June Bloom in Maratea Elaborate Mechanisms to Trigger Flowering at Reproducible Times of 1,2,3,4 5, the Growing Season in Response to Environmental Cues

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to cold (Bastow et al., 2004). In addition, plants have evolved June bloom in Maratea elaborate mechanisms to trigger flowering at reproducible times of 1,2,3,4 5, the growing season in response to environmental cues. Temperature François Parcy and Jan U. Lohmann * and day length appear to be the most relevant inputs for this behaviour, and work over recent decades has uncovered some of the Summary mechanisms that control how these inputs regulate flowering. These The International Workshop on Molecular Mechanisms studies have shown, for example, that the day-length response is Controlling Flower Development took place in the secluded mediated by circadian expression of CONSTANS (CO) mRNA, southern Italian village of Maratea in June 2011. This meeting, coupled to the light-dependent stabilisation of CO protein (Valverde which takes place biennially, gathers researchers in the fields of et al., 2004). This system ensures that CO mRNA coincides with flowering time and flower and fruit development from both light only under long days, leading to the long-day-specific Europe and overseas to enjoy the sun, the sea and, most stabilisation of CO. Light sensing, and thus day length detection, importantly, the science. As we summarise here, the results occurs in the leaves, whereas developmental decisions, such as floral presented at this workshop underlined how mechanistic studies induction, are undertaken by cells of the apical stem cell niche. Thus, of both model and diverse species are deepening our the information generated in the leaves must be transmitted over a understanding of the cellular processes involved in flowering. substantial distance, and this activity has been termed florigen. Genetics and genomics have shown that FLOWERING LOCUS T Key words: Evolution, Flower development, Flowering time, Fruit (FT) encodes a small mobile protein that carries out florigen development, Plant hormone, Transcriptional control function (Mathieu et al., 2007; Wigge et al., 2005). Interestingly, it has emerged that the CO transcription factor directly activates FT Introduction mRNA expression in leaves, while a number of floral repressors, The study of flowers, in particular how they develop and become including the transcription factors APETALA 2 (AP2), elaborated in diverse species, has attracted scientists for hundreds SCHNARCHZAPFEN (SNZ) and FLOWERING LOCUS M (FLM), of years. However, only in recent decades, since the advent of counteract this activity to balance inductive and repressive inputs genetics and molecular biology in model systems such as into FT gene activity (Yant et al., 2010). After translation, FT protein Arabidopsis, have we been able to take a quantum leap forward in moves via the phloem sap to the apex and, once unloaded from the understanding the molecular mechanisms underlying flowering. phloem, FT interacts with basic leucine zipper (bZIP) transcription Flower development can be broadly divided into several factors, including FLOWERING LOCUS D (FD), to act as a interconnected steps (Fig. 1): the repression of reproduction under transcriptional regulator that potently induces flower formation non-favourable conditions, the induction of flowering sensor (Wigge et al., 2005). pathways that integrate environmental and endogenous cues, the Once the floral inductive signals have overcome the repressive specification of floral identity to young stem cell centres by inputs, as described above, newly arising stem cell centres are meristem identity genes, and, finally, the elaboration and specified to become flowers by floral meristem identity genes such patterning of floral organs. The International Workshop on as LEAFY (LFY) and APETALA 1 (AP1) (reviewed by Liu et al., Molecular Mechanisms Controlling Flower Development, which 2009). The activity of these transcription factors is a prerequisite for took place in Maratea, Italy, earlier this year, provided researchers the formation of floral primordia and for the appropriate expression in this field with the opportunity to present their latest insights into of floral organ identity genes, which in turn take over the patterning the molecular mechanisms that control these important steps of of the emerging organs (reviewed by Lohmann and Weigel, 2002). flower development. The ABC model elegantly describes how floral organs are specified Since flowering represents sexual reproduction in plants, it is in a combinatorial fashion in which three overlapping genetic imperative that the pathways leading up to the generation of seeds activities specify the four distinct organ types that are arranged in are synchronised with both the growth status of the plant and its four concentric rings, termed whorls (Coen and Meyerowitz, 1991). external environment, in order to maximise the survival rate of The floral organ identity genes, which include the A-class genes offspring (reviewed by Amasino, 2010). One particularly important AP1 and AP2 required for sepal and petal development in whorls 1 external input that is connected to repression of flowering is winter and 2, respectively, the B-class genes AP3 and PISTILLATA (PI) that experience, or vernalisation, and many plants will not flower unless are responsible for specifying petal identity in whorl 2 and stamen they have experienced an extended exposure to cold. This behaviour identity in whorl 3, and the C-class gene AGAMOUS (AG), which is is driven by FLOWERING LOCUS C (FLC), which encodes a essential for stamen and carpel fate in whorls 3 and 4, respectively, potent transcription factor that represses the expression of floral are expressed in specific subdomains of the developing flower. With inducers and integrators and whose expression is reduced by a the exception of AP2, these regulators belong to the MCM1, polycomb-dependent epigenetic silencing mechanism in response AGAMOUS, DEFICIENS and SRF (MADS) domain family of transcription factors, and recent research has shown that these proteins act in higher-order complexes to direct target gene 1CEA, iRTSV, Laboratoire Physiologie Cellulaire et Végétale, F-38054 Grenoble, France. 2CNRS, UMR5168, F-38054 Grenoble, France. 3Université Joseph Fourier- expression and thus organ specification. Essential co-factors for the Grenoble I, UMR5168, F-38041 Grenoble, France. 4INRA, UMR1200, F-38054 formation of these complexes are the SEPALLATA (SEP) proteins, Grenoble, France. 5Centre for Organismal Studies, University of Heidelberg, 69121 which are also members of the MADS domain protein family and Heidelberg, Germany. which extend the ABC model to the ABCE model (reviewed by

