The John Innes Centre Publications Repository contains details of all publications resulting from our researchers.

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The creation of this publications repository was funded by BBSRC.

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Simonini S., Mas P. J., Mas C. M. V. S., Ostergaard L., Hart D. J. (2018)

Auxin sensing is a property of an unstructured domain in the Auxin Response Factor ETTIN of Arabidopsis thaliana.

Scientific reports (8) 13563

Publisher's version: 10.1038/s41598-018-31634-9

ID: 59740

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The plant hormone auxin regulates numerous aspects of the plant life cycle. Auxin signalling is mediated by auxin response factors (ARFs) that dimerise with modulating Aux/IAA repressors. ARF3 (ETTIN or ETT) is atypical as it does not interact with Aux/IAA repressors. It is proposed to be a non-canonical auxin sensor, regulating diverse functions essential for development. This sensing ability relies on a unique C-terminal ETT specific domain (ES domain). Alignments of ETT orthologues across the angiosperm phylum revealed that the length and sequence identities of ES domains are poorly conserved. Computational predictors suggested the ES domains to be intrinsically disordered, explaining their tolerance of insertions, deletions and mutations during evolution. Nevertheless, five highly conserved short linear motifs were identified suggesting functional significance. High-throughput library screening identified an almost full-length soluble ES domain that did not bind auxin directly, but exhibited a dose-dependent response in a yeast two-hybrid system against the Arabidopsis INDEHISCENT (IND) transcription factor. Circular dichroism confirmed the domain was disordered. The identification and purification of this domain opens the way to the future characterisation of the ETT auxin-sensing mechanism in planta and an improved understanding of auxin-mediated regulation.

Simonini S., Stephenson P., Ostergaard L. (2018)

A molecular framework controlling style morphology inBrassicaceae.

Development (Cambridge, England)

Publisher's version: 10.1242/dev.158105

ID: 58132

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Organ formation in multicellular organisms depends on the coordinated activities of regulatory components that integrate developmental and hormonal cues to control gene expression and mediate cell-type specification. For example, development of the Arabidopsis gynoecium is tightly controlled by distribution and synthesis of the plant hormone auxin. The function of several transcription factors (TFs) have been linked with auxin dynamics during gynoecium development; yet how their activities are coordinated is not known. Here we show that five such TFs function together to ensure polarity establishment at the gynoecium apex. The auxin response factor ETTIN (ETT) is a central component of this framework. Interaction of ETT with TF partners is sensitive to the presence of auxin and our results suggest that ETT forms part of a repressive gene-regulatory complex. We show that this function is conserved between members of theBrassicaceaefamily and that variation in an ETT subdomain affects interaction strengths and gynoecium morphology. These results suggest that variation in affinities between conserved TFs can lead to morphological differences and thus contribute to the evolution of diverse organ shapes.


Plants respond to diurnal and seasonal changes in temperature by reprogramming vital developmental pathways. Understanding the molecular mechanisms that define environmental modulation of plant growth and reproduction is critical in the context of climate change that threatens crop yield worldwide. Here, we report that elevated temperature accelerates fruit dehiscence in members of the Brassicaceae family including the model plant Arabidopsis thaliana and important crop species. Arabidopsis fruit development is controlled by a network of interacting regulatory genes. Among them, the INDEHISCENT (IND) gene is a key regulator of the valve-margin tissue that mediates fruit opening, hence facilitating fruit dehiscence. We demonstrated that the valve-margin development is accelerated at higher temperature and that IND is targeted for thermosensory control. Our results reveal that IND upregulation is facilitated via temperature-induced chromatin dynamics leading to accelerated valve-margin specification and dispersal of the seed. Specifically, we show that temperature-induced changes in IND expression are associated with thermosensory H2A.Z nucleosome dynamics. These findings establish a molecular framework connecting tissue identity with thermal sensing and set out directions for the production of temperature-resilient crops.

van der Knaap E., Ostergaard L. (2017)

Shaping a fruit: Developmental pathways that impact growth patterns.

