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

The repository also includes Open Access publications, which can be identified by the icons found on search results.

 Green open access publications are marked by the PDF icon. Click on the publication title, or the PDF icon, and read a pre-print PDF version of the publication.  Gold open access publications have the gold open padlock icon. You can read the full version of these papers on the publishing journal’s website without a subscription. 

The creation of this publications repository was funded by BBSRC.

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Sanchez-Corrales Y. E., Hartley M., van Rooij J., Maree A. F. M., Grieneisen V. A. (2018)

Morphometrics of complex cell shapes: Lobe Contribution Elliptic Fourier Analysis (LOCO-EFA).

Development (Cambridge, England)

Publisher's version: 10.1242/dev.156778

ID: 58031

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Quantifying cell morphology is fundamental to the statistical study of cell populations, and can help unravel mechanisms underlying cell and tissue morphogenesis. Current methods, however, require extensive human intervention, are highly parameter sensitive, or produce metrics difficult to interpret biologically. We therefore developed a method, Lobe Contribution Elliptical Fourier Analysis (LOCO-EFA), which generates from digitalised 2D cell outlines meaningful descriptors that can be directly matched to morphological features. This is shown by studying well-defined geometric shapes as well as actual biological cells from plant and animal tissues. LOCO-EFA provides a tool to phenotype efficiently and objectively populations of cells, here demonstrated by applying it to the complex shaped pavement cells ofArabidopsis thalianawild type andspeechlessleaves, andDrosophilaamnioserosa cells. To validate our method's applicability on large populations, we analysed computer-generated tissues. By controllingin silicocell shape, we explored the potential impact of cell packing on individual cell shape, quantifying through LOCO-EFA deviations between the specified shape of single cells in isolation and the resultant shape when they interact within a confluent tissue.

Carter R., Sánchez-Corrales Y. E., Hartley M., Grieneisen V., Marée A. F. M. (2017)

Pavement cells and the topology puzzle.

Development (Cambridge, England) (144) 4386-4397

Publisher's version: 10.1242/dev.157073

ID: 58030

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D'Arcy Thompson emphasised the importance of surface tension as a potential driving force in establishing cell shape and topology within tissues. Leaf epidermal pavement cells grow into jigsaw-piece shapes, highly deviating from such classical forms. We investigate the topology of developing Arabidopsis leaves composed solely of pavement cells. Image analysis of around 50,000 cells reveals a clear and unique topological signature, deviating from previously studied epidermal tissues. This topological distribution is established early during leaf development, already before the typical pavement cell shapes emerge, with topological homeostasis maintained throughout growth and unaltered between division and maturation zones. Simulating graph models, we identify a heuristic cellular division rule that reproduces the observed topology. Our parsimonious model predicts how and when cells effectively place their division plane with respect to their neighbours. We verify the predicted dynamics through in vivo tracking of 800 mitotic events, and conclude that the distinct topology is not a direct consequence of the jigsaw piece-like shape of the cells, but rather owes itself to a strongly life history-driven process, with limited impact from cell-surface mechanics.

Mambro R. D., De Ruvo M., Pacifici E., Salvi E., Sozzani R., Benfey P. H., Busch W., Novak O., Ljung K., Di Paola L., Maree A. F. M., Costantino P., Grieneisen V. A., Sabatini S. (2017)

Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root.

Proceedings of the National Academy of Sciences of the United States of America (114) E7641-E7649

Publisher's version: 10.1073/pnas.1705833114

ID: 57043

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In multicellular organisms, a stringent control of the transition between cell division and differentiation is crucial for correct tissue and organ development. In the Arabidopsis root, the boundary between dividing and differentiating cells is positioned by the antagonistic interaction of the hormones auxin and cytokinin. Cytokinin affects polar auxin transport, but how this impacts the positional information required to establish this tissue boundary, is still unknown. By combining computational modeling with molecular genetics, we show that boundary formation is dependent on cytokinin's control on auxin polar transport and degradation. The regulation of both processes shapes the auxin profile in a well-defined auxin minimum. This auxin minimum positions the boundary between dividing and differentiating cells, acting as a trigger for this developmental transition, thus controlling meristem size.