*Author for correspondence ([email protected]) Gutierrez-Cortines and Davies, 2000). Once the basic floral pattern DEVELOPMENT 4336 MEETING REVIEW Development 138 (20)

Fig. 1. The regulatory steps of flower Environmental cues Endogenous cues e.g. light, day length, temperature development. Environmental and endogenous cues are detected by sensor pathways, which in turn act on floral pathway integrators (such as FT and FD). These then activate genes and proteins involved in specifying Sensor pathways Sensor pathways meristem identity (e.g. LFY, ABC genes, SEP proteins), eventually leading to floral and organ patterning. Hormones, such as auxin and jasmonic acid, can also Floral repressors, influence flowering in various ways. AP2, APETALA 2; Cold FLC Floral pathway integrators e.g. FT, FD e.g. AP2, SNZ, FLM FD, FLOWERING LOCUS D; FLC, FLOWERING LOCUS C; FLM, FLOWERING LOCUS M; FT, FLOWERING LOCUS T; LFY, LEAFY; SEP, SEPALLATA; SNZ, SCHNARCHZAPFEN. Meristem identity regulators e.g. LFY, ABC genes, SEP proteins

Flower Hormones development e.g. auxin, jasmonic acid

has been laid down by organ identity genes, organs are elaborated ‘winter beet’ that can be planted in the autumn without flowering the by intricate regulatory networks that involve plant hormones and next spring (Pin et al., 2010). In addition, Timo Hytönen (University other transcription factors (reviewed by Østergaard, 2009). of Helsinki, Finland) reported that the TERMINAL FLOWER 1 Although most of the mechanisms described above (as (TFL1) gene, which controls inflorescence architecture in summarised in Fig. 1) have been elucidated using the power of Arabidopsis and other species, appears to be a key regulator of genetics and molecular approaches in Arabidopsis, we are currently flowering in strawberry, thus explaining the major differences witnessing a trend to study these processes in diverse species that between seasonal and continuously flowering accessions. exhibit divergent flowering behaviours or morphologies, using the Several talks dealt with the evolution of inflorescence molecular knowledge established in model systems as a stepping- architecture. These included three presentations on plants that bear stone. The results presented at the Maratea meeting, which was an inflorescence called cyme, in which the primary meristem organised by Lucia Colombo and Martin Kater (University of Milan, terminates in a flower and growth continues due to a lateral structure Italy), mirrored this trend, but also underlined the importance of called the sympodial meristem. Ronald Koes (University of mechanistic studies of model systems for expanding and deepening Amsterdam, The Netherlands) and Claire Périlleux (University of our understanding of the cellular processes involved in flowering. Liège, Belgium) unravelled the central role of the Petunia EXTRA Several major themes emerged during course of the workshop, and, PETALS (EXP) and tomato JOINTLESS genes, two MADS domain in the following sections, we summarise the data that was presented family genes that prevent the sympodial meristem from acquiring relating to each of these themes. floral fate. Serena Della Pina (University of Amsterdam, The Netherlands) presented evidence to suggest that the differences in Evolution of regulatory networks the expression patterns observed between Arabidopsis and Petunia One exciting concept that emerged during the meeting was that for LFY and UNUSUAL FLORAL ORGANS (UFO) in Arabidopsis conserved regulatory networks have been rewired during evolution, and ABERRANT LEAF AND FLOWER (ALF) and DOUBLE TOP leading to differential responses to environmental cues in diverse (DOT) in Petunia are due to differences in cis-elements between species. Thus, despite the fact that the same regulators act on the UFO and DOT and to differences in trans factors acting on the LFY same biological process, the developmental outcome of a network and ALF promoters. can be modified during adaptation. In this context, Richard Several laboratories focusing on fruit development in Arabidopsis Macknight (University of Ontago, New Zealand) presented and rape seed presented their work on the evolution of regulatory collaborative work with Jim Weller (University of Tasmania, networks. Central regulators of Arabidopsis fruit development have Australia) showing that legumes have three distinct subclades of FT been isolated in genetic screens in the past, and recent work aimed genes. In the legume Medicago truncatula, these FT genes respond to link these regulators together. Monica Colombo from the differentially to day length and vernalisation, and the combined laboratory of Cristina Ferrandiz (University of Valencia, Spain) action of at least two of these FTs determines flowering time (Laurie showed that the formation of the apical part of the gynoecium, the et al., 2011). Studies presented by Ove Nilsson (Umeå Plant Science style, is dependent on a higher-order protein complex involving the Centre, Sweden) on the regulation of flowering time demonstrated NGATHA (NGA), STYLISH (STY) and YABBY (YAB) that, in sugar beet (Beta vulgaris), gene duplication has given rise to transcription factors (Trigueros et al., 2009). NGA factors are also two FT paralogues that have evolved antagonistic functions. One able to interact with other factors that play a role in apical gene (BvFT2) behaves as all previously described FT-like genes, gynoecium development, such as AINTEGUMENTA (ANT), activating flowering, whereas the other paralogue (BvFT1) is a suggesting that a combinatorial NGA complex code might dictate strong repressor of flowering. BvFT1 appears to have a central role tissue identity in the fruit. in the regulation of vernalisation in biennial sugar beet, and Work from Robert Sablowski and Lars Østergaard (John Innes overexpression of BvFT1 leads to non-flowering vernalisation- Centre, Norwich, UK) pinpointed a single nucleotide regulatory

