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Bishopp, A.

Publications and source records attributed to Bishopp, A..

7 recordsLinked to original sources

A general mathematical framework for modelling subnetworks of the nuclear auxin pathway

Auxins are a family of plant hormones involved in various processes across plant tissues and species. The Nuclear Auxin Pathway (NAP) consists of interacting transcription factors (ARFs) and repressors (Aux/IAAs), which govern an individual cell's response to changes in auxin concentration. These components are present in all land plants, and many species possess multiple copies of each signalling component. We present a general framework for ODE-based models of NAP submodules with the flexibility to model the promotion and repression of target genes by any combination of transcriptional regulators. We analyse published data and show that auxin treatment in Arabidopsis thaliana roots triggers a range of characteristically distinct temporal response profiles-for both target genes and the signalling components themselves. Using our modelling framework, we recapitulate aspects of this behaviour by presenting examples of real and theoretical NAP subnetworks, and by analysing the effect that these network dynamics have on auxin-mediated transcriptional responses. This work demonstrates the utility of our modelling framework as a general-purpose tool for understanding the function of certain protein-protein and protein-DNA interactions through their effects on the NAP. This exploration of the rich dynamics of more complex signalling pathways promises to advance our understanding of the NAP.

plant biology↗

Elucidating tissue and sub-cellular specificity of the entire SUMO network reveals how stress responses are fine-tuned in a eukaryote

SUMOylation is essential in plant and animal cells, but it remains unknown how SUMO components act in concert to modify specific targets in response to environmental stresses. In this study we characterise every SUMO component in the Arabidopsis root to create the first complete SUMO Cell Atlas in eukaryotes. This unique resource reveals wide spatial variation, where SUMO proteins and proteases have sub-functionalized in both their expression and subcellular localisation. During stress SUMO conjugation is mainly driven by tissue specific regulation of the SUMO E2 ligase. Stress-specific modulation of the SUMO pathway reveals unique combinations of Proteases being targeted for regulation in distinct root tissues by salt, osmotic and biotic signals. Our SUMO Cell Atlas resources reveal how this PTM influences cellular and tissue scale adaptations during root development and stress responses. We provide the first comprehensive study elucidating how multiple stress inputs can regulate an entire PTM system.

plant biology↗

The evolution of the duckweed ionome mirrors losses in structural complexity

Background and AimsThe duckweeds consist of 36 species exhibiting impressive phenotypic variation, including the progressive evolutionary loss of a fundamental plant organ, the root. Loss of roots and reduction of vascular tissues in recently derived taxa occur in concert with genome expansions of up to 14-fold. Given the paired loss of roots and reduction in structural complexity in derived taxa, we focus on the evolution of the ionome (whole-plant elemental contents) in the context of these fundamental body plan changes. We expect that progressive vestigiality and eventual loss of roots may have both adaptive and maladaptive consequences which are hitherto unknown. MethodsWe quantify the ionomes of 34 accessions in 21 species across all duckweed genera, spanning 70 million years in this rapid cycling plant (doubling times are as low as 24 hours). We relate both micro- and macroevolutionary ionome contrasts to body plan remodelling and show nimble microevolutionary shifts in elemental accumulation and exclusion in novel accessions. Key ResultsWe observe a robust directional trend in calcium and magnesium levels decreasing from the ancestral representative Spirodela genus towards the derived rootless Wolffia, with the latter also accumulating cadmium. We also identify abundant within-species variation and hyperaccumulators of specific elements, with this extensive variation at the fine- as opposed to broad-scale. ConclusionsThese data underscore the impact of root loss, and reveal the very fine scale of microevolutionary variation in hyperaccumulation and exclusion of a wide range of elements. Broadly, they may point to trade-offs not well recognized in ionomes.

plant biology↗

Fluctuations in auxin levels depend upon synchronicity of cell divisions in a one-dimensional model of auxin transport

Auxin is a well-studied plant hormone, the spatial distribution of which remains incompletely understood. Here, we investigate the effects of cell growth and divisions on the dynamics of auxin patterning, using a combination of mathematical modelling and experimental observations. In contrast to most prior work, models are not designed or tuned with the aim to produce a specific auxin pattern. Instead, we use well-established techniques from dynamical systems theory to uncover and classify ranges of auxin patterns as exhaustively as possible, as parameters are varied. Previous work using these techniques has shown how a multitude of stable auxin patterns may coexist, each attainable from a specific ensemble of initial conditions. When a key parameter spans a range of values, these steady patterns form a geometric curve with successive folds, often nicknamed a snaking diagram. As we introduce growth and cell divisions into a one-dimensional model of auxin distribution, we observe new behaviour which can be conveniently explained in terms of this diagram. Cell growth changes the shape of the snaking diagram, corresponding to deformations of auxin patterns. As divisions occur this can lead to abrupt creation or annihilation of auxin peaks. We term this phenomenon snake-jumping. Under rhythmic cell divisions, we show how this can lead to stable oscillations of auxin. However, we also show that this requires a high level of synchronisation between cell divisions. Using 18 hour time-lapse imaging of the auxin reporter DII:Venus in roots of Arabidopsis thaliana, we show auxin fluctuates greatly, both in terms of amplitude and periodicity, consistent with the snake-jumping events observed with non-synchronised cell divisions. Periodic signals downstream the auxin signalling pathway have previously been recorded in plant roots. The present work shows that auxin alone is unlikely to play the role of a pacemaker in this context. Author summaryAuxin is a crucial plant hormone, the function of which underpins almost every known plant development process. The complexity of its transport and signalling mechanisms, alongside the inability to image directly, make mathematical modelling an integral part of research on auxin. One particularly intriguing phenomenon is the experimental observation of oscillations downstream of auxin pathway, which serve as initiator for lateral organ formation. Existing literature, with the aid of modelling, has presented both auxin transport and signalling as potential drivers for these oscillations. In this study, we demonstrate how growth and cell divisions may trigger fluctuations of auxin with significant amplitude, which may lead to regular oscillations in situations where cell divisions are highly synchronised. More physiological conditions including variations in the timing of cell divisions lead to much less temporal regularity in auxin variations. Time-lapse microscope images confirm this lack of regularity of auxin fluctuations in the root apical meristem. Together our findings indicate that auxin changes are unlikely to be strictly periodic in tissues that do not undergo synchronous cell divisions and that other factors may have a robust ability to convert irregular auxin inputs into the periodic outputs underpinning root development.

