bioRxiv Science⌕ Search

Biology subjects

Bovio, S.

Publications and source records attributed to Bovio, S..

9 recordsLinked to original sources

Interlayer Communication Integrates Genetic and Mechanical Signals for Robust Leaf Morphogenesis

Leaf development requires coordinated growth across distinct tissue layers, integrating genetic regulation with mechanical coupling to achieve proper organ shaping. However, the mechanisms coordinating differentiation and growth across layers to ensure coherent leaf morphogenesis remain poorly understood. Therefore, we investigated the role of TCP4 as a potential central regulator of interlayer communication coupling genetic and mechanical signals during Arabidopsis leaf development. Three-dimensional analyses revealed pronounced asymmetry in the expression of TCP4 and its negative regulator, MIR319C, across developing primordia, establishing spatially patterned differentiation cues. Tissue-specific perturbations demonstrated that TCP4 activity in either epidermis or subepidermis modulates cell proliferation and expansion across layers through both protein mobility and mobility-independent signalling mechanisms. Strong epidermal TCP4 induction arrested leaf development by prematurely suppressing proliferation and preventing symmetry breaking, thereby locking primordia in cylindrical states. Live imaging revealed fundamental reprogramming of growth anisotropy, with TCP4 driving cortical microtubule alignment, increasing cell wall stiffness, and establishing layer-specific pectin patterns. Together, these findings establish TCP4 as an integrator of genetic and mechanical signals across leaf tissue layers, coupling transcriptional programmes to cytoskeletal organisation, cell wall remodelling, and cross-layer mechanical feedback.

plant biology↗

Plant cells at the organ surface use mechanical cues to activate a specific growth control programme

During morphogenesis of multicellular organs, cells acquire distinct identities that meet specific functional requirements. Epidermal identity is widely considered essential for plant morphogenesis due to the role of the epidermis in both restricting and promoting growth. In the root, epidermal cells are partially covered by a protective root cap, and partially positioned at the organ surface. Here, we propose that epidermal cells at the organ surface have unique requirements for growth control due to high mechanical tension, while covered epidermal cells are mechanically shielded by the root cap. We present in silico and in vivo evidence that plants use surface mechanical cues to activate a cell-type specific growth control programme involving the small GTPase RAB-A5c, allowing them to maintain directional growth at the organ surface. Positional mechanical cues may thus be used to control expression of a sub-population of epidermal genes, linking gene regulation to surface-specific functional requirements.

plant biology↗

Root hair growth phases are coordinated by cytoskeleton, nucleus dynamics and cell mechanics in Arabidopsis

Polar cell growth is a fundamental process across organisms, yet its coordination with nuclear movement and cytoskeleton dynamics remains underexplored. Focusing on Arabidopsis thaliana root hairs, we investigate these processes using high-resolution live imaging within microfluidics-based experiments. By incorporating data on cytoskeletal dynamics, nuclear positioning, and tip growth into a mathematical model, we analyse how their interactions shape the different growth phases that we reveal for the first time in this study. Chemical treatments and mutant analyses further support our model, revealing that timely cytoskeletal changes drive transitions between these growth phases, and correlate with shifts in nuclear movement and morphology. This regulation suggests a microtubule-actin crosstalk in the root hair subapical region. Additionally, we present novel findings on vacuole movement and cell stiffness, further refining our understanding of tip growth dynamics. Collectively, our work provides a comprehensive framework for understanding how transitions between growth phases are orchestrated in plant tip-growing cells.

cell biology↗

Chimeric identities and reduced stiffness characterise the shoot apex of Arabidopsis stem cell mutants

Stem cell homeostasis in the shoot apical meristem involves a core regulatory feedback loop between the signalling peptide CLAVATA3, produced in stem cells, and the transcription factor WUSCHEL, expressed in the underlying organising centre. clavata mutants display massive meristem overgrowth, which is thought to be caused by stem cell overproliferation, although it is unknown how uncontrolled stem cell divisions lead to this altered morphology. Here we first reveal local buckling defects in mutant meristems, and use analytical models to show how mechanical properties and growth rates may contribute to the phenotype. Indeed, clavata meristems are mechanically more heterogeneous than the wild type, and also display regional growth heterogeneities. Furthermore, stereotypical wild-type meristem organisation is lost in mutants, in which cells simultaneously express distinct fate markers. Finally, cells in mutant meristems are auxin responsive, suggesting that they are functionally different from wild-type stem cells. Thus all benchmarks show that clavata meristem cells are different from wild-type stem cells, suggesting that fasciation is caused by the disruption of a more complex regulatory framework that maintains distinct genetic and functional domains at the shoot apex. Summary statementHeterogeneities in cell mechanics, growth, function and identity contribute to buckling in clavata mutant shoot apices.

plant biology↗

Genomic insights into variation in thermotolerance between hybridizing swordtail fishes

