MOLECULAR BASES OF PLANT DEVELOPMENTAL PHASE TRANSITIONS

Group leader: Jose Antonio Jarillo Quiroga - Researcher INIA

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Group leader: Manuel Angel Piñeiro Galvín - Researcher INIA

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During their life cycle plants undergo a number of 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 the molecular mechanisms involved in the regulation of plant developmental transitions. In particular we are interested in phase transitions such as flowering and germination with adaptive value for plant species as well as a significant impact on crop yield.

The floral transition marks the opening of the reproductive development and the timing of this developmental switch is essential to determine the reproductive success of plant species. For that reason plants tune very precisely the time of flowering initiation in response to both endogenous and environmental factors, ensuring that the production of flowers and fruits take place under optimal conditions. Using the model plant species Arabidopsis thaliana, and related Brassicaceae species, we are focused on studying the mechanisms that work to repress flowering until plants reach a particular developmental stage or are under optimal environmental conditions.

 

In addition, we are analysing the molecular basis of germination repression during seed dormancy in Arabidopsis. As for the floral transition, germination is also under the control of both endogenous and environmental factors, ensuring that seed growth is restarted under optimal conditions for the survival of the organism. Dormancy, or the transitory inability of viable seeds to germinate under favourable conditions, is from that point of view a trait with a high adaptive value and relevance in cultivated species.

Relevant results

Chromatin remodeling plays a crucial role in the establishment and maintenance of specific gene expression patterns associated with plant developmental transitions. For that reason, one of our main interests is to understand how epigenetic changes participate in the regulation of floral initiation and germination, and how environmental changes influence the structural dynamics of chromatin and affect developmental gene expression patterns. To accomplish these tasks we are using a combination of genetic, molecular and functional genomics approaches directed to identify and characterise master genes and regulatory circuits involved in the control of these developmental processes.

During recent years our lab has got a deeper insight in the epigenetic mechanisms that participate in the regulation of the floral transition through the molecular and genetic characterization of several Arabidopsis mutations affecting subunits 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. We have characterized the EARLY IN SHORT DAYS 1 (ESD1) locus, encoding ACTIN-RELATED PROTEIN 6 (AtARP6), a nuclear protein similar to conventional actin, and also the AtSWC6 locus, that encodes a zinc finger- harboring protein. Both proteins are part of the SWR1 complex and mutations in the corresponding genes cause an acceleration of flowering. In addition, we are studying AtSWC4 and AtYAF9-like proteins, whose yeast orthologs are present in the SWR1 complex and are shared by the histone acetyl transferase complex NuA4, indicating a possible functional interplay between these two complexes. We have demonstrated that AtSWC4 and AtYAF9 control flowering time and other developmental responses.

 

Inappropriate flowering time in cultivated species results in negative impacts in crop yield. It is our interest to translate the knowledge gained in Arabidopsis to close relatives such as Brassica napus or B. rapa oilseed crops. We are deepening in the chromatin-mediated regulation of developmental traits affecting crop yield in Brassica crops through the functional characterization of homologues of NuA4 complex subunits and other chromatin remodelers like the histone H3 lysine 27 demethylase ELF6, a key epigenetic regulator of flowering time that is being characterized by Pedro Crevillén (RyC fellow in our group). In the context of SYBRACLIM (FACCE-JPI ERANET Climate Smart Agriculture project), we are also evaluating the impact of climate variability on developmental traits and its effect on yield stability in Brassica crops.

Hypothetical model for HOS1 function in the photoperiodic flowering control.

On the other hand, we have characterized a mutation affecting the Arabidopsis ESD7 gene encoding the catalytic subunit of DNA polymerase epsilon, AtPOL2a. Our studies show that ESD7 is required for the repression of master genes of flowering in Arabidopsis and that this DNA polymerase is involved in chromatin-mediated cellular memory. We are now exploring the possible interplay between the DNA replication machinery and different chromatin remodeling complexes in the repression of flowering through a mechanism involving epigenetic gene silencing.

esd7 mutants are early flowering and display pleiotropic alterations in vegetative and reproductive development.

We have also addressed the molecular characterization of other chromatin remodeling mechanisms required to repress master flowering genes. EBS gene is required to repress FT expression and prevent a premature initiation of flowering, and regulates other developmental processes. The EBS protein is related to chromatin remodeling factors and is part of a plant-specific family of transcriptional regulators.

EBS and SHL belong to a family of plant specific chromatin remodelling factors, and play partially redundant roles in the control of flowering time in Arabidopsis.

 

To better understand the function of these chromatin remodeling factors in plant development we are characterizing another member of this family in Arabidopsis, SHORT LIFE (SHL). As for EBS, SHL also has a role in the repression of flowering, and is required to repress the expression of the floral integrator SOC1, indicating that SHL and EBS have independent functions in the regulation of flowering time. Moreover, both EBS and SHL bind specific histone modifications and modulate the chromatin structure of target loci. In the context of a European Initial Training Network, we are currently using a multidisciplinary approach involving molecular and cell biology, informatics and mathematical modeling to understand how chromatin changes mediated by EBS influence the expression of flowering genes. Altogether, these results are contributing to increase our knowledge of the regulatory networks controlling floral initiation.

In addition to a role in the inhibition of flowering, EBS is also involved in the repression of germination during the period of seed dormancy. By means of transcriptomic analysis we have identified a number of master genes of germination that are misregulated in ebs mutants. This strategy is allowing us to unveil the role of this chromatin remodeling factor in seed dormancy control. In order to further explore the molecular mechanisms by which chromatin dynamics participates in the regulation of this process we are also investigating the interaction of EBS gene with other loci encoding chromatin remodeling factors that modulate seed dormancy.

Moreover, within a collaborative project focused on the functional characterization of Arabidopsis transcription factors, we have generated a collection of plants that conditionally overexpress 1000 of these transcriptional regulators. The lines generated have been screened in our laboratory for transcription factors involved in the regulation of flowering time and seed dormancy. Some of the transcription factors isolated for their involvement in the regulation of these developmental phases are currently being characterized in our laboratory.

Arabidopsis lines with reduced seed dormancy identified in our laboratory.

 
 

Representative Publications

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.

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.

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