EPIGENETIC REGULATION OF AGRONOMIC TRAITS


Group leader: Pedro Crevillen Lomas - Researcher CSIC-INIA
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INTRODUCTION


Epigenetics, the study of heritable changes in gene function that occur without altering the DNA sequence, is a hot topic in biology nowadays. Epigenetic modifications include DNA methylation, histone posttranslational modifications, chromatin remodelling and the actions of non-coding RNAs. These modifications are crucial regulating gene transcription, ultimately determining cell identity and function.

In plants, epigenetic modifications are essential for development and response to environmental cues. Leveraging epigenetic variation provides exciting opportunities for obtaining novel crop varieties more efficiently. By exploiting these modifications, we aim to identify genetic differences between plant species, develop transfer strategies, and improve crop yields and sustainability. Plant epigenetics is a rapidly evolving area of research that have the potential to revolutionize agriculture and improve food security.

In our lab, we work with the model plant Arabidopsis thaliana and related Brassica crops species such as Brassica rapa (turnip, Chinese cabbage) and Brassica napus (oilseed rape). We are studying the impact of epigenetic mechanisms on plant development, genome organization and fundamental cell processes like transcription using molecular genetics, biochemical analyses and state-of-the-art epigenomics approaches.




Figure 1. Translational research program from Arabidopsis to Brassica crops.

 

 

RESEARCH LINES



1. ROLE OF HISTONE DEMETHYLASES ON FLOWERING TIME REGULATION


Much of our research concentrate on the Jumonji-C domain protein (JmjC) family, which comprises histone demethylases that regulate the levels of H3 trimethylation (H3K27me3), an evolutionarily conserved epigenetic mark associated with gene silencing in both animal and plant cells.

 



Figure 2. Gene activation and transcriptional reprogramming by H3K27 demethylases

 

Plants flower in response to a defined set of endogenous and environmental cues like photoperiod or temperature. This developmental switch is an important crop trait because untimely flowering reduces crop yields. We have a longstanding interest in studying flowering time in Arabidopis and Brassica crops. Our research has revealed both conserved and distinct roles for H3K27me3 demethylases in the regulation of flowering time in A. Arabidopis and Brassica crops. This knowledge contributes to a better understanding of the epigenetic control of flowering time in plants, shedding light on the shared and unique regulatory mechanisms across different plant species.

 

Figure 3. Epigenetic mechanisms regulating flowering are conserved but work differently between model plants and Brassica crops.

 

 

2. DECIPHERING THE PLANT EPIGENOME


Epigenome studies in plant crops and its comparison with model plant systems is scarce. In collaboration with the Biological Informatics group at CBGP we are investigating, we are producing new state-of-the-art epigenome dataset and develop new computational methods to precisely infer different epigenetic states in plants.

 



Figure 4. ChIP-seq analysis of H3K27me3 regions.
IGV viewer snapshots showing the H3K27me3 ChIP-seq and 3’RNA-seq data of BraA.AG.a in B. rapa leaves and inflorescences

 

 

3. MECHANISMS OF PLANT TOLERANCE TO VIRUSES BY VIRUS-INDUCED FLOWERING TIME REGULATION


Flowering time regulation has been much studied in Arabidopsis, however their regulation in response to pathogen infection has not been analyse. In collaboration with the Plant-virus interaction and coevolution group at CBGP we are analysing the role of master floral regulators in plant-virus interactions. This research line significantly contributes to understand the interaction between plant development and plant-pathogen interactions, a novel area of research that may become soon a hot topic.

 

 

Figure 5. Plant tolerance to CMV virus. Functional alleles of the flowering genes FLC and FRI are required for both tolerance of Arabidopsis thaliana to cucumber mosaic virus (CMV) and resource reallocation from growth to reproduction.