Seminars in Cell and Developmental Biology (79) 27-36

Publisher's version: 10.1016/j.semcdb.2017.10.028

ID: 59191

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Angiosperms produce seeds as their progeny enclosed in maternally-derived structures called fruits. Evolutionarily, fruits have contributed enormously to the success of the Angiosperms phylum by providing protection and nutrition to the developing seeds, while ensuring the efficient dispersal upon maturity. Fruits vary massively in both size and shape and certain species have been targeted for domestication due to their nutritional value and delicious taste. Among the vast array of 3D fruit shapes that exist in nature, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. In this review, we discuss the latest results in identifying components that control fruit morphology and their effect on isotropic and anisotropic growth. Moreover, we will compare the current knowledge on the mechanisms that control fruit growth, size and shape between the domesticated Solanaceae species, tomato and members of the large family of Brassicaceae.

Deb J., Bland H., Ostergaard L. (2017)

Developmental cartography: coordination via hormonal and genetic interactions during gynoecium formation

Current Opinion in Plant Biology (41) 54-60

Publisher's version: 10.1016/j.pbi.2017.09.004

ID: 57272

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Development in multicellular organisms requires the establishment of tissue identity through polarity cues. The Arabidopsis gynoecium presents an excellent model to study this coordination, as it comprises a complex tissue structure which is established through multiple polarity systems. The gynoecium is derived from the fusion of two carpels and forms in the centre of the flower. Many regulators of carpel development also have roles in leaf development, emphasizing the evolutionary origin of carpels as modified leaves. The gynoecium can therefore be considered as having evolved from a simple setup followed by adjustment in tissue polarity to facilitate efficient reproduction. Here, we discuss concepts to understand how hormonal and genetic systems interact to pattern the gynoecium.

Simonini S., Bencivenga S., Trick M., Østergaard L. (2017)

Auxin-Induced Modulation of ETTIN Activity Orchestrates Gene Expression in Arabidopsis.

Plant Cell (29) 1864-1882

Publisher's version: 10.1105/tpc.17.00389

ID: 57138

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The phytohormone auxin governs crucial developmental decisions throughout the plant life cycle. Auxin signaling is effectuated by auxin response factors (ARFs) whose activity is repressed by Aux/IAA proteins under low auxin levels, but relieved from repression when cellular auxin concentrations increase. ARF3/ETTIN (ETT) is a conserved noncanonical Arabidopsis thaliana ARF that adopts an alternative auxin-sensing mode of translating auxin levels into multiple transcriptional outcomes. However, a mechanistic model for how this auxin-dependent modulation of ETT activity regulates gene expression has not yet been elucidated. Here, we take a genome-wide approach to show how ETT controls developmental processes in the Arabidopsis shoot through its auxin-sensing property. Moreover, analysis of direct ETT targets suggests that ETT functions as a central node in coordinating auxin dynamics and plant development and reveals tight feedback regulation at both the transcriptional and protein-interaction levels. Finally, we present an example to demonstrate how auxin sensitivity of ETT-protein interactions can shape the composition of downstream transcriptomes to ensure specific developmental outcomes. These results show that direct effects of auxin on protein factors, such as ETT-TF complexes, comprise an important part of auxin biology and likely contribute to the vast number of biological processes affected by this simple molecule.

Moubayidin L., Østergaard L. (2017)

Gynoecium formation: an intimate and complicated relationship.

Current opinion in genetics & development (45) 15-21

Publisher's version: 10.1016/j.gde.2017.02.005

ID: 55747

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Multicellular organisms rely on the activity of organs that develop to a specific size and shape and are patterned into particular tissues. One of the most complicated plant structures is the female reproductive organ, the gynoecium, which must integrate a range of developmental cues to ensure efficient reproduction. Here we review recent discoveries on gene networks and hormonal activities that are required to (1) control cell division, (2) pattern the gynoecium along polarity axes and (3) specify organ shape and seed dispersal. Comparisons are made to other plant organs to understand how a developmental programme, which is evolutionarily derived from the formation of leaves, has been recruited and modified to create a reproductive machinery that has allowed angiosperms to dominate the world.