insensitive plants that appear to fulfil all the requirements of a mutation in the REPLUMLESS (RPL) gene as the molecular origin DEVELOPMENT Development 138 (20) MEETING REVIEW 4337 of developmental variation in Brassicaceae seed dispersal (Arnaud regulators with SEP proteins in a tetrameric complexes (Honma and et al., 2011). An equivalent mutation in RPL has been selected to Goto, 2001; Theissen and Saedler, 2001). In addition to the limit seed dispersal during rice domestication (Konishi et al., 2006), interactions between MADS domain proteins, the Angenent suggesting that a common genetic toolkit regulates both laboratory discovered a number of other transcription factors and domestication and natural evolution, highlighting how plant chromatin-remodelling factors that are associated with the floral evolutionary developmental biology studies and breeding research MADS proteins, taking us a substantial step closer to understanding can inform each other. how the floral pattern is translated into organ specification. MADS domain transcription factors are represented by large and Transcription factor behaviour diverse gene families in all land plants, and floral patterning is not Since flowering is controlled largely by transcriptional mechanisms, their only role. Thus, several talks were devoted to functional the development of novel genome-wide techniques, such as analyses of MADS domain transcription factors in diverse species. chromatin immunoprecipitation-sequencing (ChIP-seq), has deeply The take-home message was that, despite the conserved role of this impacted work in this field. The laboratories of Gerco Angenent gene family in flower development, the number of genes in each (University of Wageningen, The Netherlands) and Markus Schmid subclade of the MADS domain family and the degree of (Max-Planck Institute for Developmental Biology, Tübingen, subfunctionalisation of these proteins differ greatly between species. Germany) presented genome-wide transcription factor binding Martin Kater (University of Milan, Italy) presented genetic profiles for several key regulators of flower development, including interactions between the four AG subfamily genes present in rice and the AP1, SEP3 and FLM MADS domain proteins, as well as AP2 showed that carpel identity was completely lost in an osmads3 and LFY (Moyroud et al., 2011; Yant et al., 2010; Kaufmann et al., osmads58 double-mutant stamen, similar to the carpel identity loss 2010; Kaufmann et al., 2009). These studies revealed a multitude of observed in the Arabidopsis ag mutant. Dabing Zhang’s group potential new direct targets for these factors and further work is now (Shanghai Jiao Tong University, China) identified several key floral needed to confirm their regulation and to study their function. organ regulators in the monocot rice, including the C-class gene Because ChIP-seq combined with expression studies usually yields OsMADS3 (Hu et al., 2011), the E-class gene OsMADS34 (Gao et a wealth of targets, the results of ChIP-seq studies of the al., 2010), an ancient AGAMOUS-LIKE 6 gene OsMADS6 (Li et al., FRUITFULL (FUL) MADS domain protein presented by Marian 2010) and the CYCLOIDEA-like homologue RETARDED PALEA 1. Bemer (University of Zurich, Switzerland) came as a surprise: very More recently, they have investigated the interactions between few of the potentially regulated genes were identified as direct OsMADS3, OsMADS13 (a D-class gene) and DROOPING LEAF targets using the ChIP-seq approach. Although FUL is known to (DL) during floral organ identity specification and floral meristem negatively regulate the valve margin identity genes determinacy (Li et al., 2011). Furthermore, the Zhang group showed