plant biology↗

Duckweed roots are dispensable and are on a trajectory toward vestigiality

Duckweeds are morphologically simplified, free floating aquatic monocots comprising both rooted and rootless genera. This has led to the idea that roots in these species may be vestigial, but empirical evidence supporting this is lacking. Here we show that duckweed roots are no longer required for their ancestral role of nutrient uptake. Comparative analyses of nearly all rooted duckweed species revealed a highly reduced anatomy, with greater simplification in the more recently diverged genus Lemna. A series of root excision experiments demonstrated that roots are dispensable for normal growth in Spirodela polyrhiza and Lemna minor. Furthermore, ionomic analyses of fronds in these two species showed little difference in the elemental composition of plants in rooted versus root-excised samples. In comparison, another free-floating member of the Araceae, Pistia stratiotes, which colonized the aquatic environment independently of duckweeds, has retained a more complex root anatomy. Whilst Pistia roots were not absolutely required for growth, their removal inhibited plant growth and resulted in a broad change in the mineral profile of aerial tissues. Collectively, these observations suggest that duckweeds and Pistia may be different stages along a trajectory towards root vestigialization Given this, along with the striking diversity of root phenotypes, culminating in total loss in the most derived species, we propose that duckweed roots are a powerful system with which to understand organ loss and vestigiality. One sentence summaryThrough their adaption to the aquatic environment, duckweed roots have progressively become structurally reduced making them an ideal plant model with which to study vestigiality.

evolutionary biology↗

Auxin export from proximal fruits drives arrest in competent inflorescence meristems

A well-defined set of regulatory pathways control entry into the reproductive phase in flowering plants [1]. Conversely, little is known about the mechanisms that control the end of the reproductive phase ( floral arrest), despite this being a critical process for optimising fruit and seed production. Complete fruit removal or lack of fertile fruit-set in male sterile mutants, for example male sterile1 (ms1), prevents timely floral arrest in the model plant Arabidopsis [2]. These observations formed the basis for Hensel and colleagues model in which end-of-flowering was proposed to result from a cumulative fruit/seed-derived signal that caused simultaneous global proliferative arrest (GPA) in all inflorescences [2]. Recent studies have suggested that end-of-flowering involves gene expression changes at the floral meristem which are at least in part controlled by the FRUITFULL-APETELA2 pathway [3,4], however there is limited understanding of how this process is controlled and the communication needed at the whole plant level. Here, we provide new information providing a framework for the fruit-to-meristem (F-M) communication implied by the GPA model [5]. We show that floral arrest in Arabidopsis is not global and does not occur synchronously between branches, but rather that the arrest of each inflorescence is a local process, driven by auxin export from fruit proximal to the inflorescence meristem (IM). Furthermore, we show that inflorescence meristems are only competent for floral arrest once they reach a certain developmental age. Understanding the regulation of floral arrest is of major importance for the future manipulation of flowering to extend and maximise crop yields.

plant biology↗

A network of transcriptional repressors mediates auxin response specificity

INTRODUCTORY PARAGRAPHThe regulation of signalling capacity plays a pivotal role in setting developmental patterns in both plants and animals (1). The hormone auxin is a key signal for plant growth and development that acts through the AUXIN RESPONSE FACTOR (ARF) transcription factors (2). A subset of these ARFs comprises transcriptional activators of target genes in response to auxin, and are essential for regulating auxin signalling throughout the plant lifecycle (3). While ARF activators show tissue-specific expression patterns, it is unknown how their expression patterns are established. Chromatin modifications and accessibility studies revealed the chromatin of loci encoding ARF activators is constitutively open for transcription. Using a high-throughput yeast one-hybrid (Y1H) approach, we discovered a network of transcriptional regulators of ARF activator genes from Arabidopsis thaliana. Expression analyses demonstrated that the majority of these regulators act as repressors of ARF transcription in planta. Our observations support a scenario where the default configuration of open chromatin enables a network of transcriptional repressors to shape the expression pattern of ARF activators and provide specificity in auxin signalling output throughout development.

plant biology↗