Flowering: Keeping it cool
A well-established model for how plants start the process of flowering in periods of cold weather may need revisiting.
- Department of Molecular and Biomedical Sciences, School of Biological Sciences, The University of Adelaide, Australia
The timing of flowering is one of the most important transitions during the life of a plant. Synchronising the flowering period with warmer temperatures enhances the reproductive success of a plant (and its impact on pollinators). To do so, plants must be able to sense cold temperatures, distinguish between short- and long-term periods of cold, and remember when these changes take place. This requires a complex interplay between internal regulators and environmental cues (Simpson and Dean, 2002; Wellmer and Riechmann, 2010).
In some plants, such as the model plant Arabidopsis thaliana, prolonged periods of cold lasting several weeks are required to initiate flowering via a process known as vernalisation. During this time, a gene called Flowering Locus C (FLC), which acts as a brake to flowering, gets switched off by epigenetic processes that stably hold the gene in the off position long after the vernalisation period (Michaels and Amasino, 1999; Sheldon et al., 1999; Michaels and Amasino, 2000; Whittaker and Dean, 2017).
Several decades of intensive research using a wide range of techniques has led to a well-established model for how the flowering block imposed by FLC is regulated. A long, non-coding RNA, called COOLAIR, is thought to play an important role in this model. Since COOLAIR is an antisense RNA with a complementary sequence of nucleotides to FLC, it is assumed to be an ideal candidate for suppressing the expression of this gene. Now, in eLife, Ilha Lee and colleagues – including Myeongjune Jeon and Goowon Jeong as joint first authors – report new results that challenge this theory (Jeon et al., 2023).
To better understand the role of COOLAIR in vernalisation, the researchers – who are based at the Seoul National University, the Chinese Academy of Sciences, and the Peking University Institute of Advanced Agricultural Sciences – did a combination of molecular, genetic and physiology experiments before, during and after vernalisation in A. thaliana plants and cells to explore the role of COOLAIR and some DNA transcription factors, known as CBFs, in vernalisation.
In a search for factors involved in the early stages of the vernalisation process, Jeon et al. focussed on the cold signal transduction that regulates the transcription of COOLAIR. The results revealed that the CBFs are required for COOLAIR transcription (Figure 1). CBF proteins have been known to play a central role for plants to increase their tolerance to freezing but they had not been linked to the vernalisation response before. Moreover, the CBF-binding DNA sequence in the COOLAIR promoter (a critical sequence for transcription) is conserved amongst different plant species, suggesting the CBF-COOLAIR regulator mechanism evolved some significant time ago.
Figure 1
Vernalisation in Arabidopsis thaliana.
Some plants need a prolonged period of cold lasting several weeks to permit flowering in a process known as vernalisation. In A. thaliana, a gene called FLC stops plants from flowering during winter. During this time, FLC is highly expressed (black bars), but this activity is reduced after vernalisation. Jeong et al. show that early in the vernalisation process, CBF proteins (dark blue) bind to conserved DNA sequences (DREs) at the end of FLC to transcribe a long non-coding RNA, called COOLAIR (light blue). During vernalisation, the amount of CBFs increases, while COOLAIR levels decrease. The upstream regulator of CBF transcription remains unknown (shown as question mark).
In genetically modified plants that only had inactive forms of the genes coding for CBFs, cold-induced expression of COOLAIR was severely impaired. In modified plants with overactive CBF-coding genes, COOLAIR levels were high even when temperatures were warm. Unexpectedly, Jeon et al. found that these genetically modified plants were still able to go through vernalisation, even though they were unable to produce COOLAIR during the cold period. In addition, well described epigenetic histone modifications responsible for switching off the FLC gene remained unchanged before and after vernalisation in the genetically modified plants. This suggest that neither COOLAIR, nor the CBF transcription factors that transcribe COOLAIR, are required to induce vernalisation.
Jeon et al. used an elegant combination of genetic and molecular experiments to paint a compelling picture that suggests that the previously well-established vernalisation model requires updating. This is also in accordance with recent research, suggesting a similar theory (Helliwell et al., 2011; Luo et al., 2019). There are only a few genes where an in-depth analysis of how they are controlled has improved our overall knowledge of gene regulation. These include the trp operon genes in Escherichia coli, which regulate synthesis of the essential amino acid tryptophan and the beta-globin locus in mammals, famous for their involvement in the transport of oxygen (Yanofsky, 1981; Myers et al., 1986). It is clear the FLC locus also deserves a spot on this list.