Simonini S., Deb J., Moubayidin L., Stephenson P., Valluru M., Freire-Rios A., Sorefan K., Weijers D., Friml J., Ostergaard L. (2016)

A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis

Genes & Development (30) 2286-2296

Publisher's version: 10.1101/gad.285361.116

ID: 55277

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Tissue patterning in multicellular organisms is the output of precise spatio–temporal regulation of gene expression coupled with changes in hormone dynamics. In plants, the hormone auxin regulates growth and development at every stage of a plant’s life cycle. Auxin signaling occurs through binding of the auxin molecule to a TIR1/AFB F-box ubiquitin ligase, allowing interaction with Aux/IAA transcriptional repressor proteins. These are subsequently ubiquitinated and degraded via the 26S proteasome, leading to derepression of auxin response factors (ARFs). How auxin is able to elicit such a diverse range of developmental responses through a single signaling module has not yet
been resolved. Here we present an alternative auxin-sensing mechanism in which the ARF ARF3/ETTIN controls gene expression through interactions with process-specific transcription factors. This noncanonical hormone-sensing mechanism exhibits strong preference for the naturally occurring auxin indole 3-acetic acid (IAA) and is important for coordinating growth and patterning in diverse developmental contexts such as gynoecium morphogenesis, lateral root emergence, ovule development, and primary branch formation. Disrupting this IAA-sensing ability induces morphological aberrations with consequences for plant fitness. Therefore, our findings introduce a novel transcription factor-based mechanism of hormone perception in plants.

Eldridge T., Langowski L., Stacey N., Jantzen F., Moubayidin L., Sicard A., Southam P., Kennaway R., Lenhard M., Coen E. S., Ostergaard L. (2016)

Fruit shape diversity in the Brassicaceae is generated by varrying patterns of anisotropy

Development (143) 3394-3406

Publisher's version: 10.1242/dev.135327

ID: 55244

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Fruits exhibit a vast array of different 3D shapes, from simple spheres and cylinders to more complex curved forms; however, the mechanism by which growth is oriented and coordinated to generate this diversity of forms is unclear. Here, we compare the growth patterns and orientations for two very different fruit shapes in the Brassicaceae: the heart-shaped Capsella rubella silicle and the near-cylindrical Arabidopsis thaliana silique. We show, through a combination of clonal and morphological analyses, that the different shapes involve different patterns of anisotropic growth during three phases. These experimental data can be accounted for by a tissue-level model in which specified growth rates vary in space and time and are oriented by a proximodistal polarity field. The resulting tissue conflicts lead to deformation of the tissue as it grows. The model allows us to identify tissue-specific and temporally specific activities required to obtain the individual shapes. One such activity may be provided by the valve-identity gene FRUITFULL, which we show through comparative mutant analysis to modulate fruit shape during post-fertilisation growth of both species. Simple modulations of the model presented here can also broadly account for the variety of shapes in other Brassicaceae species, thus providing a simplified framework for fruit development and shape diversity.

Langowski L., Stacey N., Østergaard L. (2016)

Diversification of fruit shape in the Brassicaceae family.

Plant reproduction (DOI 10.1007/s00497-016-0278-6) 1-15

Publisher's version: 10.1007/s00497-016-0278-6

ID: 53378

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Diversity in fruit shape. Angiosperms (flowering plants) evolved during the Cretaceous Period more than 100 million years ago and quickly colonized all terrestrial habitats on the planet. A major reason for their success was the formation of fruits that would protect and nurture the developing seeds. Moreover, a massive range of diversity in fruit shape occurred during a relatively short time, which allowed for the development of ingenious ways of fertilization as well as strategies for efficient seed dispersal. The Brassicaceae family more than any exemplifies the diversity in fruit morphologies, thus providing an ideal group of plants to study how specific shapes are established. Although many genes controlling fruit patterning in the model plant Arabidopsis thaliana have been identified, the processes of carpel and fruit morphogenesis are still poorly understood. Moreover, Arabidopsis fruits are relatively simple in their structure and are therefore not ideally suited for analyzing processes of morphology determination without comparison to species with differently shaped fruits. Here, we review the diversity of fruit shape within the Brassicaceae family. As an example we describe the close relative of Arabidopsis, Capsella rubella that develops flat, heart-shaped fruits showing and highlighting its potential as a model system for research into organ shape. Recent progress in genomics including fast and cheap genome sequencing and annotation as well as development of mutant populations has opened entirely new and exciting possibilities of studying the mechanisms and processes underlying fruit formation in angiosperms.