SHATTERPROOF 1 and 2 (SHP1 and SHP2), INDEHISCENT that OsMADS6 is able to positively regulate the expression of B-, (IND) and ALCATRAZ (ALC), only SHP2 was identified as a direct C- and E-class floral patterning genes during early flower FUL target. development, and proposed a working model to explain the role of Genome-wide data are not only useful for compiling extensive floral homeotic genes in the specification of flower organ identity lists of target genes, but they can also be used to understand the rules and meristem determinacy in rice. governing DNA binding and transcriptional logic. To this end, Jose Teemu Teeri (University of Helsinki, Finland) showed that E- Muiño (University of Wageningen, The Netherlands) presented class floral patterning genes show a higher level of tools that allow multiple ChIP-seq datasets to be processed, analysed subfunctionalisation in Gerbera than in Arabidopsis, with individual and compared (Muiño et al., 2011). François Parcy (University genes specialised for either stamen development or carpel Joseph Fourier, Grenoble, France) also showed how, based on in development. Brendan Davies (University of Leeds, UK) showed vitro biochemical studies combined with ChIP-seq analysis, a how a single amino acid change in the K (keratin) domain of a biophysical model can be constructed to predict binding sites of the MADS box factor can modify the identity of its interacting partners, LFY master floral regulator (Moyroud et al., 2011). Such a tool can thereby explaining the functional difference between the efficiently track regulatory evolution based on the analysis of FARINELLI and PLENA proteins from Antirrhinum (Airoldi et al., primary genome sequence. 2010). Lucia Colombo (University of Milan, Italy) explained how Given their central roles in most steps of flower development, the SEEDSTICK (STK) MADS gene acts redundantly with the understanding the regulatory logic for complexes of MADS domain ARABIDOPSIS B-SISTER (ABS) gene in controlling several aspects transcription factors is a key issue. Günter Theissen and Rainer of ovule and seed development, demonstrating that MADS Melzer (University of Jena, Germany) along with Gerco Angenent regulators play essential roles in all steps of flower development, presented exciting results obtained by combining in vitro from the control of flowering time to the final stages of flower experiments and computational analyses of ChIP-seq data. They development. demonstrated that the DNA-binding ability of MADS complexes (dimer or tetramers) not only depends on DNA sequence but also on Integration of transcriptional and hormonal DNA shape, the orientation of binding sites, the distance between signals binding sites and even temperature (Melzer et al., 2009; Melzer and Another topic that emerged during the course of the workshop was Theissen, 2009). Along these lines, the existence of MADS protein the importance of interactions between local transcriptional tetramers in vitro and in vivo has been substantiated by data from networks and hormonal signals during the regulation of diverse the Angenent laboratory: using affinity purification and mass processes, ranging from stem cell regulation in the shoot apical spectrometry followed by bimolecular fluorescence meristem to patterning the fruit for seed dispersal. Jan Lohmann complementation (BiFC) validation, they showed that five major (University of Heidelberg, Germany) identified a basic helix-loop- floral homeotic MADS domain proteins (AP1, AP3, PI, AG and helix (bHLH) transcription factor as a direct transcriptional target of SEP3) interact in floral tissues as suggested in the ‘floral quartet’ the meristem regulator WUSCHEL (WUS) (Busch et al., 2010).

