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Training in Systems Biology Applied to Flowering

Final Report Summary - SYSFLO (Training in Systems Biology Applied to Flowering)

SYSFLO: Training in Systems Biology Applied to Flowering

SYSFLO was a European Marie Curie Initial Training Network, running from December 2009 to November 2013, training 9 early stage researchers (ESRs) in systems biology, a form of interdisciplinary research linking the capture of large scale datasets to advanced computational analysis and modelling. This approach has a huge potential to take our understanding of biological systems forward from studying individual pathways to reveal the emergent properties of interconnected networks.

Although the systems approach is very widely applicable, SYSFLO focussed on applying it to advance our understanding of flowering, using the model plant Arabidopsis thaliana.

The formation of a flower is an exquisitely controlled process involving the change from vegetative to reproductive growth, followed by the correct development of all the floral organs: sepals, petals, stamens and carpel. Not only is the control of floral development an important biological question, but flowering and seed formation is of huge economic significance to the European Union, as it is vital to crop breeding and agricultural productivity.

Master genetic regulators act as switches, controlling the expression of different developmental pathways. At the start of SYSFLO, a good proportion of the master genetic regulators involved in flowering had been characterised in Arabidopsis, but there were still large gaps in our knowledge of what happened between these regulators and the outcome of their actions. SYSFLO aimed to address this gap.

Downstream targets of master gene regulators were investigated for all stages of flower development, from floral initiation, floral organ identity and organ growth to ovule development:

• Sandra Biewers separated the actions of floral identity genes SEPALLATA 1-4 (SEP1-4)
• Alice Pajoro identified targets of floral identity genes APETALA 1 (AP1) and SEP3, at different stages of flower development, and changes in chromatin accessibility.
• Marta Mendes explored targets of the ovule development gene SEEDSTICK (STK), in combination with SHATTERPROOF1-2 (SHP1-2) or SEP3.
• Aimone Porri investigated the flowering time regulator SHORT VEGETATIVE PHASE (SVP), its relationship with the plant hormone Gibberellin, and their effect on flowering time.
• Katharina Schiessl identified targets of the organ growth regulator, JAGGED (JAG).

Extracting meaningful results from the large-scale next generation sequencing data-sets created by such experimental work is dependent on the quality of the analysis and interpretation of the data. SYSFLO integrated experimental work with computational partners who focussed on improving bioinformatics techniques for data analysis and creating gene regulatory network models to elucidate the interplay of regulatory mechanisms.

• Miguel Godinho extended the Biobase product ExPlain to join it to Genehub (core biological data) and ExplainTree (user data management), and couple with PRI-CAT (ChIP-seq tool), allowing for better data handling and analysis.
• Pedro Madrigal developed more efficient algorithms for identification of candidate transcription-factor binding-sites in ChIP-seq data (released as open-access software NarrowPeaks) and protein binding footprints in DNase-seq data.
• Evangelia Dougali modelled gene networks to reveal underlying regulatory modules
• Felipe Leal Valentim developed techniques to predict protein-protein binding sites (released as open-access software SLIDERbio), and a model of flowering time regulation

Through the application of a systems biology approach to investigate all the different stages of flower development, from initiation to fertilisation, several strong themes have emerged.

While there are only a few key master gene regulators at the top of the cascade, changes in expression of these key genes result in changes in gene expression of tens to thousands of downstream genes, both direct and indirect targets. Even taking just the few regulatory genes studied as part of SYSFLO (AP1, SEP3, SEP4, STK, SVP and JAG), the enormity of the task ahead to identify all their direct targets and the targets’ actions is apparent.

In addition, many of the key regulators also act in concert with each other, forming multiple protein complexes that regulate different targets. For example, AP1 and SEP3 form a complex that targets genes involved in phyllotaxis, setting up the organ placement early in flower development, whereas SEP3 forms a separate complex with STK that controls the gene VERDANDI (VDD), which has an important and direct role in fertilisation as it is required for synergid degeneration and the consequent migration of the two sperm cells.

Furthermore, many of the key regulators, such as SEP1-4, AP1 and STK, act redundantly. These regulators were shown to have partly overlapping yet also distinctive sets of target genes, which may also change in a stage-specific fashion. It is suggested that this high level of redundancy may help to confer robustness to the system as well as helping integrate developmental and environmental cues.

Interactions of the genetic network with hormone signalling pathways will also need to form part of future work. It was shown here the plant hormone gibberellin (GA) acts above the floral transition promoter FT in leaf tissue, but downstream of FT in shoot apical meristem. In addition, PETAL LOSS, a direct target of JAG, is linked to changes in auxin signalling.

As highlighted above, the gene regulatory network linking master regulators to their outcome forms a system of such complexity that continued application and refinement of the systems biology approach will be essential to untangle the myriad of interactions. The time for simple diagrams has passed.

Further project and contact details can be found on our website at: http://www.sysflo.eu


COORDINATOR
Prof Brendan Davies, University of Leeds, UK.

PARTNERS
University of Leeds, UK. Prof Brendan Davies, ESR Sandra Biewers.

Plant Research International, Wageningen UR, Netherlands. Group a: Prof Gerco Angenent, ESR Alice Pajoro. Group b: Dr Aalt-Jan van Dijk, ESR Felipe Leal
Valentim

University of Milan, Italy. Prof Lucia Colombo, ESR Marta Mendes.

Max Planck Institute for Plant Breeding, Germany. Prof George Coupland, ESR Aimone Porri.

John Innes Centre, UK. Prof Robert Sablowski, ESR Katharina Schiessl.

BIOBASE, Germany. Dr Birgit Lewicki-Potapov, ESR Miguel Godinho.

Polish Academy of Sciences, Poland. Prof Pawel Krajewski. ESR Pedro Madrigal.

Vlaams Instituut voor Biotechnologie (VIB), Belgium. Prof Yves Van de Peer, ESR Evangelia Dougali.