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Biology subjects

Formosa-Jordan, P.

Publications and source records attributed to Formosa-Jordan, P..

12 recordsLinked to original sources

Stomatal patterning is shaped by the interplay with giant cell patterning in Arabidopsis

In developing tissues, cells differentiate into distinct cell types and form complex spatial patterns. How distinct patterning systems interact during tissue growth to shape tissue composition and spatial organization remains poorly understood. Here, we investigate this question in the abaxial leaf epidermis of Arabidopsis thaliana, in which the same pool of progenitor cells gives rise to stomata, pavement cells, and giant cells. Using a quantitative approach combining Euclidean and network-based spatial analysis, we show that stomatal number and density are robust to reduced endoreduplication, whereas forced endoreduplication actively competes with the stomatal lineage to reduce stomatal number. Furthermore, we show that the stomatal spatial pattern is also shaped by the broader tissue context such as cell growth, cell division, and giant cell patterning, with distinct consequences for stomatal spatial distribution and cellular arrangement. Our results highlight that the interplay between patterning systems must be considered to understand how tissue organization is established.

plant biology↗

Lateral inhibition governs ancestral cellular patterning in fossil and extant liverworts

The incompleteness of the fossil record and the absence of genetic information limit our ability to understand ancient developmental processes and reconstruct their evolution. Here, we use comparative and mathematical analyses to uncover an evolutionarily conserved patterning mechanism underlying liverwort oil body cell specification. We demonstrate that patterns of oil body cell homologs in fossils of the oldest known liverwort (Metzgeriothallus sharonae) exhibit the spatial organization characteristic of lateral inhibition. A mechanism with local activation and lateral inhibition not only reproduces the patterns observed in fossils, but also oil body cell patterns in the extant liverworts Treubia lacunosa, Apotreubia nana, and Marchantia polymorpha. Our results point to an ancestral patterning mechanism that has been modulated by lineage-specific selective pressures over evolutionary time.

developmental biology↗

Time-dependent bistability leads to critical slowing down during floral transition in Arabidopsis

Developmental transitions occur in the life cycles of all multicellular organisms. Despite their fundamental relevance, the underlying dynamics remain poorly understood. In plants, floral transition is a key developmental process whereby the shoot apical meristem changes from producing leaves to forming flowers. Using quantitative imaging, developmental genetics and dynamical systems theory, we show that a time-dependent bistable switch between expression of APETALA2, a key floral inhibitor, and the floral activators SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 and FRUITFULL, can explain the dynamics of floral transition in Arabidopsis. Notably, we detect a slowing down of the inhibitor dynamics, consistent with the system crossing a critical point of a bistable switch and transiently experiencing a ghost attractor. We demonstrate that this time-dependent bistability is essential to generate the range of dynamical behaviours measured across genotypes, including oscillations in the inhibitor, and that it also confers robustness in the transition. Collectively, our work provides quantitative evidence of time-dependent bistability underlying floral transition, which introduces a new timescale to this developmental process.

systems biology↗

Spatial ploidy inference using quantitative imaging

Polyploidy (whole-genome multiplication) is a common yet under-surveyed property of tissues across multicellular organisms. Polyploidy plays a critical role during tissue development, following acute stress, and during disease progression. Common methods to reveal polyploidy involve either destroying tissue architecture by cell isolation or by tedious identification of individual nuclei in intact tissue. Therefore, there is a critical need for rapid and high-throughput ploidy quantification using images of nuclei in intact tissues. Here, we present iSPy (Inferring Spatial Ploidy), a new unsupervised learning pipeline that is designed to create a spatial map of nuclear ploidy across a tissue of interest. We demonstrate the use of iSPy in Arabidopsis, Drosophila, and human tissue. iSPy can be adapted for a variety of tissue preparations, including whole mount and sectioned. This high-throughput pipeline will facilitate rapid and sensitive identification of nuclear ploidy in diverse biological contexts and organisms.

developmental biology↗

Plasticity and invariance of Arabidopsis inflorescence and floral shoot apical meristems in response to mineral nutrients

In many species, floral organ production is invariant while flower production rate can be plastic. This allows plants to adapt flower number to their environment whilst maintaining a constant flower structure. The CLAVATA/WUSCHEL feedback loop underpins both inflorescence (IM) and floral meristem (FM) activity, respectively responsible for flower and floral organ production. We explore how plasticity and invariance can differ between IM and FM in response to nutrient availability. FM size is less sensitive to changes in nutrients than IM size, and floral organ production is insensitive to these small size changes. However, clavata3 mutants display larger changes in FM size, approaching those observed in WT IM under nutrient change, with increased floral organ number. This suggests that invariant floral organ production requires that FM size undergoes limited changes in response to nutrients. Compared to the IM, in the FM, levels of cytokinin (CK) signaling are lower and CK signaling and WUSCHEL expression are less impacted by nutrient level. Through genetic perturbations, we show a reduced response of FMs to varying cytokinin levels. Our work shows one way that the balance between plasticity and invariance can be set differently in different contexts.

plant biology↗

The receptor-like kinase ALE2 promotes giant cell formation in the sepal epidermis