References
-
Memories of winter: vernalization and the competence to flowerPlant, Cell and Environment 23:1145–1153.https://doi.org/10.1046/j.1365-3040.2000.00643.x
-
Gene networks controlling the initiation of flower developmentTrends in Genetics 26:519–527.https://doi.org/10.1016/j.tig.2010.09.001
-
The FLC locus: a platform for discoveries in epigenetics and adaptationAnnual Review of Cell and Developmental Biology 33:555–575.https://doi.org/10.1146/annurev-cellbio-100616-060546
Article and author information
Author details
Publication history
Copyright
© 2023, Nguyen and Searle
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 607
- views
-
- 71
- downloads
-
- 1
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Flowering: Keeping it cool
eLife 12:e86885.
https://doi.org/10.7554/eLife.86885
Further reading
-
- Chromosomes and Gene Expression
- Genetics and Genomics
The preservation of genome integrity during sperm and egg development is vital for reproductive success. During meiosis, the tumor suppressor BRCA1/BRC-1 and structural maintenance of chromosomes 5/6 (SMC-5/6) complex genetically interact to promote high fidelity DNA double strand break (DSB) repair, but the specific DSB repair outcomes these proteins regulate remain unknown. Using genetic and cytological methods to monitor resolution of DSBs with different repair partners in Caenorhabditis elegans, we demonstrate that both BRC-1 and SMC-5 repress intersister crossover recombination events. Sequencing analysis of conversion tracts from homolog-independent DSB repair events further indicates that BRC-1 regulates intersister/intrachromatid noncrossover conversion tract length. Moreover, we find that BRC-1 specifically inhibits error prone repair of DSBs induced at mid-pachytene. Finally, we reveal functional interactions of BRC-1 and SMC-5/6 in regulating repair pathway engagement: BRC-1 is required for localization of recombinase proteins to DSBs in smc-5 mutants and enhances DSB repair defects in smc-5 mutants by repressing theta-mediated end joining (TMEJ). These results are consistent with a model in which some functions of BRC-1 act upstream of SMC-5/6 to promote recombination and inhibit error-prone DSB repair, while SMC-5/6 acts downstream of BRC-1 to regulate the formation or resolution of recombination intermediates. Taken together, our study illuminates the coordinated interplay of BRC-1 and SMC-5/6 to regulate DSB repair outcomes in the germline.
-
- Chromosomes and Gene Expression
The hox operon in Synechocystis sp. PCC 6803, encoding bidirectional hydrogenase responsible for H2 production, is transcriptionally upregulated under microoxic conditions. Although several regulators for hox transcription have been identified, their dynamics and higher-order DNA structure of hox region in microoxic conditions remain elusive. We focused on key regulators for the hox operon: cyAbrB2, a conserved regulator in cyanobacteria, and SigE, an alternative sigma factor. Chromatin immunoprecipitation sequencing revealed that cyAbrB2 binds to the hox promoter region under aerobic conditions, with its binding being flattened in microoxic conditions. Concurrently, SigE exhibited increased localization to the hox promoter under microoxic conditions. Genome-wide analysis revealed that cyAbrB2 binds broadly to AT-rich genome regions and represses gene expression. Moreover, we demonstrated the physical interactions of the hox promoter region with its distal genomic loci. Both the transition to microoxic conditions and the absence of cyAbrB2 influenced the chromosomal interaction. From these results, we propose that cyAbrB2 is a cyanobacterial nucleoid-associated protein (NAP), modulating chromosomal conformation, which blocks RNA polymerase from the hox promoter in aerobic conditions. We further infer that cyAbrB2, with altered localization pattern upon microoxic conditions, modifies chromosomal conformation in microoxic conditions, which allows SigE-containing RNA polymerase to access the hox promoter. The coordinated actions of this NAP and the alternative sigma factor are crucial for the proper hox expression in microoxic conditions. Our results highlight the impact of cyanobacterial chromosome conformation and NAPs on transcription, which have been insufficiently investigated.
