EPIGENETIC REGULATION OF AGRONOMIC TRAITS

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


Twitter @CrevillenLab



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

Epigenetic regulation of agronomic traits in response to environmental cues in Brassicaceae

Plants are able to track and measure a number of environmental cues. They regulate their growth and metabolism according to these conditions to adapt perfectly to an ever-changing environment. We are studying how epigenetic modifier factors regulate plant developmental transitions in response to light quality and ambient temperature. In particular, we study the role of histone demethylases on flowering time regulation, a crucial step for the production of seeds and fruits. We found conserved and novel roles for histone H3 trimethylation (H3K27me3) demethylases in B. rapa flowering time regulation. Our work emphasizes that the regulatory pathways defined in model plants are relevant, but we should build on top of this knowledge the specific mechanisms controlling development in crop plants.

 

Figure 2. braA.ref6 mutant lines are late flowering whereas braA.elf6 mutants are early flowering. A-B) Pictures of braA.ref6-1 (A) and braA.elf6-1 (B) mutant lines compared to wild-type (WT) plants grown under controlled-environment conditions. C) Representation of B. rapa FLC3 locus indicating the regions analyzed by ChIP-qPCR. D) H3K27me3 ChIP-qPCR data of FLC3 locus in WT, braA.ref6-1, braA.ref6-2, braA.elf6-1 and braA.elf6-2 leaves. E) Genomic viewer snapshot of H3K27me3 ChIP-seq data at FLC3 locus in WT, braA.ref6-1 and braA.elf6-1.

 


Deciphering the plant epigenome


Epigenome studies in plant crops and its comparison with model plant systems is scarce. The epigenome comprises alternative chromatin states that can impact gene activity. We are producing new state-of-the-art epigenome dataset and develop new computational methods to precisely infer different epigenetic states in plants. We have been pioneer studying the histone H3 trimethylation (H3K27me3) landscape in B. rapa and providing novel genomics datasets and bioinformatics analytical resources. Our work highlights the importance of H3K27me3 deposition in the regulation of developmental transitions in plants and leads the way to further epigenomic studies in the complex genome of Brassica crops.

 

Figure 3. ChIP-seq analysis of H3K27me3 regions in B. rapa leaves. A) Metagene plot of ChIP-seq signal over marked genes. B) Gene heat map of H3K27me3 marked genes, ordered by ChIP-seq signal density. C) IGV viewer snapshots showing the H3K27me3 ChIP-seq and 3’RNA-seq data of BraA.AG.a in B. rapa leaves and inflorescences.

 


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 4. 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:

  1. Epigenetic regulation of fruit development and seed yield in Brassica oilseed crops. Proyectos generación del conocimiento 2021, Agencia Estatal de Investigación, PID2021-122241OB-I00. PI: Pedro Crevillén
  2. Ayuda Ramón y Cajal RYC2021‐030895‐I, Agencia Estatal de Investigación. PI: Eduardo Mateo-Bonmatí


Relevant Publications

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".