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ten Tusscher, K. H.

Publications and source records attributed to ten Tusscher, K. H..

8 recordsLinked to original sources

A complex balance: PLETHORA - JANUS ratiometry explains the PLETHORA dosage regeneration paradox

Molecular gradients are classically thought to encode positional information through concentration thresholds, but how transcription factor dosage is translated into regenerative competence remains unclear. In Arabidopsis roots, PLETHORA (PLT) transcription factors form a gradient that defines a regeneration competence zone and, following injury, rapidly re-establishes their transcriptional domain through an auto-activation. Yet, increasing PLT levels has a paradoxical effect: moderate increases expand the competence zone, whereas further increases impair regeneration. Here, combining mathematical modelling with experiments, we uncover the molecular basis of this non-monotonic response. Our model reveals that PLT activity depends not simply on its abundance, but on the balance between PLT protein complexes and unbound PLT. Following injury, PLT auto-activation rapidly restores the transcriptional domain, whereas increasing PLT dosage progressively shifts the equilibrium towards unbound PLT, reducing the availability of active PLT complexes. We identify and experimentally validate a strategy to extend regeneration competence by maintaining an appropriate ratio of PLT complexes to unbound PLT. Our findings reveal a ratiometric mechanism for decoding transcription factor dosage, in which excess regulator can attenuate rather than enhance activity. Such molecular balancing provides a mechanism by which a single transcription factor gradient can generate distinct, context-dependent outcomes during development and regeneration.

developmental biology↗

The (un)likelihood of clock-driven lateral root priming; A modeling exploration

Lateral root formation starts with priming, predisposing subsets of pericycle cells with the potential of future lateral root formation through semi-periodic elevations in auxin (signalling). While various mechanisms have been suggested, the most broadly accepted hypothesis proposes a genetic, cell-autonomous root clock akin to the clock underlying vertebrate somitogenesis. Still, while gene expression variations were observed, so far this clock has not been proven. From a functional and evolutionary perceptive it is furthermore an open question whether lateral root priming is not more likely to arise from an emergent tissue level process similar to phyllotaxis. To help settle this debate in this study I use general knowledge of oscillator dynamics and simple models of auxin signalling to underline the unlikelihood of a root clock driving lateral root priming. I show how within a single cell oscillations are limited to a small parameter domain, with constraints intensifying due to the presence of multiple AUX/IAA and ARF types. Furthermore, I demonstrate how non-meristem based oscillations, due to a lack of memory of oscillator phase, can not drive periodic prebranch site formation.

developmental biology↗

Ensuring Robustness in Scientific Research, Split-root assays as an example case

Scientific progress relies on reproducibility, replicability, and robustness of research outcomes. After briefly discussing these terms and their significance for reliable scientific discovery, we argue for the importance of investigating robustness of outcomes to experimental protocol variations. We highlight challenges in achieving robust, replicable results in multi-step plant science experiments, using split-root assays in Arabidopsis thaliana as a case study. These experiments are important for unraveling the contributions of local, systemic and long-distance signalling in plant responses and play a central role in nutrient foraging research. The complexity of these experiments allows for extensive variation in protocols. We investigate what variations do or do not result in similar results and provide concrete recommendations for enhancing replicability and robustness of these and other complex experiments through extending the level of detail in research protocols.

plant biology↗

A coordinated switch in sucrose and callose metabolism enables enhanced symplastic unloading in potato tubers

One of the early changes upon tuber induction is the switch from apoplastic to symplastic unloading. Whether and how this change in unloading mode contributes to sink-strength has remained unclear. In addition, developing tubers also change from energy to storage-based sucrose metabolism. Here we investigated the coordination between changes in unloading mode and sucrose metabolism and their relative role in tuber sink strength by looking into callose and sucrose metabolism gene expression combined with a model of apoplastic and symplastic unloading. Decreased callose deposition in tubers is driven by decreased callose synthase activity. Furthermore, changes in callose metabolism and sucrose metabolism are strongly correlated, indicating a well-coordinated developmental switch. Modelling indicates that symplastic unloading is not the most efficient unloading mode per se. Instead, it is the concurrent metabolic switch that provides the physiological conditions necessary to potentiate symplastic transport and thereby enhance tuber sink strength.

plant biology↗

Identification of cambium stem cell factors and their positioning mechanism

Wood constitutes the majority of terrestrial biomass. Composed of xylem, it arises from one side of the vascular cambium, a bifacial stem cell niche that also produces phloem on the opposing side. It is currently unknown which molecular factors endow cambium stem cell identity. Here we show that TDIF ligand-activated PXY receptors promote the expression of CAMBIUM AINTEGUMENTA-LIKE (CAIL) transcription factors to define cambium stem cell identity in the Arabidopsis root. By sequestrating the phloem-originated TDIF, xylem-dependent PXY confines the TDIF signaling front, resulting in the activation of CAIL expression and stem cell identity in only a narrow domain. Our findings show how signals emanating from cells on opposing sides ensure robust yet dynamically adjustable positioning of a bifacial stem cell.

