Geometric cues forecast the switch from two- to three-dimensional growth in Physcomitrella patens
2020-12-3, Tang, Han, Duijts, Kilian, Bezanilla, Magdalena, Scheres, Ben, Vermeer, Joop, Willemsen, Viola
During 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.
Dynamic cytokinin signalling landscapes during lateral root formation in Arabidopsis
2021-10-20, Nenadić, Milica, Vermeer, Joop
By 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.
Plant Biology: Journey to the Center of the Casparian Strip
2020-10-19, Stöckle, Dorothee, Vermeer, Joop
Diffusion 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.
GDSL-domain proteins have key roles in suberin polymerization and degradation
2021-3-8, Ursache, Robertas, De Jesus Teixeira, Cristovão, Dénervaud Tendon, Valérie, Gully, Kay, De Bellis, Damien, Schmid-Siegert, Emanuel, Grube Andersen, Toni, Shekhar, Vinay, Calderon, Sandra, Pradervand, Sylvain, Nawrath, Christiane, Geldner, Niko, Vermeer, Joop
Plant 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.
Translating Ribosome Affinity Purification (TRAP) to Investigate Arabidopsis thaliana Root Development at a Cell Type-Specific Scale
2020-5-1, Thellmann, Martha, Grube Andersen, Toni, Vermeer, Joop
In this article, we give hands-on instructions to obtain translatome data from different Arabidopsis thaliana root cell types via the translating ribosome affinity purification (TRAP) method and consecutive optimized low-input library preparation. As starting material, we employ plant lines that express GFP-tagged ribosomal protein RPL18 in a cell type-specific manner by use of adequate promoters. Prior to immunopurification and RNA extraction, the tissue is snap frozen, which preserves tissue integrity and simultaneously allows execution of time series studies with high temporal resolution. Notably, cell wall structures remain intact, which is a major drawback in alternative procedures such as fluorescence-activated cell sorting-based approaches that rely on tissue protoplasting to isolate distinct cell populations. Additionally, no tissue fixation is necessary as in laser capture microdissection-based techniques, which allows high-quality RNA to be obtained. However, sampling from subpopulations of cells and only isolating polysome-associated RNA severely limits RNA yields. It is, therefore, necessary to apply sufficiently sensitive library preparation methods for successful data acquisition by RNA-seq. TRAP offers an ideal tool for plant research as many developmental processes involve cell wall-related and mechanical signaling pathways. The use of promoters to target specific cell populations is bridging the gap between organ and single-cell level that in turn suffer from little resolution or very high costs. Here, we apply TRAP to study cell-cell communication in lateral root formation.
Microtubule-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, Marc-Martin, Sophie, Bald, Lotte, Ursache, Robertas, Fujita, Satoshi, Maizel, Alexis, Vermeer, Joop
Precise 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.
Cytoskeleton Dynamics Are Necessary for Early Events of Lateral Root Initiation in Arabidopsis
2019-7-18, Vicles Barro, Amaya, Stöckle, Dorothee, Thellmann, Martha, Ruiz-Duarte, Paola, Bald, Lotte, Louveaux, Marion, von Born, Patrick, Denninger, Philipp, Goh, Tatsuaki, Fukaki, Hidehiro, Vermeer, Joop, Maizel, Alexis
How plant cells re-establish differential growth to initiate organs is poorly understood. Morphogenesis of lateral roots relies on the asymmetric cell division of initially symmetric founder cells. This division is preceded by the tightly controlled asymmetric radial expansion of these cells. The cellular mechanisms that license and ensure the coordination of these events are unknown. Here, we quantitatively analyze microtubule and F-actin dynamics during lateral root initiation. Using mutants and pharmacological and tissue-specific genetic perturbations, we show that dynamic reorganization of both microtubule and F-actin networks is necessary for the asymmetric expansion of the founder cells. This cytoskeleton remodeling intertwines with auxin signaling in the pericycle and endodermis in order for founder cells to acquire a basic polarity required for initiating lateral root development. Our results reveal the conservation of cell remodeling and polarization strategies between the Arabidopsis zygote and lateral root founder cells. We propose that coordinated, auxin-driven reorganization of the cytoskeleton licenses asymmetric cell growth and divisions during embryonic and post-embryonic organogenesis.
The role of plant root systems in evolutionary adaptation
2019, Vinay Shekhar, Dorothee Stӧckle, Martha Thellmann, Vermeer, Joop
Roots provide a means to plants for gathering belowground resources. They are plastic and can adapt to ever-changing environmental cues. The plasticity of the roots comes from their ability to branch out by developing lateral and/or adventitious roots. In this chapter, we make an attempt to document the diversity in plant root systems and understand their role in evolutionary adaptation. After a brief introduction to different root systems, such as homorhizic and allorhizic ones, the relationship of plant roots with their surroundings, i.e., the rhizosphere and its effect on adaptation, will be discussed. Despite the difficulty to conclusively construct a timeline of evolution of plant root systems, documented facts from previous publications are examined and an effort has been made to delve into how rooting structures in plants adapted to prevailing conditions by bringing about endogenous changes vis-à-vis evolutionary development and exogenous changes to their surroundings.
Pluripotent Pericycle Cells Trigger Different Growth Outputs by Integrating Developmental Cues into Distinct Regulatory Modules
2020-9-10, Xiao, Wei, Molina, David, Ripper, Dagmar, Vermeer, Joop, Ragni, Laura
During 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.