model, which predicts the interaction of floral homeotic ABC Interestingly, this factor is able to uncouple stem cell proliferation DEVELOPMENT 4338 MEETING REVIEW Development 138 (20) from the well-characterised WUSCHEL-CLAVATA system of Furthermore, this core genetic network underlying Arabidopsis fruit meristem maintenance (Brand et al., 2000; Schoof et al., 2000). development was shown to be conserved in Brassica, and this Gain- and loss-of-function studies highlighted both auxin-dependent knowledge is now being used to improve yield in oilseed rape. and -independent functions for this transcription factor, suggesting From these presentations, it is clear that the local modulation of that auxin could be directly involved in stem cell control (Zhao et hormone signalling represents a widely used regulatory regime. This al., 2010). Rüdiger Simon (University of Düsseldorf, Germany) would suggest that, in contrast to many animal systems, hormones presented new results on the control of KNOTTED1-LIKE primarily act as regional signals and thus represent efficient HOMEOBOX (KNOX) and of PIN-FORMED (PIN), which encodes morphogenetic executors. Furthermore, the presentations made it an auxin transporter, expression in Arabidopsis shoot meristems. clear that intricate feedback and feedforward loops operate in many Genetic analysis and direct molecular studies revealed that of the described signalling circuits. Thus, for a complete mechanistic LATERAL ORGAN BOUNDARY DOMAIN (LBD) proteins, a understanding of these regulatory events, mathematical modelling class of plant-specific transcription factors, interact with each other is likely to become even more important if we are to uncover the and form different heteromeric complexes that jointly act at the wiring and layouts of these complex networks. boundary region, a cleft that separates the meristem from laterally arising organs. Meristems that lack LBD protein activity, such as Imaging, morphodynamics and biophysical those present in jagged lateral organs mutants, fail to support further modelling organ growth and arrest activity at early stages. Moving on to floral Although transcription factors and hormones play key roles in meristems, David Smyth (Monash University, Melbourne, diverse processes during plant development, their activity alone is Australia) reported novel insights into petal emergence. He proposed not sufficient to define the shape of complex organs. Several an elegant mechanism by which the tri-helix transcription factor exciting talks addressed the issue of plant morphogenesis using PETAL LOSS (PTL) mediates growth suppression between sepals, advanced imaging and mathematical modelling. Robert Sablowski thus allowing auxin signalling from neighbouring cells to trigger demonstrated how quantitative three-dimensional analysis of cell petal outgrowth. Ptl enhancer screens identified the auxin geometry and DNA replication can be used to monitor how cell transporter AUX1, further substantiating the role of auxin during growth and the cell cycle are coupled in the meristem and in organ petal emergence. Once the petal has been specified, its growth and primordia, and how this coupling is modified by regulatory genes shape need to be defined. The group of Mohammed Bendahmane that affect organ growth. The presentation by Jan Traas (Ecole (Ecole Normale Supérieure, Lyon, France) demonstrated that the Normale Supérieure, Lyon, France) focused on the biophysical bHLH transcription factor BIG PETALp is involved in controlling properties of cells during the early stages of flower development. postmitotic cell expansion during petal development by functioning Using a combined imaging-modelling approach, he showed that the in the jasmonate pathway and through an interaction with AUXIN local modulation of cellular parameters, such as cell wall stiffness RESPONSE FACTOR 8 (Brioudes et al., 2009; Varaud et al., 2011). and anisotropy, can be sufficient to produce organ outgrowth. The intricate connection between hormone signalling and Zooming in on organogenesis during floral patterning, Susana transcriptional regulation became further apparent in talks that Sauret-Gueto (John Innes Centre, Norwich, UK) presented a focused on the development of reproductive organs. Maura quantitative staging system of petal development over time, which Cardarelli (Sapienza University of Rome, Italy) showed how auxin was used as a framework for extracting local growth parameters and jasmonic acid work hand in hand in late stamen development through clonal analysis. She used computational models of genetic (Cecchetti et al., 2008). She showed that auxin first controls the factors that locally control growth rate and the direction of growth timing of endothecium lignification, an early event of the anther through the establishment of an organ polarity field (Fig. 2). These opening process during which jasmonic acid has no role. Auxin then talks clearly showed that, despite the fact that Arabidopsis has been activates jasmonic acid biosynthesis, which in turn stimulates anther a major reference species for investigating plant development, many opening. Auxin is also essential for patterning the gynoecium and aspects of Arabidopsis morphogenesis are still poorly understood Eva Sundberg (University of Uppsala, Sweden) presented data on and poorly described. However, it is clear that the ever-improving the direct transcriptional regulation of the YUCCA class of auxin imaging techniques and the development of mathematical models to biosynthesis genes and other transcription factor genes by SHORT describe plant tissues at the biophysical level will open new avenues INTERNODES (SHI)/STY zinc-finger transcription factors (Eklund of research that will help to elucidate the mechanisms that regulate et al., 2010a). Interestingly, the regulatory interaction between plant morphogenesis. SHI/STY genes and auxin biosynthesis in Arabidopsis is conserved in moss, and SHI/STY expression overlaps with auxin responses in Data analysis and network reconstruction the moss Physcomitrella (Eklund et al., 2010b). Charles Gasser Throughout the meeting, it became clear that both the complexity of (University of California, Davis, USA) reported that, in the complex genetic, regulatory and biochemical interactions and the amount of regulatory network of ovule patterning, the KANADI transcription data derived from high-throughput and genome-wide approaches are factor ABERRANT TESTA SHAPE physically interacts with the increasing at exponential rates. Thus, the importance of systematic ETTIN auxin response factor and that both are essential for data handling, analysis and modelling of networks emerged as a integument growth. Thus, auxin appears to play a role not only in major theme of the meeting. Elena Alvarez-Buylla (University of ovule initiation, but also in later morphogenetic events. Even later Mexico City, Mexico) demonstrated that a complex mathematical in flower development, when the fruit is fine-patterned to allow seed model based on experimental data obtained from Arabidopsis can dispersal, localised hormonal activity is essential. The laboratory of be used not only to recapitulate flower development in this species, Lars Østergaard identified the IND and SPATULA (SPT) but also to predict the regulatory changes that underlie macro- transcription factors as key regulators of auxin transport in both early evolutionary modulations in flower morphology. As an example, she gynoecium development and later during fruit opening. This presented data on Lacandonia, a Mexican plant species that uniquely regulation occurs through direct interactions of IND and SPT with has male reproductive organs in the centre of the flower (Alvarez-

target genes involved in the control of polar auxin transport. Buylla et al., 2010). Focusing on data integration and analysis, Yves DEVELOPMENT Development 138 (20) MEETING REVIEW 4339

Acknowledgements We apologise to our colleagues whose work we could not describe owing to space constraints.

Funding Work in the F.P. laboratory is funded by ANR, CNRS, INRA and UJF and work in the J.U.L. laboratory is funded by HSFP, EMBO and the Max Planck Society.

Competing interests statement The authors declare no competing financial interests.

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