Understanding how organisms adapt to changing environments is a core focus of research in evolutionary biology. One common mechanism is adaptive introgression, which has received increasing attention as a potential route to rapid adaptation in populations struggling in the face of ecological change, particularly global climate change. However, hybridization can also result in deleterious genetic interactions that may limit the benefits of adaptive introgression. Here, we used a combination of genome-wide quantitative trait locus mapping and differential gene expression analyses between the swordtail fish species Xiphophorus malinche and X. birchmanni to study the consequences of hybridization on thermotolerance. While these two species are adapted to different thermal environments, we document a complicated architecture of thermotolerance in hybrids. We identify a region of the genome that contributes to reduced thermotolerance in individuals heterozygous for X. malinche and X. birchmanni ancestry, as well as widespread misexpression in hybrids of genes that respond to thermal stress in the parental species, particularly in the circadian clock pathway. We also show that a previously mapped hybrid incompatibility between X. malinche and X. birchmanni contributes to reduced thermotolerance in hybrids. Together, our results highlight the challenges of understanding the impact of hybridization on complex ecological traits and its potential impact on adaptive introgression.

evolutionary biology↗

Dandelion pappus morphing is actuated by radially patterned material swelling

Plants can generate motion by absorbing and releasing water. Such motion often facilitates reproductive success through the dispersal of seeds and fruits or their self-burial into the soil. Asteraceae plants, such as the dandelion, often have a hairy pappus attached to their fruits to allow them to fly and in many cases, these can open and close depending on moisture levels to modify dispersal. Here we demonstrate the relationship between structure, composition and function of the underlying hygroscopic actuator. By investigating the structure and properties of the actuator cell walls we have identified the mechanism by which the dandelion pappus closes and developed a structural computational model that can capture observed pappus closing. This model was used to explore the contribution of differential material domains in the actuator function and the critical design features. We find that the actuator relies on the radial arrangement of vascular bundles and surrounding tissues including cortex and the floral podium around a central cavity. This allows heterogeneous swelling in a radially symmetric manner to co-ordinate precise movements of the pappus hairs attached at the upper flank. This actuator is a derivative of bilayer structures, but is radial and can synchronise the movement of a planar or lateral attachment. The simple, material-based mechanism presents a promising biomimetic potential in robotics and functional materials.

bioengineering↗

Timing of organ initiation is crucial for robust organ size

AbstractOrgans precisely regulate their size and shape to ensure proper function1-6. The contribution of organ initiation timing to final organ size and shape is often masked by compensatory adjustments to growth later in development7-9. Here we show that DEVELOPMENT RELATED MYB-LIKE1 (DRMY1) is required for both proper organ initiation timing and growth leading to robust sepal size in Arabidopsis. Within each drmy1 flower, the initiation of some sepals is variably delayed. Late-initiating sepals in drmy1 mutants remain smaller throughout development resulting in variability in sepal size. DRMY1 focuses the spatiotemporal signaling patterns of the plant hormones auxin and cytokinin, which jointly control the timing of sepal initiation. Contrary to expectation, our findings demonstrate that timing of organ initiation contributes to robust organ size throughout development.

plant biology↗

Xyloglucan homeostasis and microtubule dynamics synergistically maintain meristem geometry and robustness of phyllotaxis in Arabidopsis

The shoot apical meristem (SAM) gives rise to all aerial organs of the plant. The cell walls are supposed to play a central role in this process, translating molecular regulation into dynamic changes of growth rates and directions, although their precise role in morphogenesis during organ formation remains not well understood. Here we investigate the role of xyloglucans (XyGs), which form a major, yet functionally poorly characterized, wall component in the SAM. Using immunolabeling, biochemical analysis, genetic approaches, micro-indentation, laser ablations and live imaging, we show that XyGs are important for meristem shape and phyllotaxis, although no difference in cell wall stiffness could be observed when XyGs are perturbed. Mutations in enzymes required for XyG synthesis also affect other cell wall components such as cellulose content and the pectin methylation status. Interestingly, we show that the control of cortical microtubules dynamics by the severing enzyme KATANIN becomes vital when XyGs are perturbed or absent. This suggests an active role of the cytoskeleton in compensating for altered wall composition.

plant biology↗

Biomechanical control of lysosomal secretion via the VAMP7 hub: a tug-of-1 war mechanism between VARP and LRRK1

The rigidity of the cell environment can vary tremendously between tissues and in pathological conditions. How this property may affect intracellular membrane dynamics is still largely unknown. Here, using atomic force microscopy, we found that cells deficient in the secretory lysosome v-SNARE VAMP7 were impaired in adapting to substrate rigidity. Conversely VAMP7-mediated secretion was stimulated by more rigid substrate and this regulation depended on the Longin domain of VAMP7. We further found that the Longin domain bound the kinase and retrograde trafficking adaptor LRRK1 and LRRK1 negatively regulated VAMP7-mediated exocytosis. Conversely, VARP, a VAMP7- and kinesin 1-interacting protein, further controlled the availability for secretion of peripheral VAMP7 vesicles and response of cells to mechanical constraints. We propose a mechanism whereby biomechanical constraints regulate VAMP7- dependent lysosomal secretion via LRRK1 and VARP tug-of-war control of the peripheral readily- releasable pool of secretory lysosomes.

cell biology↗