MOLECULAR BASES OF PLANT DEVELOPMENTAL PHASE TRANSITIONS


Group leader: Jose Antonio Jarillo Quiroga - Research Professor CSIC-INIA
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Group leader: Manuel Angel Piñeiro Galvín - Research Professor CSIC-INIA
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Personnel:

 

During their life cycle plants undergo different developmental phases, including embryonic, vegetative and reproductive development. These developmental stages are characterised by specific patterns of cellular differentiation. The switch from a developmental phase to the next is under the control of spatial and temporal patterns of gene expression, so that selective activation or silencing of genes directs plant development through different phase changes. Our group is focused on understanding different molecular mechanisms involved in the regulation of plant developmental transitions. In particular, we are interested in a couple of phase transitions: flowering and seed germination/seedling establishment, with adaptive value for plant species as well as a significant impact on crop yield.

 

Since epigenetic processes are key players in the regulation of plant development and chromatin represents the interphase mediating genome interaction with the environment, the characterization of chromatin-mediated regulatory processes represents a corner stone in our investigations. Our current research directions are devoted to dissect the role of chromatin remodeling in the regulation of plant development, focusing on the role of the histone acetyltransferase (HAT) complex NuA4 (NuA4-C) in the regulation of flowering time and other developmental processes in Arabidopsis like chloroplast biogenesis during the transition from heterotrophic to autotrophic growth (Gomez-Zambrano et al., 2018; Crevillen et al., 2019; Espinosa-Cores et al., 2020; Barrero-Gil et al., 2021; Barrero-Gil et al., 2022). Our results show that different NuA4-C subunits may perform distinct functions in the flowering response to environmental cues such as photoperiod or ambient temperature. Also, mutants affected in particular subunits of NuA4-C display specific phenotypic alterations regarding other developmental traits or environmental responses. We are focused on elucidating the molecular basis for specific responses of Piccolo NuA4-C subunits. Furthermore, we are expanding the characterization of the two Arabidopsis HAM homologs using genomic approaches to further delve into the role of the NuA4-C catalytic subunit in the control of plant development. Since HAM proteins are present in additional chromatin remodeling complexes, the comparative analysis with other subunits of this HAT complex will also shed light on NuA4-C-dependent and -independent roles of HAM proteins. Altogether, these analyses will enlighten the relevance of histone acetylation in the regulation of plant development. Furthermore, our recent work revealed a novel attenuation mechanism of stress responses during the flowering initiation mediated by the MRG subunits of NuA4-C (Barrero-Gil et al., 2021). Under our CEPEI´s CHROPTIPLANT initiative, we are further exploring the basis for this epigenetic switch likely involved in the optimization of plant reproduction and fitness at the expense of costly responses to environmental challenges.

 

In addition, with the goal of assisting the agrifood sector in developing crops better suited to withstand increasing environmental temperature, we are analyzing plant developmental responses to warm ambient temperature in Brassica crops. Our analyses have identified several differentially expressed genes in Brassica napus (oilseed rape, OSR) varieties displaying differential flowering responses to warmth (Abelenda et al., 2023). We are currently characterizing at the functional level factors that could mediate plant developmental responses to temperature through chromatin reorganization. In parallel, we are following similar approaches in the PRIMA´s project BrasExplor involving B. rapa (turnips) (Del Olmo et al., 2019) and B. oleracea (cabbage, cauliflower), focused on the wide exploration of genetic diversity in Brassica species for sustainable crop production. Finally, in the EpiSeedLink MSCA-Doctoral Network we are addressing at the molecular level the effects that the exposure of mother plants to warm ambient temperature has on the performance of OSR seeds during germination and seedling establishment, two key developmental stages influencing crop yield. Environmental conditions experienced by mother plants affect seed performance in the progeny, and chromatin remodeling processes are likely involved in this memory. We are interested in identifying molecular and epigenetic mechanisms underlying plant responses to temperature, with the overarching goal of contributing to enhance crop resilience to suboptimal environments.

