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Vermeer, Joop
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Vermeer, Joop
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- PublicationAccès libreA tightly regulated auxin signaling landscape is requiredfor spatial accommodation of lateral roots in Arabidopsis(2025)
;Thai Bui ;Vinay Shekhar ;Kevin Bellande; In Arabidopsis thaliana, lateral root (LR) development requires spatial accommodation responses in overlying endodermal cells. This includes loss of cell volume whilst maintaining membrane integrity to allow the expansion of the underlying LR primordia(LRPs). These accommodation responses are regulated by auxin-mediated signaling, specifically through Aux/IAA proteins, involving IAA3/SHY2. Plants that express a stabilized version of SHY2 (shy2-2) in differentiated endodermal cells, CASP1pro::shy2-2 plants, fail to make LRs. Exogenous treatment with 1-naphthaleneacetic acid(NAA) was reported to partially restore LR formation in this spatial accommodation mutant. Using treatments with auxins having different transport properties, such asNAA, indole-3-acetic acid (IAA), and 2,4-dichlorophenoxyacetic acid (2,4-D), we assessed the ability of each auxin to rescue LR formation in CASP1 pro::shy2-2 roots. This revealed that IAA is the most effective in partially restoring LR development, NAA is effective in inducing LRPs but cannot maintain their canonical phenotype, whereas 2,4-D induces non-controlled cell divisions. In addition, we show that in CASP1pro::shy2-2 roots, AUX1 appears to be repressed in the zone where the oscillation of the auxin response has been described. Our study advances the understanding of auxin-regulated spatial accommodation mechanisms during LRP formation and highlights the complex interplay of auxin transport and signaling in bypassing the endodermal constraints. - PublicationAccès libreLateral root formation in "Arabidopsis thaliana" and "Brachypodium distachyon": comparison of spatial accommodating responsesRoots are essential for anchoring plants to the soil and for the uptake of water and nutrients. Root branching significantly enhances the morphological adaptability of the root system in response to various biotic and abiotic factorsDespite significant findings in recent decades within the LR context, there remain major questions about the role of the endodermis during the emergence of the LRP. Our research has identified two important groups of auxin-mediated enzymatic components (GDSL-type esterase/lipase proteins - GELPs) that regulate suberin polymerization and likely its degradation. Additionally, we have demonstrated that developmental plasticity of the endodermis is necessary for normal LR emergence. Higher order mutants, almost completely lacking suberization in the endodermis, were highly sensitive to stress conditions. The wild grass Brachypodium distachyon, with its small genome, short life cycle, and small stature, is suitable for genetic transformation and has been developed as a model organism for both laboratory and field studies. However, it presents considerable challenges for studying LRs in their early developmental stages. We adapted a clearing method that significantly reduces clearing time, is compatible with various fluorescence dyes, and allows deep imaging of early cell divisions in the LRP. Using this toolkit, we were able to systematically categorize each LRP stage similar to what is used in Arabidopsis. We also demonstrated that, unlike in Arabidopsis, in Brachypodium the endodermis reactivates the cell cycle during LR formation. Moreover, we could show that the LRP appears to modify its Casparian strips to allow the emergence of the new organ. Surprisingly, the auxin reporter DR5 was not detected in early stages of LR formation, which does not necessarily imply that auxin is not involved in the initiation steps since we observed expression of auxin transporters during LR initiation events. We employed a root tip excision (RTE) method to synchronize LR development in Brachypodium, revealing distinct responses between accessions Bd21 and Bd21-3. In the latter accession, LRs appeared to be delayed in their emergence towards the nutrient medium along the root axis compared to Bd21. Additionally, osmotic stresses and hormonal treatments significantly reduced LR number and size in Bd21-3. Histological analyses suggested that the observed challenges in LRP emergence could be caused by early lignification of the exodermis in Bd21-3, unlike Bd21, where a delayed lignification was associated with facilitated LRP emergence. Integrating RTE with RNA-seq analysis of selected time points revealed a rapid induction of genes with a predicted function in cell-wall modification following the synchronized LR formation. Further studies, such as single-cell sequencing, will be essential to investigate the genetic programs underlying cell wall remodelling during LRP emergence in Brachypodium. In conclusion, we believe that this thesis contributed to advance our understanding of LR development in a wild grass, particularly emphasizing the pivotal role of the endodermis and its interactions with hormonal pathways and suberin dynamics.
