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.
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: 57272read more
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.
Plant Cell (29) 1864-1882
Publisher's version: 10.1105/tpc.17.00389
ID: 57138read more
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.
Current opinion in genetics & development (45) 15-21
Publisher's version: 10.1016/j.gde.2017.02.005
ID: 55747read more
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.
Genes & Development (30) 2286-2296
Publisher's version: 10.1101/gad.285361.116
ID: 55277read more
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.
Development (143) 3394-3406
Publisher's version: 10.1242/dev.135327
ID: 55244read more
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.
Plant reproduction (DOI 10.1007/s00497-016-0278-6) 1-15
Publisher's version: 10.1007/s00497-016-0278-6
ID: 53378read more
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.
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: 52292read more
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.
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: 55375read more
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.
New Phytologist (207) 551558
Publisher's version: 10.1111/nph.13526
ID: 51448read more
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.
Dynamic control of auxin distribution imposes a bilateral-to-radial symmetry switch during gynoecium development
Current Biology (24) 2743-2748
Publisher's version: 10.1016/j.cub.2014.09.080
ID: 48624read more
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  and SPATULA  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.
Journal of Integrative Plant Biology (55) 847-63
Publisher's version: 10.1111/jipb.12092
ID: 47419read more
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.
Journal of Integrative Plant Biology
Publisher's version: 10.1111/jipb.12092
ID: 43438read more
Annual Review of Plant Biology (64) 219-41
Publisher's version: 10.1146/annurev-arplant-050312-120057
ID: 43522read more
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.
Plant Cell (24) 3982-3996
Publisher's version: 10.1105/tpc.112.103192
ID: 40992read more
Plant Cell (24) 2262-2278
Publisher's version: 10.1105/tpc.112.096677
ID: 40648read more
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: 39765read more
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: 39515read more
The same regulatory point mutation changed seed-dispersal structures in evolution and domestication.
Current Biology (21) 1215-9
Publisher's version: 10.1016/j.cub.2011.06.008
ID: 39282read more
Genes & Development (24) 2127-2132
Publisher's version: 10.1101/gad.593410
ID: 38011read more
Plant Journal (63) 329-338
Publisher's version: 10.1111/j.1365-313X.2010.04244.x
ID: 37505read more
A clade in the QUASIMODO2 family evolved with vascular plants and supports a role for cell wall composition in adaptation to environmental changes.
Plant Molecular Biology (73) 605-615
Publisher's version: 10.1007/s11103-010-9640-5
ID: 37468read more
BMC Plant Biology (10) 62
Publisher's version: 10.1186/1471-2229-10-62
ID: 37211read more
The Brassicaceae family includes the model plant Arabidopsis thaliana as well as a number of agronomically important species such as oilseed crops (in particular Brassica napus, B. juncea and B. rapa) and vegetables (eg. B. rapa and B. oleracea). Separated by only 10-20 million years, Brassica species and Arabidopsis thaliana are closely related, and it is expected that knowledge obtained relating to Arabidopsis growth and development can be translated into Brassicas for crop improvement. Moreover, certain aspects of plant development are sufficiently different between Brassica and Arabidopsis to warrant studies to be carried out directly in the crop species. However, mutating individual genes in the amphidiploid Brassicas such as B. napus and B. juncea may, on the other hand, not give rise to expected phenotypes as the genomes of these species can contain up to six orthologues per single-copy Arabidopsis gene. In order to elucidate and possibly exploit the function of redundant genes for oilseed rape crop improvement, it may therefore be more efficient to study the effects in one of the diploid Brassica species such as B. rapa. Moreover, the ongoing sequencing of the B. rapa genome makes this species a highly attractive model for Brassica research and genetic resource development.
Seeds from the diploid Brassica A genome species, B. rapa were treated with ethyl methane sulfonate (EMS) to produce a TILLING (Targeting Induced Local Lesions In Genomes) population for reverse genetics studies. We used the B. rapa genotype, R-o-18, which has a similar developmental ontogeny to an oilseed rape crop. Hence this resource is expected to be well suited for studying traits with relevance to yield and quality of oilseed rape. DNA was isolated from a total of 9,216 M2 plants and pooled to form the basis of the TILLING platform. Analysis of six genes revealed a high level of mutations with a density of about one per 60 kb. This analysis also demonstrated that screening a 1 kb amplicon in just one third of the population (3072 M2 plants) will provide an average of 68 mutations and a 97% probability of obtaining a stop-codon mutation resulting in a truncated protein. We furthermore calculated that each plant contains on average approximately 10,000 mutations and due to the large number of plants, it is predicted that mutations in approximately half of the GC base pairs in the genome exist within this population.
We have developed the first EMS TILLING resource in the diploid Brassica species, B. rapa. The mutation density in this population is approximately 1 per 60 kb, which makes it the most densely mutated diploid organism for which a TILLING population has been published. This resource is publicly available through the RevGenUK reverse genetics platform http://revgenuk.jic.ac.uk.