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How LEAFY makes flowers

Published on 15 January 2019

Flowers and flowering plants

In today's flora, flowering plants or angiosperms represent the vast majority of plant species but it has not always been the case. Plants started to grow on earth surface about 450 million years ago. At the beginning, there were only mosses, later followed by ferns and gymnosperms (such as Ginkgo biloba or coniferous trees): all these plant species reproduce without flowers. Flowering plants appeared only about 130 million years ago and but they quickly diversified to conquer most ecosystems. Thanks to the interaction with insects, flowers are an extremely efficient structure for reproduction, explaining the success of angiosperms in evolution.
The origin of flowering plants (how and where they appeared) and their rapid diversification intrigued Charles Darwin (who called it an “abominable mystery” and is still the focus of intense scientific investigation. In our lab., we study a protein called LEAFY (LFY) that acts as a master regulator of floral development in all angiosperms species and was already present in non flowering plants.
By analyzing this protein in many different plants species, we aim at better understand how it works at the molecular level and how it evolved and contributed to the origin of flowers.

From atomic to genomic resolution: studies on LEAFY structure, function and evolution

LEAFY is a special plant transcription factor (TF): it is present in all land plants, it does not resemble any other protein and did not form a multigene family like most other TF did. We still do not know where it comes from.

We use biochemical and structural analysis to characterize the properties of this interesting protein from various plants. In collaboration with the lab. of Dr. C. Müller, we have solved the crystallographic structure of Arabidopsis LFY DNA binding domain in complex with its cognate DNA. This work revealed that LFY possesses an Helix-Turn-Helix motif buried in a unique seven-helix fold that contacts DNA over a large region (19 pb).

Movie for LFY DNA binding:

Other videos of LEAFY.

3D pictures of LEAFY.

To understand how LFY targets the genes it regulates, we characterized and modeled its DNA binding specificity (Moyroud et al. 2011). Until now, LFY was considered to bind a poorly defined 7-bp consensus sequence. Based on biochemical experiments guided by the structural data, we have built a mathematical model describing LFY binding to DNA. This model predicts well DNA binding in Arabidopsis plants at the genomic level. We are developing several bioinformatics methods to apply this methodology to any transcription factor (See the Morpheus Web page).

The APETALA1 gene is regulated by LFY. The peaks correspond to the regions bound by LFY
in vivo (ChIP-seq experiment) and the bars show the LFY binding sites predicted by our model.

LFY builds the flower by regulating large sets of genes including the ABC and E homeotic regulators of floral organ identity. Genome scale experiments have identified thousands of other genes, bound and potentially regulated by LEAFY, including pathogen response, hormonal signaling and many other pathways. This work opened numerous novel avenues to understand the role of this fascinating protein.

Since LFY is present in all land plants (mostly as a single and easily recognizable copy), it provides a unique opportunity to study transcription factor evolution in the plant kingdom. We compare the biochemical properties of LEAFY proteins obtained from various plants such as grape wine, rice, Amborella trichopoda, Ginkgo biloba, Welwitschia mirabilis, Physcomitrella patens. We also try to understand the function of LFY in non flowering plants and aim at determining the origin of the regulatory network that today controls flower development in living angiosperms.

LEAFY orchestrates the regulatory network leading to the formation of flowers and to the expression of floral homeotic genes.

A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor

We discovered that the domain Nterminal of LEAFY is an oligomerization domain of the SAM type (Sterile Alpha Motif). Such domain is very common in other organisms but much less was known in plants. We have demonstrated it facilitated the binding of LEAFY in genome regions that do not necessarily possess very good affinity binding sites. More surprisingly, this domain also facilitated binding to closed regions of the genome suggesting that it confers LEAFY pioneer factor properties.
Sayou et al., Nature Communications.
Read the press release.
Judged Exceptional on F1000.

Selected recent publications

Sayou C, Nanao MH, Jamin M, Posé D, Thévenon E, Grégoire L, Tichtinsky G, Denay G, Ott F, Peirats Llobet M, Schmid M, Dumas R and Parcy F
A SAM oligomerization domain shapes the genomic binding landscape of the LEAFY transcription factor.
Nature Communications 2016, 7: 11222
Abstract - Reprint - Press release
3D pictures of LEAFY
Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF, Thévenon E, Chahtane H, Warthmann N, Melkonian M, Zhang Y, Wong GK, Weigel D, Parcy F and Dumas R
A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity
Science, 2014, 343(6171): 645-648
Abstract - Reprint - Press release

Videos of LEAFY
Benlloch R, Kim MC, Sayou C, Thévenon E, Parcy F and Nilsson O
Integrating long-day flowering signals: A LEAFY binding site is essential for proper photoperiodic activation of APETALA1.
Plant Journal, 2011, 67(6): 1094-1102
Moyroud E, Minguet EG, Ott F, Yant L, Posé D, Monniaux M, Blanchet S, Bastien O, Thévenon E, Weigel D, Schmid M and Parcy F
Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor.
Plant Cell, 2011, 23(4): 1293-1306
Moyroud E, Kusters E, Monniaux M, Koes R and Parcy F
LEAFY blossoms.
Trends in Plant Sciences, 2010, 15(6): 346-352

Moyroud E, Reymond MCA, Hamès C, Parcy F and Scutt CP
The Analysis of Entire Gene Promoters by Surface Plasmon Resonance.
Plant Journal, 2009, 59(5) : 851 – 858
Hamès C, Ptchelkine D, Grimm C, Thevenon E, Moyroud E, Gérard F, Martiel JL, Benlloch R, Parcy F, Müller CW
Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins.
The EMBO Journal, 2008, 27(19): 2628-2637