- PublicationAccès libreAn atlas of Brachypodium distachyon lateral root development(2024)
; ;Kevin Bellande ;Alja van der Schuren ;Devin O'Connor ;Christian S. HardtkeThe root system of plants is a vital part for successful development and adaptation to different soil types and environments. A major determinant of the shape of a plant root system is the formation of lateral roots, allowing for expansion of the root system. Arabidopsis thaliana, with its simple root anatomy, has been extensively studied to reveal the genetic program underlying root branching. However, to get a more general understanding of lateral root development, comparative studies in species with a more complex root anatomy are required. Here, by combining optimized clearing methods and histology, we describe an atlas of lateral root development in Brachypodium distachyon, a wild, temperate grass species. We show that lateral roots initiate from enlarged phloem pole pericycle cells and that the overlying endodermis reactivates its cell cycle and eventually forms the root cap. In addition, auxin signaling reported by the DR5 reporter was not detected in the phloem pole pericycle cells or young primordia. In contrast, auxin signaling was activated in the overlying cortical cell layers, including the exodermis. Thus, Brachypodium is a valuable model to investigate how signaling pathways and cellular responses have been repurposed to facilitate lateral root organogenesis. - PublicationAccès libreMicrotubule-based perception of mechanical conflicts controls plant organ morphogenesis(2022-2-9)
;Stöckle, Dorothee ;Reyes-Hernández, Blanca Jazmin ;Vicles Barro, Amaya ;Nenadić, Milica ;Winter, Zsofiá; ;Bald, Lotte ;Ursache, Robertas ;Fujita, Satoshi ;Maizel, AlexisPrecise coordination between cells and tissues is essential for differential growth in plants. During lateral root formation in Arabidopsis thaliana, the endodermis is actively remodeled to allow outgrowth of the new organ. Here, we show that microtubule arrays facing lateral root founder cells display a higher order compared to arrays on the opposite side of the same cell, and this asymmetry is required for endodermal remodeling and lateral root initiation. We identify that MICROTUBULE ASSOCIATED PROTEIN 70-5 (MAP70-5) is necessary for the establishment of this spatially defined microtubule organization and endodermis remodeling and thus contributes to lateral root morphogenesis. We propose that MAP70-5 and cortical microtubule arrays in the endodermis integrate the mechanical signals generated by lateral root outgrowth, facilitating the channeling of organogenesis. - PublicationAccès libreDynamic cytokinin signalling landscapes during lateral root formation in Arabidopsis(2021-10-20)
;Nenadić, MilicaBy forming lateral roots, plants expand their root systems to improve anchorage and absorb more water and nutrients from the soil. Each phase of this developmental process in Arabidopsis is tightly regulated by dynamic and continuous signalling of the phytohormones cytokinin and auxin. While the roles of auxin in lateral root organogenesis and spatial accommodation by overlying cell layers have been well studied, insights on the importance of cytokinin is still somewhat limited. Cytokinin is a negative regulator of lateral root formation with versatile modes of action being activated at different root developmental zones. Here, we review the latest progress made towards our understanding of these spatially separated mechanisms of cytokinin-mediated signalling that shape lateral root initiation, outgrowth and emergence and highlight some of the enticing open questions. - PublicationAccès libreGDSL-domain proteins have key roles in suberin polymerization and degradation(2021-3-8)