 

 

4. EFFECT OF FLUCTUATING TEMPERATURES ON CHROMATIN SILENCING


Plant development occurs at different pace in diverse ambient temperatures but also under constant versus fluctuating temperature conditions. In collaboration with the Turck lab at the MPIPZ (Germany), under the CBGP-CEPLAS International Collaborative Scientific Program, we are investigating how changes in chromatin states are associated with both short-term and long-term responses to fluctuating ambient temperatures. This research is crucial for gaining a better understanding of how plants adapt to temperature changes, which, in turn, is essential for developing crops that are resilient to the challenges of climate change.

 

 

 Figure 6. Working model for the chromatin mediated regulation of Arabidopsis and B. rapa FT loci in response to warm ambient temperature.

 

 

5. NEW MECHANISMS LINKING NON-CODING RNA TRANSCRIPTION AND EPIGENETIC SILENCING


We recently started a new line of research lead by Eduardo Mateo-Bonmatí studying how non-coding RNA contribute to chromatin-mediated regulation of transcription. Gene transcription in eukaryotic genomes involves a complex interplay between trans factors and chromatin environment, and our understanding of this regulation is rapidly evolving. Recent work has shown that the chromatin environment of a locus is a central factor in transcriptional output. How long and short non-coding RNAs regulate the chromatin environment is thus an important question in transcriptional control.

Comprehensive characterization of small RNAs involved in establishment and maintenance of heterochromatin has been carried out. However, even though new sequencing technologies have revealed the big proportion of non-coding transcription, they failed to provide a thorough mechanistic understanding. The link between non-coding RNAs and chromatin regulation represents an important gap in our understanding of transcription. This link is not only interesting from a curiosity-driven scientific perspective but also to fully understand how to manipulate gene expression for human benefit, such as advancing in plant engineering approaches through development of transgenes with predictable expression over generations in variable field conditions.

 


Figure 7. Chromatin regulation by non-coding transcription remains an open question. The vast majority of eukaryotic transcription is known to be non-coding. Even if, as some people believes, a proportion is just noisy transcription, increasing evidence points to many biological roles for these non-coding RNAs. More specifically, how those molecules are processed during transcription (co-transcriptional processes) seem to be very relevant to define the chromatin environment.

 


FUNDING


Epigenetic regulation of fruit development and seed yield in Brassica oilseed crops. “Proyectos I+D+i Generación de Conocimiento 2021” grant PID2021-122241OB-I00 funded by MCIN/AEI/ 10.13039/501100011033 and by ERDF A way of making Europe. PI: Pedro Crevillén


Ayuda Ramón y Cajal 2021 grant RYC2021‐030895‐I funded by MCIN/AEI/ 10.13039/501100011033 and by European Union NextGenerationEU/PRTR. PI: Eduardo Mateo-Bonmatí


Effect of fluctuating temperatures on chromatin silencing and its impact on growth in Brassica crops. CBGP-CEPLAS International Collaborative Scientific Program (CSPINT). Severo Ochoa program grant CEX2020-000999-S funded by MCIN/AEI /10.13039/501100011033. PI: Pedro Crevillén

 

PUBLICATIONS

Full publication list of Pedro Crevillén and Eduardo-Mateo Bonmatí 


Relevant Publications

Mateo-Bonmatí, E., Montez, M., Maple, R., Fiedler, M., Fang, X., Saalbach, G., Passmore, L.A., Dean, C. 2024. A CPF-like phosphatase module links transcription termination to chromatin silencing. Molecular Cell. DOI: 10.1016/j.molcel.2024.05.016

 

Menon, G., Mateo-Bonmati, E., Reeck, S., Maple, R., Wu, Z., Ietswaart, R., Dean, C., Howard, M. 2024. Proximal termination generates a transcriptional state that determines the rate of establishment of Polycomb silencing. Molecular Cell. DOI: 10.1016/j.molcel.2024.05.014


Nielsen, M., Menon, G., Zhao, Y., Mateo-Bonmati, E., Wolff, P., Zhou, S., Howard, M., Dean, C. 2024. COOLAIR and PRC2 function in parallel to silence FLC during vernalization. Proceedings of the National Academy of Sciences 121, e2311474121. DOI: 10.1073/pnas.2311474121