Lawrenson T., Shorinola O., Stacey N., Li C., Ostergaard L., Patron N., Uauy C., Harwood W. (2015)

Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease.

Genome Biology (16) 258

Publisher's version: 10.1186/s13059-015-0826-7

ID: 52292

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Background The RNA-guided Cas9 system represents a flexible approach for genome editing in plants. This method can create specific mutations that knock-out or alter target gene function. It provides a valuable tool for plant research and offers opportunities for crop improvement. Results We investigated the use and target specificity requirements of RNA-guided Cas9 genome editing in barley (Hordeum vulgare) and Brassica oleracea by targeting multicopy genes. In barley, we targeted two copies of HvPM19 and observed Cas9-induced mutations in the first generation of 23% and 10% of the lines, respectively. In B. oleracea, targeting of BolC.GA4.a led to Cas9-induced mutations in 10% of first generation plants screened. In addition, a phenotypic screen identified T0 plants with the expected dwarf phenotype associated with knock-out of the target gene. In both barley and B. oleracea stable Cas9-induced mutations were transmitted to T2 plants independently of the T-DNA construct. We did observe off-target activity in both species, despite the presence of at least one mismatch between the single guide RNA and the non-target gene sequences. In barley, a transgene-free plant had concurrent mutations in the target and non-target copies of HvPM19. Conclusion We demonstrate the use of RNA-guided Cas9 to generate mutations in target genes of both barley and B. oleracea and show stable transmission of these mutations thus establishing the potential for rapid characterisation of gene function in these species. In addition, the off-target effects reported offer both potential difficulties and specific opportunities to target members of multigene families in crops.

Lawrenson T., Shorinola O., Stacey N., Li C., Ostergaard L., Patron N., Uauy C., Harwood W. (2015)

Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease.

Genome biology (16) 258

Publisher's version: 10.1186/s13059-015-0826-7

ID: 55375

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The RNA-guided Cas9 system represents a flexible approach for genome editing in plants. This method can create specific mutations that knock-out or alter target gene function. It provides a valuable tool for plant research and offers opportunities for crop improvement.

Moubayidin L., Østergaard L. (2015)

Symmetry matters.

New Phytologist (207) 551558

Publisher's version: 10.1111/nph.13526

ID: 51448

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I. II. III. IV. V. References SUMMARY: The development of multicellular organisms depends on correct establishment of symmetry both at the whole-body scale and within individual tissues and organs. Setting up planes of symmetry must rely on communication between cells that are located at a distance from each other within the organism, presumably via mobile morphogenic signals. Although symmetry in nature has fascinated scientists for centuries, it is only now that molecular data to unravel mechanisms of symmetry establishment are beginning to emerge. As an example we describe the genetic and hormonal interactions leading to an unusual bilateral-to-radial symmetry transition of an organ in order to promote reproduction.

Lawrenson T., Goldsack C., Ostergaard L., Hundleby P. A. C. (2015)

Brassica rapa

Publisher's version: 10.1007/978-1-4939-1658-0_1

ID: 48626

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Symmetry formation is a remarkable feature of biological life forms associated with evolutionary advantages and often with great beauty. Several examples exist in which organisms undergo a transition in symmetry during development [1-4]. Such transitions are almost exclusively in the direction from radial to bilateral symmetry [5-8]. Here we describe the dynamics of symmetry establishment during development of the Arabidopsis gynoecium. We show that the apical style region undergoes an unusual transition from a bilaterally symmetric stage engrained in the gynoecium due to its evolutionary origin to a radially symmetric structure. We also identify two transcription factors, INDEHISCENT [9] and SPATULA [10] that are both necessary and sufficient for the radialization process. Our work furthermore shows that these two transcription factors control style symmetry by directly regulating auxin distribution. Establishment of specific auxin-signaling foci and the subsequent development of a radially symmetric auxin ring at the style are required for the transition to radial symmetry, since genetic manipulations of auxin transport can either cause loss of radialization in a wild-type background or rescue mutants with radialization defects. While many examples have described how auxin provides polarity and specific identity to cells in a range of developmental contexts, our data presented here demonstrate that auxin can also be recruited to impose uniform identity to a group of cells that are otherwise differentially programmed.


