EPIGENETIC REGULATION OF AGRONOMIC TRAITS

Group leader: Pedro Crevillen Lomas - Researcher INIA
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Personnel:


Twitter @CrevillenLab

Epigenetics, the study of heritable changes in gene function that happens without DNA sequence change, is a relevant topic in Biology nowadays. Epigenetic mechanisms are crucial for the proper development of plants and it is now possible to exploit epigenetic variation to obtain novel crops varieties in a more rational and efficient way. We are developing a translational research program from the model plant Arabidopsis thaliana to Brassica crops species (Figure 1). To unravel the epigenetic basis of key agronomic traits we are using molecular genetic analyses together with state-of-the-art epigenomics approaches.

 

Figure 1. Translational research program from Arabidopsis to Brassica crops

 


RESEARCH LINES

Epigenetic regulation of flowering time

Flowering time is a developmental transition that has a direct impact on crop yield because it is crucial for the formation of fruit and seeds. Over the past decades, research in Arabdiopsis has shown that flowering time is regulated by a number of epigenetic mechanisms in response to endogenous and environmental cues. However, detailed characterization of flowering pathways and epigenetic phenomena in crop species is scarce. To address this issue, we are investigating flowering time in a Brassica rapa oilseed type cultivar by using a series of B. rapa tilling mutants in master floral regulators and epigenetic modifiers factors (Figure 2). Our work includes comprehensive flowering time phenotyping, molecular characterization of flowering time gene expression and genomics analyses.

 

Figure 2. B. rapa plants mutated in a floral promoting gene delay flowering time (A) whereas a mutation in a epigenetic modifier gene confers early flowering phenotype (B).

 


Response to environmental stimuli 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 plants regulate key developmental transitions in response to light and ambient temperature (Figure 3A). In addition, to flowering time we also are interested in other environmentally regulated developmental processes like seedling emergence (Figure 3B). This process is tightly regulated in response to light and temperature and it is a determinant of seed vigour, an important agronomic trait.

 

Figure 3. (A) B. rapa development of plants grown at 21 °C vs 28 °C ambient temperature. (B) B. rapa seedlings germinate differently in darkness or constant light.

 


Deciphering the plant epigenome


The study of the epigenome landscape and its relation with the underlying genome sequence in animal and plant cells has become a central question nowadays. The methylation of specific amino acid resides at histone tails is a conserved epigenetic mechanism involved in the regulation of fundamental processes like transcription or DNA replication. Nevertheless, epigenome studies in plant crops and its comparison with model plant systems is uncommon. In collaboration with the BIOLOGICAL INFORMATICS group we are investigating the lysine methylation epigenome in Arabidopsis and Brassica crops with an emphasis on the evolutionary relationships of epigenomic signatures. We are producing new state-of-the-art epigenome dataset and developing new computational methods to precisely infer different epigenetic states in plants (Figure 4). We will also study the evolutionary patterns of histone modifications that regulate gene expression and define novel epigenomic features. Being able to study the plant epigenome will help us to understand the complex gene regulatory processes that control plant development and are the basis for important crop traits.


 

Figure 4. H3K27me3 B. rapa epigenome. IGV browser snapshots of ChIP-seq signal across representative genes.

 

Mechanisms of virus-induced flowering time regulation

The transition from vegetative growth to reproduction is critical in plant life and determines plant fitness. Flowering time regulation has been much studied in Arabidopsis, however their regulation in response to pathogen infection has not been analysed, to our knowledge. In collaboration with the PLANT-VIRUS INTERACTION AND CO-EVOLUTION group, we are analysing the role of master floral regulators in plant-virus interactions. Our results contribute to understand the interaction between plant development and plant-pathogen interactions, a novel area of research that may become soon a hot topic.

FUNDING:

  1. PAPEL DE LOS MODIFICADORES EPIGENETICOS EN LA REPUESTA DE BRASSICACEAE A ESTIMULOS AMBIENTALES, Proyectos de I+D+i «RETOS INVESTIGACIÓN» 2018, (Agencia Estatal de Investigación RTI2018-097749-B-I00)
  2. Programa “Apoyo a Centros de Excelencia Severo Ochoa” al CBGP (UPM-INIA) (MINECO SEV2016-0672).
  3. REGULACION EPIGENETICA DEL TIEMPO DE FLORACION EN CULTIVOS OLEAGINOSOS DE BRASSICA Programa Estatal de I+D+i Orientada a los Retos de la Sociedad (MINECO BIO2015-68031-R).
  4. Ayuda Contrato Ramón y Cajal (MINECO RYC-2103-14689)
  5. Control of flowering time by chromatin remodeling (European Commission, Marie Curie Actions—Intra-European Fellowship 298790 FP7-PEOPLE-2011-IEF)


Representative 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".