Poza-Viejo, L., Payá-Milans, M., Martín-Uriz, P.S., Castro-Labrador, L., Lara-Astiaso, D., Wilkinson, M.D., Piñeiro, M., Jarillo, J.A., Crevillén, P. 2022. Conserved and distinct roles of H3K27me3 demethylases regulating flowering time in Brassica rapa. Plant, Cell & Environment n/a. DOI: 10.1111/pce.14258


Shukla, A., Pagán, I., Crevillén, P., Alonso-Blanco, C., García-Arenal, F. 2021. A role of flowering genes in the tolerance of Arabidopsis thaliana to cucumber mosaic virus. Molecular Plant Pathology. DOI: 10.1111/mpp.13151


Crevillén, P. 2020. Histone Demethylases as Counterbalance to H3K27me3 Silencing in Plants. iScience 23, 101715. DOI: 10.1016/j.isci.2020.101715


Payá-Milans, M., Poza-Viejo, L., Martín-Uriz, P.S., Lara-Astiaso, D., Wilkinson, M.D., Crevillén, P. 2019. Genome-wide analysis of the H3K27me3 epigenome and transcriptome in Brassica rapa. GigaScience 8. DOI: 10.1093/gigascience/giz147


del Olmo, I., Poza‐Viejo, L., Piñeiro, M., Jarillo, J.A., Crevillén, P. 2019. High ambient temperature leads to reduced FT expression and delayed flowering in Brassica rapa via a mechanism associated with H2A.Z dynamics. The Plant Journal. DOI: 10.1111/tpj.14446


Crevillén, P., Gómez‐Zambrano, Á., López, J.A., Vázquez, J., Piñeiro, M., Jarillo, J.A. 2019. Arabidopsis YAF9 histone readers modulate flowering time through NuA4-complex-dependent H4 and H2A.Z histone acetylation at FLC chromatin. New Phytologist. DOI: 10.1111/nph.15737


Huertas, R., Catalá, R., Jimenez-Gomez, J., Castellano, M.M., Crevillén, P., Piñeiro, M., Jarillo, J.A., Salinas, J. 2019. Arabidopsis SME1 regulates plant development and response to abiotic stress by determining spliceosome activity specificity. The Plant Cell tpc.00689.2018. DOI: 10.1105/tpc.18.00689


Gómez-Zambrano, Á; Crevillén, P; Franco-Zorrilla, JM; López, JA; Moreno-Romero, J; Roszak, P; Santos-González, J; Jurado, S; Vázquez, J; Köhler, C; Solano, R; Piñeiro, M; Jarillo, JA. 2018. "Arabidopsis SWC4 binds DNA and recruits the SWR1 complex to modulate histone H2A.Z deposition at key regulatory genes". Molecular Plant. DOI: 10.1016/j.molp.2018.03.014".


Crevillén, P; Yang, H; Cui, X; Greeff, C; Trick, M; Qiu, Q; Cao, X; Dean, C. 2014. "Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state". Nature. DOI: 10.1038/nature13722".


Crevillén, P; Sonmez, C; Wu, Z; Dean, C. 2013. "A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization". EMBO Journal. DOI: 10.1038/emboj.2012.324".


Castrillo, G; Sánchez-Bermejo, E; de Lorenzo, L; Crevillén, P; Fraile-Escanciano, A; TC, M; Mouriz, A; Catarecha, P; Sobrino-Plata, J; Olsson, S; Leo Del Puerto, Y; Mateos, I; Rojo, E; Hernández, LE; Jarillo, JA; Piñeiro, M; Paz-Ares, J; Leyva, A. 2013. "WRKY6 transcription factor restricts arsenate uptake and transposon activation in Arabidopsis". Plant Cell. DOI: tpc.113.114009 [pii] 10.1105/tpc.113.114009".