maturation, PRC1 promotes the exchange of H3K4me3 for H3K27me3 at DELAY OF GERMINATION1 (DOG1) and ABSCISIC ACID INSENSITIVE3 (ABI3) [ 24 ].

We have previously found that H3K27me3 increases at MIR156A/C in a PRC2-dependent manner during juvenile development, and that vegetative phase change is delayed in swn mutants [ 19 ]. The temporal deposition of H3K27me3 is accompanied by depletion of the antagonistic H3K27ac mark that is associated with active transcription. miR156 accumulation is also repressed by PRC1, as atbmi1a/b mutants exhibit delayed vegetative phase change [ 20 ]. In addition, we have found that accumulation of the active histone mark H3K4me3 decreases at MIR156A/C during vegetative development [ 21 ].

The molecular mechanisms that lead to the temporal repression of MIR156A/C are only beginning to be understood. The activity of Polycomb Group (PcG) transcriptional repressors appears critical. There are two functional complexes of PcG proteins in plants, both of which repress gene expression through covalent histone modifications. PcG repressive complex 1 (PRC1) consists of a H2A E3 ubiquitin ligase module containing one AtBMI1 protein (AtBMI1A/B/C) and one AtRING1 protein (RING1A/B). PRC1 represses gene expression through ubiquitination of H2A (H2AK121ub) [ 14 – 16 ]. The PRC2 complex includes histone methyltransferases such as CURLY LEAF (CLF) and SWINGER (SWN) and promotes H3 trimethylation (H3K27me3) [ 17 , 18 ].

Vegetative phase change is triggered by activity of members of the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) family of transcription factors, which are post-transcriptionally repressed during juvenile development by the microRNAs miR156/miR157 [ 7 – 10 ]. miR156/miR157 are encoded by multiple genes of which MIR156A and MIR156C are the most functionally significant [ 11 ]. The expression of MIR156A and MIR156C declines during juvenile growth [ 12 , 13 ], leading to the de-repression of their SPL targets and the transition to adult growth. Elucidating what controls the decline in MIR156A/C expression is therefore critical to understanding how the juvenile-to-adult transition is regulated in plants.

Flowering plant development is underpinned by transitions between stereotypical stages of growth: embryogenesis, seed maturation, juvenile and adult phases of vegetative development and flowering [ 1 ]. The correct timing of these transitions is critical to plant survival and, ultimately, reproductive success. Vegetative phase change describes the transition from juvenile-to-adult vegetative growth and is associated with changes to multiple traits, including leaf morphology, light-use efficiency, herbivore resistance and shoot physiology [ 2 – 5 ]. In Arabidopsis thaliana, the juvenile phase is characterized by small round leaves that lack both trichomes on the abaxial surface and serrations. Adult leaves, on the other hand, are larger, more elongated, serrated and produce abaxial trichomes [ 6 ].

Results

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[1] Url: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009626

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