Sotta N., Duncan S., Tanaka M., Sato T., Maree A. F. M., Fujiwara T., Grieneisen V. A. (2017)

Rapid transporter regulation prevents substrate flow traffic jams in boron transport.

eLife (6)

Publisher's version: 10.7554/eLife.27038

ID: 57042

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Nutrient uptake by roots often involves substrate-dependent regulated nutrient transporters. For robust uptake, the system requires a regulatory circuit within cells and a collective, coordinated behaviour across the tissue. A paradigm for such systems is boron uptake, known for its directional transport and homeostasis, as boron is essential for plant growth but toxic at high concentrations. In Arabidopsis thaliana, boron uptake occurs via diffusion facilitators (NIPs) and exporters (BORs), each presenting distinct polarity. Intriguingly, although boron soil concentrations are homogenous and stable, both transporters manifest strikingly swift boron-dependent regulation. Through mathematical modelling, we demonstrate that slower regulation of these transporters leads to physiologically detrimental oscillatory behaviour. Cells become periodically exposed to potentially cytotoxic boron levels, and nutrient throughput to the xylem becomes hampered. We conclude that, while maintaining homeostasis, swift transporter regulation within a polarised tissue context is critical to prevent intrinsic traffic-jam like behaviour of nutrient flow.

Grieneisen V., McCleery W. T., Radzman N. (2017)

Root branching plasticity: collective decision-making results from local and global signalling.

Current Opinion in Cell Biology (44) 51-58

Publisher's version: 10.1016/

ID: 55817

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Cells within tissues can be regarded as autonomous entities that respond to their local environment and to signals from neighbours. Coordination between cells is particularly important in plants, as the architecture of the plant adapts to environmental cues. To explain the architectural plasticity of the root, we propose to view it as a swarm of coupled multi-cellular structures, rhizomers, rather than a large set of autonomous cells. Each rhizomer contains a primed site with the potential to develop a single lateral root. Rhizomers are spaced through oscillatory genetic events that occur at the basal root tip. The decision whether or not to develop a lateral root primordium results from the interplay between local interactions of the rhizomer with its immediate environment, such as local nutrient availability, long-range interactions between the rhizomers and global cues, such as overall nutrient uptake. It can halt lateral root progression through its developmental stages, resulting in the observed complex root architecture.

el Showk S., Help-Rinta-Rahko H., Blomster T., Siligato R., Maree A. F. M., Mahonen A. P., Grieneisen V. A. (2015)

Parsimonious Model of Vascular Patterning Links Transverse Hormone Fluxes to Lateral Root Initiation: Auxin Leads the Way, while Cytokinin Levels Out.

PLoS Computational Biology (11) e1004450

Publisher's version: 10.1371/journal.pcbi.1004450

ID: 52019

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An auxin maximum is positioned along the xylem axis of the Arabidopsis root tip. The pattern depends on mutual feedback between auxin and cytokinins mediated by the PIN class of auxin efflux transporters and AHP6, an inhibitor of cytokinin signalling. This interaction has been proposed to regulate the size and the position of the hormones' respective signalling domains and specify distinct boundaries between them. To understand the dynamics of this regulatory network, we implemented a parsimonious computational model of auxin transport that considers hormonal regulation of the auxin transporters within a spatial context, explicitly taking into account cell shape and polarity and the presence of cell walls. Our analysis reveals that an informative spatial pattern in cytokinin levels generated by diffusion is a theoretically unlikely scenario. Furthermore, our model shows that such a pattern is not required for correct and robust auxin patterning. Instead, auxin-dependent modifications of cytokinin response, rather than variations in cytokinin levels, allow for the necessary feedbacks, which can amplify and stabilise the auxin maximum. Our simulations demonstrate the importance of hormonal regulation of auxin efflux for pattern robustness. While involvement of the PIN proteins in vascular patterning is well established, we predict and experimentally verify a role of AUX1 and LAX1/2 auxin influx transporters in this process. Furthermore, we show that polar localisation of PIN1 generates an auxin flux circuit that not only stabilises the accumulation of auxin within the xylem axis, but also provides a mechanism for auxin to accumulate specifically in the xylem-pole pericycle cells, an important early step in lateral root initiation. The model also revealed that pericycle cells on opposite xylem poles compete for auxin accumulation, consistent with the observation that lateral roots are not initiated opposite to each other.