 

Recent relevant results

The deposition of histone variant H2A.Z and histone acetylation mediate different aspects of chromatin function and modulate flowering responses in Arabidopsis


During recent years our lab has analyzed epigenetic mechanisms that participate in the regulation of the floral transition through the molecular and genetic characterization of several Arabidopsis subunits (ARP6, SWC6) of the plant SWR1 chromatin remodeling complex, which catalyzes the exchange of H2A histone by the H2A.Z variant and that regulates flowering time in plants (Jarillo & Piñeiro, 2015). In addition, we have studied AtSWC4 and AtYAF9-like proteins, whose yeast orthologues are present in the SWR1 complex and are shared by the HAT complex NuA4 (Espinosa-Cores et al., 2020), indicating a possible functional interplay between these two complexes. Remarkably, we have shown that SWC4 participates in the recruitment of the SWR1 complex and H2A.Z deposition to modulate gene expression through the specific binding to AT-rich elements in regulatory regions of target genes such as the floral integrator FT (Gómez-Zambrano et al., 2018). We have also demonstrated that Arabidopsis YAF9 histone readers modulate flowering time through NuA4-complex-dependent H4 and H2A.Z histone acetylation at FLC chromatin (Crevillen et al., 2019).


Functions of the putative NuA4 subunits in different plant biological responses.

 

 

A chromatin switch attenuates abiotic stress responses during the floral transition


While stress conditions are known to impact plant development, how developmental transitions influence plant responses to adverse conditions has not been addressed, and the molecular mechanisms underlying the integration of plant development with stress responses remain obscure. We have revealed a novel molecular mechanism of stress response attenuation during the onset of flowering in Arabidopsis (Barrero-Gil et al., 2021). This mechanism involves NuA4 proteins (MRGs) that bind methylated forms of histone H3 and function as a chromatin switch on the floral integrator gene SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) to coordinate flowering initiation with plant responsiveness to hostile environments. These chromatin proteins are required to directly activate SOC1 expression during flowering induction by promoting histone H4 acetylation. In turn, SOC1 represses a broad array of genes that mediate abiotic stress responses such as cold or drought tolerance. The results obtained indicate that during the transition from vegetative to reproductive growth, this epigenetic switch that acts on SOC1 constitutes a central hub in a mechanism that tunes down stress responses to enhance reproductive success and plant fitness at the expense of costly efforts for adaptation to challenging environments.


Hypothetical working model showing how MRG-mediated chromatin acetylation at the SOC1 locus 
coordinates the floral transition and abiotic stress responses

 

 

How chromatin contributes to make plants green: Unveiled a NuA4-mediated histone acetylation mechanism regulating Arabidopsis chloroplast biogenesis


Photomorphogenic changes encompass a wide range of responses including the differentiation of non-photosynthetic plastids into chloroplasts, a crucial step in the transition from heterotrophic to autotrophic growth in plants. This process is light-induced and relies on the orchestrated transcription of nuclear and plastid genes, enabling the effective assembly and regulation of the photosynthetic machinery. Our group has revealed a novel regulation level for this process by unveiling the involvement of chromatin remodelling in the nuclear control of plastid gene expression for proper chloroplast biogenesis and function (Barrero-Gil et al., 2022). The two Arabidopsis homologs of the yeast EPL1 protein, components of the NuA4 histone acetyltransferase complex, are essential for plastid transcription and correct chloroplast development and performance. We showed that EPL1 proteins are light-regulated and necessary for concerted expression of nuclear genes encoding most components of chloroplast transcriptional machinery, directly mediating H4K5ac deposition at these loci and promoting the expression of plastid genes required for chloroplast biogenesis. These data unveil a NuA4-mediated mechanism regulating chloroplast biogenesis that links the transcription of nuclear and plastid genomes during chloroplast development.


Working model of light-induction of chloroplast biogenesis showing how NuA4-C coordinates nuclear and plastid gene expression during this process by promoting H4 acetylation in the regulatory regions of genes that are crucial for plastid transcription.  

 

 

Securing yield stability of Brassica crops in changing climate conditions


Elevated growth temperatures associated with climate change impact growth and flowering time and affect crop productivity by increasing yield losses. Oilseed rape is a premium oilseed crop also threatened by growing ambient temperatures. To shed light on the oilseed rape vegetative to reproductive phase transition under warm temperatures, our group took advantage of the diverse flowering responses of oilseed rape spring cultivated varieties at different temperature regimes. The current model for flowering response to warm temperature in Arabidopsis hypothesizes that high-temperature induction of FT expression is caused by changes in chromatin accessibility after the eviction of H2A.Z-containing nucleosomes, although the exact mechanism is not well understood. Additionally, a working mechanism behind H2A.Z control of temperature-dependent flowering repression in Brassica rapa proposes that BraFT is repressed through H2A.Z accumulation under non-inductive high ambient temperature. Our results identified BnaFTA2 as a key candidate gene in temperature-dependent flowering control in oilseed rape. Furthermore, the variety displaying the earliest flowering time (Wesway), showed consistent differences in H2A.Z deposition in BnaFTA2 between 21ºC and 28ºC, in line with previous results in Arabidopsis and the observed flowering phenotype. However, we found no clear correlation between H2A.Z occupancy and BnaFTA2 repression in late flowering accessions under high-temperature, including the commonly used variety RV31. In addition, ChIP analysis in oilseed rape ARP6 RNAi silenced plants with low H2A.Z levels corroborates that BnaFTA2 expression is only slightly affected by the presence of this non-canonical histone. These observations led us to propose that high ambient temperature impacts oilseed rape flowering time through both H2A.Z-dependent and independent mechanisms. Our analyses will help to harness crop response mechanisms for improving adaptation under the current climatic scenario.