;Ursache, Robertas; ;Dénervaud Tendon, Valérie ;Gully, Kay ;De Bellis, Damien ;Schmid-Siegert, Emanuel ;Grube Andersen, Toni ;Shekhar, Vinay ;Calderon, Sandra ;Pradervand, Sylvain ;Nawrath, Christiane ;Geldner, NikoPlant roots acquire nutrients and water while managing interactions with the soil microbiota. The root endodermis provides an extracellular diffusion barrier through a network of lignified cell walls called Casparian strips, supported by subsequent formation of suberin lamellae. Whereas lignification is thought to be irreversible, suberin lamellae display plasticity, which is crucial for root adaptative responses. Although suberin is a major plant polymer, fundamental aspects of its biosynthesis and turnover have remained obscure. Plants shape their root system via lateral root formation, an auxin-induced process requiring local breaking and re-sealing of endodermal lignin and suberin barriers. Here, we show that differentiated endodermal cells have a specific, auxin-mediated transcriptional response dominated by cell wall remodelling genes. We identified two sets of auxin-regulated GDSL lipases. One is required for suberin synthesis, while the other can drive suberin degradation. These enzymes have key roles in suberization, driving root suberin plasticity. - PublicationAccès libreGeometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens(2020-12-3)
;Tang, Han ;Duijts, Kilian ;Bezanilla, Magdalena ;Scheres, Ben; Willemsen, ViolaDuring land colonization, plants acquired a range of body plan adaptations, of which the innovation of three-dimensional (3D) tissues increased organismal complexity and reproductivity. In the moss, Physcomitrella patens, a 3D leafy gametophore originates from filamentous cells that grow in a two-dimensional (2D) plane through a series of asymmetric cell divisions. Asymmetric cell divisions that coincide with different cell division planes and growth directions enable the developmental switch from 2D to 3D, but insights into the underlying mechanisms coordinating this switch are still incomplete. Using 2D and 3D imaging and image segmentation, we characterized two geometric cues, the width of the initial cell and the angle of the transition division plane, which sufficiently distinguished a gametophore initial cell from a branch initial cell. These identified cues were further confirmed in gametophore formation mutants. The identification of a fluorescent marker allowed us to successfully predict the gametophore initial cell with > 90% accuracy before morphological changes, supporting our hypothesis that, before the transition division, parental cells of the gametophore initials possess different properties from those of the branch initials. Our results suggest that the cell fate decision of the initial cell is determined in the parental cell, before the transition division. - PublicationRestriction temporairePlant Biology: Journey to the Center of the Casparian Strip(2020-10-19)
;Stöckle, DorotheeDiffusion barriers in roots play an important role in regulating the movement of compounds between the soil environment and the vasculature. A new study provides new mechanistic insights into how a pair of copperbinding proteins facilitate the formation of a lignified nanodomain within Casparian strips. - PublicationAccès librePluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules(2020-9-10)
;Xiao, Wei ;Molina, David ;Ripper, Dagmar; Ragni, LauraDuring post-embryonic development, the pericycle specifies the stem cells that give rise to both lateral roots (LRs) and the periderm, a suberized barrier that protects the plant against biotic and abiotic stresses. Comparable auxin-mediated signaling hubs regulate meristem establishment in many developmental contexts; however, it is unknown how specific outputs are achieved. Using the Arabidopsis root as a model, we show that while LR formation is the main auxin-induced program after de-etiolation, plants with age become competent to form a periderm in response to auxin. The establishment of the vascular cambium acts as the developmental switch required to trigger auxin-mediated periderm initiation. Moreover, distinct auxin signaling components and targets control LR versus periderm formation. Among the periderm-specific-promoting transcription factors, WUSCHEL-RELATED HOMEOBOX 4 (WOX4) and KNAT1/BREVIPEDICELLUS (BP) stand out as their specific overexpression in the periderm results in an increased number of periderm layers, a trait of agronomical importance in breeding programs targeting stress tolerance. These findings reveal that specificity in pericycle stem cell fate is achieved by the integration of developmental cues into distinct regulatory modules.