plant biology↗

Reverse engineering lateral root stable prebranch site formation; Complementary roles for auxin and auxin signalling

Priming is the process through which periodic elevations in auxin signalling prepattern future sites for lateral root formation, called prebranch sites. Thusfar is has remained a matter of debate to what extent elevations in auxin concentration and/or auxin signalling are critical for priming and prebranch site formation. Recently, we discovered a reflux-and-growth mechanism for priming generating periodic elevations in auxin concentration that subsequently dissipate. Here we reverse engineer a mechanism for prebranch site formation that translates these transient elevations into a persistent increase in auxin signalling, resolving the prior debate into a two-step process of auxin concentration mediated initial signal and auxin signalling capacity mediated memorization. A critical aspect of the prebranch site formation mechanism is its activation in response to time integrated rather than instantaneous auxin signalling. The proposed mechanism is demonstrated to be consistent with prebranch site auxin signalling dynamics, lateral inhibition and symmetry breaking mechanisms and perturbations in auxin homeostasis. Summary statementUsing computational modeling we reveal the likely complementary roles of auxin and auxin signalling in one of the earliest step in the formation of plant lateral roots, prebranch site formation.

developmental biology↗

Modeling of root nitrate responses suggests preferential foraging arises from the integration of demand, supply and local presence signals

A plants fitness to a large extent depends on its capacity to adapt to spatio-temporally varying environmental conditions. One such environmental condition to which plants display extensive phenotypic plasticity is soil nitrate levels and patterns. In response to heterogeneous nitrate distribution, plants show a preferential foraging response, enhancing root growth in high nitrate patches and repressing root growth in low nitrate locations beyond a level that can be explained from local nitrate sensing. Although various molecular players involved in this preferential foraging behavior have been identified, how these together shape root system adaptation has remained unresolved. Here we use a simple modeling approach in which we incrementally incorporate the various known molecular pathways to investigate the combination of regulatory mechanisms that underly preferential root nitrate foraging. Our model suggests that instead of a thus far not discovered growth suppressing supply signal, growth reduction on the low nitrate side may simply arise from a reduced root foraging and increased competition for carbon. Additionally, our work suggests that the long distance CK signaling involved in root growth increase in high nitrate patches may represent a supply signal specifically functioning in modulating demand signaling strength. We illustrate how this integration of demand and supply signals prevents excessive preferential foraging under conditions in which demand is not met by sufficient supply and a more generic foraging in search of nitrate should be maintained.

plant biology↗

Lateral root priming synergystically arises from root growth and auxin transport dynamics

The root system is a major determinant of plant fitness. Its capacity to supply the plant with sufficient water and nutrients strongly depends on root system architecture, which arises from the repeated branching off of lateral roots. A critical first step in lateral root formation is priming, which prepatterns sites competent of forming a lateral root. Priming is characterized by temporal oscillations in auxin, auxin signalling and gene expression in the root meristem, which through growth become transformed into a spatially repetitive pattern of competent sites. Previous studies have demonstrated the importance of auxin synthesis, transport and perception for the amplitude of these oscillations and their chances of producing an actual competent site. Additionally, repeated lateral root cap apoptosis was demonstrated to be strongly correlated with repetitive lateral root priming. Intriguingly, no single mutation has been identified that fully abolishes lateral root formation, and thusfar the mechanism underlying oscillations has remained unknown. In this study, we investigated the impact of auxin reflux loop properties combined with root growth dynamics on priming, using a computational approach. To this end we developed a novel multi-scale root model incorporating a realistic root tip architecture and reflux loop properties as well as root growth dynamics. Excitingly, in this model, repetitive auxin elevations automatically emerge. First, we show that root tip architecture and reflux loop properties result in an auxin loading zone at the start of the elongation zone, with preferential auxin loading in narrow vasculature cells. Second, we demonstrate how meristematic root growth dynamics causes regular alternations in the sizes of cells arriving at the elongation zone, which subsequently become amplified during cell expansion. These cell size differences translate into differences in cellular auxin loading potential. Combined, these properties result in temporal and spatial fluctuations in auxin levels in vasculature and pericycle cells. Our model predicts that temporal priming frequency predominantly depends on cell cycle duration, while cell cycle duration together with meristem size control lateral root spacing.

plant biology↗