In the past 20-30 years, developmental biologists have made tremendous progress in identifying genes required for the specification of individual cell types of an organ and in describing how they interact in genetic networks. In comparison, very little is known about the mechanisms that regulate tissue polarity and overall organ patterning. Gynoecia and fruits from members of the Brassicaceae family of flowering plants provide excellent model systems to study organ patterning and tissue specification because they become partitioned into distinct domains whose formation is determined by polarity establishment both at a cellular and whole tissue level. Interactions among key regulators of Arabidopsis gynoecium and fruit development have revealed a network of upstream transcription factor activities required for such tissue differentiation. Regulation of the plant hormone auxin is emerging as both an immediate downstream output and input of these activities, and here we aim to provide an overview of the current knowledge regarding the link between auxin and female reproductive development in plants. In this review, we will also demonstrate how available data can be exploited in a mathematical modeling approach to reveal and understand the feedback regulatory circuits that underpin the polarity establishment, necessary to guide auxin flows.

Grieneisen V. A., Marée A. F., Ostergaard L. (2013)

Juicy Stories on Female Reproductive Tissue Development: Coordinating the Hormone Flows.

Journal of Integrative Plant Biology

Publisher's version: 10.1111/jipb.12092

ID: 43438

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Seymour G. B., Østergaard L., Chapman N. H., Knapp S., Martin C. (2013)

Fruit development and ripening.

Annual Review of Plant Biology (64) 219-41

Publisher's version: 10.1146/annurev-arplant-050312-120057

ID: 43522

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Fruiting structures in the angiosperms range from completely dry to highly fleshy organs and provide many of our major crop products, including grains. In the model plant Arabidopsis, which has dry fruits, a high-level regulatory network of transcription factors controlling fruit development has been revealed. Studies on rare nonripening mutations in tomato, a model for fleshy fruits, have provided new insights into the networks responsible for the control of ripening. It is apparent that there are strong similarities between dry and fleshy fruits in the molecular circuits governing development and maturation. Translation of information from tomato to other fleshy-fruited species indicates that regulatory networks are conserved across a wide spectrum of angiosperm fruit morphologies. Fruits are an essential part of the human diet, and recent developments in the sequencing of angiosperm genomes have provided the foundation for a step change in crop improvement through the understanding and harnessing of genome-wide genetic and epigenetic variation.

Fuentes S., Ljung K., Sorefan K., Alvey E., Harberd N. P., Ostergaard L. (2012)

Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses

Plant Cell (24) 3982-3996

Publisher's version: 10.1105/tpc.112.103192

ID: 40992

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Marshall A., Aalen R. B., Audenaert D., Beeckman T., Broadley M. R., Butenko M. A., Caño-Delgado A. I., de Vries S., Dresselhaus T., Felix G., Graham N. S., Foulkes J., Granier C., Greb T., Grossniklaus U., Hammond J. P., Heidstra R., Hodgman C., Hothorn M., Inzé D., Ostergaard L., Russinova E., Simon R., Skirycz A., Stahl Y., Zipfel C., De Smet I. (2012)

Tackling drought stress: RECEPTOR-LIKE KINASES present new approaches

Plant Cell (24) 2262-2278

Publisher's version: 10.1105/tpc.112.096677

ID: 40648

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O Lochlainn S., Amoah S., Graham N. S., Alamer K., Rios J. J., Kurup S., Stoute A., Hammond J. P., Ostergaard L., King G. J., White P. J., Broadley M. R. (2011)

High Resolution Melt (HRM) analysis is an efficient tool to genotype EMS mutants in complex crop genomes.

Plant Methods (7) 43

Publisher's version: 10.1186/1746-4811-7-43

ID: 39765

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Girin T., Paicu T., Stephenson P., Fuentes S., Koerner E., O'Brien M., Sorefan K., Wood T. A., Balanzá V., Ferrándiz C., Smyth D. R., Ostergaard L. (2011)

INDEHISCENT and SPATULA interact to specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis

Plant Cell (23) 3641-3653

Publisher's version: 10.1105/tpc.111.090944

ID: 39515

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