Background: The biophysical characteristics of cells determinethe shape of individual cells and their packing within tissues. Cellscan form regular or irregular epithelial structures, round up andform clusters, or deform and attach to substrates. The acquired shapeof cells and tissues is a consequence of (i) internal cytoskeletalprocesses, such as actin polymerisation and cortical myosin contraction,(ii) adhesion molecules within the cell membrane that interact withsubstrates and neighbouring cells, and (iii) processes that regulatecell volume. Although these processes seem relatively simple, whencombined they unleash a rich variety of cellular behaviour that isnot readily understandable outside a theoretical framework.Results: Here we present a mathematical and computationalanalysis of a commonly used class of model formalisms that describecell surface mechanics using an energy-based approach. The analyticalstudy reveals the complete possible spectrum of single cell behaviourand tissue packing in both 2D and 3D, by taking the typical core elementsof cell surface mechanics into account: adhesion, cortical tensionand volume conservation. We show that from an energy-based description,forces and tensions can be derived, as well as the prediction of cellbehaviour and tissue packing, providing an intuitive and biologicallyrelevant mapping between modelling parameters and experiments. Thesepredictions are confirmed by the computational outcomes of cell-packinggeometries, both in a vertex-model and in 2D and 3D simulations ofthe Cellular Potts Model.Conclusions: The biological insights and qualitative cellularbehaviours agree with the this analytical study, even across differentmodel formalisms. This illustrates the generality of energy-basedapproaches for cell surface mechanics and highlights how meaningfuland quantitative comparisons between models can be established. Moreover,the mathematical analysis yields direct links between known biophysicalproperties and specific parameter settings within the Cellular PottsModel.


Boron, an essential micronutrient, is transported in roots of Arabidopsis thaliana mainly by two different types of transporters, BORs and NIPs (nodulin26-like intrinsic proteins). Both are plasma membrane localized, but have distinct transport properties and patterns of cell type-specific accumulation with different polar localizations, which are likely to affect boron distribution. Here, we used mathematical modeling and an experimental determination to address boron distributions in the root. A computational model of the root is created at the cellular level, describing the boron transporters as observed experimentally. Boron is allowed to diffuse into roots, in cells and cell walls, and to be transported over plasma membranes, reflecting the properties of the different transporters. The model predicts that a region around the quiescent center has a higher concentration of soluble boron than other portions. To evaluate this prediction experimentally, we determined the boron distribution in roots using laser ablation-inductivity coupled plasma-mass spectrometry. The analysis indicated that the boron concentration is highest near the tip and is lower in the more proximal region of the meristem zone, similar to the pattern of soluble boron distribution predicted by the model. Our model also predicts that upward boron flux does not continuously increase from the root tip toward the mature region, indicating that boron taken up in the root tip is not efficiently transported to shoots. This suggests that root tip-absorbed boron is probably used for local root growth, and that instead it is the more mature root regions which have a greater role in transporting boron toward the shoots.


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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Abley K., De Reuille P. B., Strutt D., Bangham A., Prusinkiewicz P., Maree A. F., Grieneisen V. A., Coen E. (2013)

An intracellular partitioning-based framework for tissue cell polarity in plants and animals.

Development (140) 2061-74

Publisher's version: 10.1242/dev.062984

ID: 41877

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Walther G. R., Marée A. F. M., Edelstein-Keshet L., Grieneisen V. A. (2012)

Deterministic versus stochastic cell polarisation through wave-pinning.

Bulletin of Mathematical Biology (74) 2570-99

Publisher's version: 10.1007/s11538-012-9766-5

ID: 41342

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Cruz-Ramírez A., Díaz-Triviño S., Blilou I., Grieneisen V. A., Sozzani R., Zamioudis C., Miskolczi P., Nieuwland J., Benjamins R., Dhonukshe P., Caballero-Pérez J., Horvath B., Long Y., Mähönen A. P., Zhang H., Xu J., Murray J. A., Benfey P. N., Bako L., Marée A. F. M., Scheres B. (2012)

A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division.

Cell (150) 1002-15

Publisher's version: 10.1016/j.cell.2012.07.017

ID: 41339

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Grieneisen V. A., Scheres B., Hogeweg P., Marée A. F. M. (2012)

Morphogengineering roots: comparing mechanisms of morphogen gradient formation.

BMC Systems Biology (6) 37

Publisher's version: 10.1186/1752-0509-6-37

ID: 41338

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