Flowering time characterisation of selected Brassica napus varieties.

 


Representative Publications

Falentin, C., Hadj-Arab, H., Aissiou, F., Bartoli, C., Bazan, G., Boudet, M., Bousset-Vaslin, L., Chouikhi, M., Coriton, O., Deniot, G., Carvalho, J.F. de, Gay, L., Geraci, A., Glory, P., Huteau, V., Ilahy, R., Ilardi, V., Jarillo, J.A., Meglic, V., Oddo, E., Pernas, M., Pineiro, M., Pipan, B., Rhim, T., Richer, V., Rizza, F., Ronfort, J., Rousseau-Gueutin, M., Schicchi, R., Sinkovic, L., Taburel, M., Terzi, V., Théréné, S., Tiret, M., Tlili, I., Wagner, M.-H., Badeck, F.W., Chèvre, A.-M. 2024. Combined cytogenetic and molecular methods for taxonomic verification and description of Brassica populations deriving from different origins. Genetic Resources 5, 61–71. DOI: 10.46265/genresj.RYAJ6068


Abelenda, J.A., Barrero-Gil, J. 2023. ABA signaling branches out: emerging ABA-related signaling functions in Solanum tuberosum. Journal of Experimental Botany 74, 6405–6408. DOI: 10.1093/jxb/erad395


Boter, M., Pozas, J., Jarillo, J.A., Piñeiro, M., Pernas, M. 2023. Brassica napus Roots Use Different Strategies to Respond to Warm Temperatures. International Journal of Molecular Sciences 24,1143. DOI: 10.3390/ijms24021143


Abelenda, J.A., Trabanco, N., Olmo, I. del, Pozas, J., Martín-Trillo, M. del M., Gómez-Garrido, J., Esteve-Codina, A., Pernas, M., Jarillo, J.A., Piñeiro, M. 2022. High ambient temperature impacts on flowering time in Brassica napus through both H2A.Z-dependent and independent mechanisms. Plant, Cell & Environment. DOI: 10.1111/pce.14526


Barrero-Gil, J., Bouza-Morcillo, L., Espinosa-Cores, L., Piñeiro, M., Jarillo, J.A. 2022. H4 acetylation by the NuA4 complex is required for plastid transcription and chloroplast biogenesis. Nature Plants 1–12. DOI: 10.1038/s41477-022-01229-4


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


Barrero-Gil, J., Mouriz, A., Piqueras, R., Salinas, J., Jarillo, J.A., Piñeiro, M. 2021. A MRG-operated chromatin switch at SOC1 attenuates abiotic stress responses during the floral transition. Plant Physiology. DOI: 10.1093/plphys/kiab275


Espinosa-Cores, L., Bouza-Morcillo, L., Barrero-Gil, J., Jiménez-Suárez, V., Lázaro, A., Piqueras, R., Jarillo, J.A., Piñeiro, M. 2020. Insights Into the Function of the NuA4 Complex in Plants. Frontiers in Plant Science 11, 125. DOI: 10.3389/fpls.2020.00125


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


Pérez-Martín, F; Yuste-Lisbona, FJ; Pineda, B; García-Sogo, B; del Olmo, I; Alché, JdD; Egea, I; Flores, FB; Piñeiro, M; Jarillo, JA; Angosto, T; Capel, J; Moreno, V; Lozano, R. 2018. "Developmental role of the tomato Mediator complex subunit MED18 in pollen ontogeny". Plant Journal. DOI: 10.1111/tpj.14031".


Jarillo, JA; Komar, DN; Piñeiro, M. 2018. "The use of the chromatin immunoprecipitation technique for in vivo identification of plant protein–DNA interactions", p. 323-334. In L. Oñate-Sánchez (ed.), Two-Hybrid Systems: Methods and Protocols. Springer New York, New York, NY. DOI: 10.1007/978-1-4939-7871-7_23".


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".


Díaz-Manzano, FE; Cabrera, J; Ripoll, J-J; del Olmo, I; Andrés, MF; Silva, AC; Barcala, M; Sánchez, M; Ruíz-Ferrer, V; de Almeida-Engler, J; Yanofsky, MF; Piñeiro, M; Jarillo, JA; Fenoll, C; Escobar, C. 2018. "A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (miRNA172/TOE1/FT) in the feeding sites induced by Meloidogyne javanica in Arabidopsis thaliana". New Phytologist. DOI: 10.1111/nph.14839".


Narro-Diego, L; López-González, L; Jarillo, JA; Piñeiro, M. 2017. "The PHD-containing protein EARLY BOLTING IN SHORT DAYS regulates seed dormancy in Arabidopsis". Plant, Cell & Environment. DOI: 10.1111/pce.13046".


Pedroza-Garcia, J-A; Mazubert, C; del Olmo, I; Bourge, M; Domenichini, S; Bounon, R; Tariq, Z; Delannoy, E; Piñeiro, M; Jarillo, JA; Bergounioux, C; Benhamed, M; Raynaud, C. 2017. "Function of the plant DNA Polymerase epsilon in replicative stress sensing, a genetic analysis". Plant Physiology. DOI: 10.1104/pp.17.00031".


Pedroza-Garcia, JA; Domenichini, S; Mazubert, C; Bourge, M; White, C; Hudik, E; Bounon, R; Tariq, Z; Delannoy, E; del Olmo, I; Piñeiro, M; Jarillo Quiroga, Jose A; Bergounioux, C; Benhamed, M; Raynaud, C. 2016. "Role of the Polymerase ϵ sub-unit DPB2 in DNA replication, cell cycle regulation and DNA damage response in Arabidopsis". Nucleic Acids Research. DOI: 10.1093/nar/gkw449".


Olmo, ID; López, JA; Vázquez, J; Raynaud, C; Piñeiro, M; Jarillo, JA. 2016. "Arabidopsis DNA polymerase epsilon recruits components of Polycomb repressor complex to mediate epigenetic gene silencing". Nucleic Acids Research. DOI: 10.1093/nar/gkw156".


Komar, DN; Mouriz, A; Jarillo, JA; Piñeiro, M. 2016. "Chromatin Immunoprecipitation Assay for the Identification of Arabidopsis Protein-DNA Interactions In Vivo". Journal of Visualized Experiments. DOI: 10.3791/53422".


Lazaro, A; Mouriz, A; Piñeiro, M; Jarillo, JA. 2015. "Red light-mediated degradation of CONSTANS by the E3 ubiquitin ligase HOS1 regulates photoperiodic flowering in Arabidopsis". Plant Cell. DOI: 10.1105/tpc.15.00529".


Jarillo, JA; Piñeiro, M. 2015. "H2A.Z mediates different aspects of chromatin function and modulates flowering responses in Arabidopsis". Plant Journal. DOI: 10.1111/tpj.12873".


Coego, A; Brizuela, E; Castillejo, P; Ruíz, S; Koncz, C; del Pozo, JC; Piñeiro, M; Jarillo, JA; Paz-Ares, J; León, J; Transplanta Consortium, T. 2014. "The TRANSPLANTA collection of Arabidopsis lines: a resource for functional analysis of transcription factors based on their conditional overexpression". Plant Journal. DOI: 10.1111/tpj.12443".


Jarillo, JA; Gaudin, V; Hennig, L; Köhler, C; Piñeiro, M. 2014. "Plant chromatin warms up in Madrid: Meeting summary of the 3rd European Workshop on Plant Chromatin 2013, Madrid, Spain". Epigenetics. DOI: 10.4161/epi.28094".


López-González, L; Mouriz, A; Narro-Diego, L; Bustos, R; Martínez-Zapater, JM; Jarillo, JA; Piñeiro, M. 2014. "Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHD-containing proteins". Plant Cell. DOI: 10.1105/tpc.114.130781".


Piñeiro, M; Jarillo, JA. 2013. "Ubiquitination in the control of photoperiodic flowering". Plant Science. DOI: S0168-9452(12)00216-6 [pii] 10.1016/j.plantsci.2012.10.005".


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".


Lazaro, A.; Valverde, F.; Pineiro, M.; Jarillo, J.A. 2012. The Arabidopsis E3 Ubiquitin Ligase HOS1 Negatively Regulates CONSTANS Abundance in the Photoperiodic Control of Flowering. Plant Cell 24:982-999.