During sepal development in Arabidopsis thaliana, epidermal pavement cells differentiate into small cells and large, highly endoreduplicated giant cells. While the placement of giant cells differs between sepals, the number of giant cells is fairly consistent. The HD-ZIP class IV transcription factor ATML1 has been found to promote giant cell formation. ATML1 protein fluctuates within epidermal nuclei of developing sepals and high ATML1 concentrations reached in the G2 phase of the cell cycle strongly correlates with giant cell fate specification. A genetic screen for reduced giant cell number identified the receptor-like kinase ABNORMAL LEAF SHAPE2 (ALE2) as being important for giant cell formation. We find that ALE2 functions genetically upstream of ATML1 in promoting the formation of giant cells. We observe that nuclear-localized mCitrine-ATML1 fluctuates in ale2 mutants much as it does in wild type and, importantly, nuclear mCitrine-ATML1 reaches similarly high peak concentrations in ale2-1 mutants as in wild type. This indicates that ALE2 functions upstream of ATML1 by affecting protein activity rather than gene expression or protein degradation. One function of ATML1 is to promote transcription of the CDK inhibitor LGO. We find that LGO transcription is delayed and decreased in ale2-1 mutants as compared to wild-type plants, consistent with ATML1 having impaired protein function in ale2 mutants. Overall, we find that the receptor-like kinase ALE2 is necessary to sensitize cells of the developing sepal epidermis to fluctuations of the transcription factor ATML1.

plant biology↗

A common pathway controls cell size in the sepal and leaf epidermis leading to a non-random pattern of giant cells

Arabidopsis leaf epidermal cells have a wide range of sizes and ploidies, but the mechanisms patterning their size and spatial distribution remain unclear. Here, we show that the same genetic pathway creating giant cells in sepals also regulates cell size in the leaf epidermis, leading to the formation of giant cells. In both sepals and leaves, giant cells are scattered among smaller cells; therefore, we asked whether their spatial arrangement is random. By comparing sepal and leaf epidermises with computationally generated randomized tissues we show that the giant cell pattern becomes less random across the epidermis as the cells surrounding giant cells divide, leading to clustered patterns in mature tissues. Our cell-autonomous and stochastic computational model reproduces the giant cell organization, suggesting that random giant cell initiation together with the divisions of surrounding cells lead to the observed clustered pattern. These findings reveal that cell-size patterning is developmentally regulated by common mechanisms in leaves and sepals, and the spatial pattern of giant cells emerges from the interplay between stochastic cell- autonomous gene expression and tissue growth.

plant biology↗

A regulatory gene network that couples floral transition to shoot apical meristem morphology in Arabidopsis

Plants flower in response to environmental signals. These signals change the shape and developmental identity of the shoot apical meristem (SAM), causing it to form flowers and inflorescences rather than leaves. How the changes in SAM shape and identity are coordinated is poorly understood. Using genetics, confocal microscopy and RNA sequencing, we show that reciprocal repression of the APETALA2 (AP2) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) transcription factors in the SAM is crucial in coupling these processes. During vegetative development, AP2 represses SOC1 transcription to delay floral transition. Later, SOC1 is activated during floral transition in response to environmental cues and represses AP2 transcription. However, during floral transition and prior to its stable repression by SOC1, AP2 rapidly promotes an increase in the size, and changes in the morphology, of the SAM. Thus, direct reciprocal repression of AP2 and SOC1 couples floral transition and changes in SAM morphology, which initiate inflorescence development.

plant biology↗

The transcription factor ATML1 maintains giant cell identity by inducing synthesis of its own (very) long-chain fatty acid-containing ligands

During development, cells not only adopt specialized identities but also maintain those identities. Endoreduplication is thought to maintain cell identity. High concentrations of ARABIDOPSIS THALIANA MERISTEM LAYER1 (ATML1) specify giant cell identity and induce endoreduplication in sepals. How different concentrations of ATML1 can specify different identities remains unclear. Here, we show that high concentrations of ATML1 induce the biosynthesis of both long-chain and very long-chain fatty acids (LCFAs/VLCFAs), and these fatty acids are required for the maintenance of giant cell identity. Inhibition of VLCFA biosynthesis causes endoreduplicated giant cells to resume division and lose their identity, indicating that endoreduplication is not sufficient to maintain cell identity. Structural predictions suggest that LCFA-containing lipids bind to the START domain 2 of ATML1, causing ATML1 dimerization and its auto-activation. Our data and modeling imply that ATML1 induces biosynthesis of its own lipid ligands in a positive feedback loop, shedding light on the intricate network dynamics that specify and maintain giant cell identity. Teaser: Endoreduplicated cells in Arabidopsis thaliana sepals divide and de-differentiate in the absence of VLCFA biosynthesis.

plant biology↗

Sugar signaling modulates SHOOT MERISTEMLESS expression and meristem function in Arabidopsis

In plants, development of all above-ground tissues is controlled by the shoot apical meristem (SAM) which balances cell proliferation and differentiation to allow life-long growth. To maximize fitness and survival, meristem activity is adjusted to the prevailing conditions through a poorly understood integration of developmental signals with environmental and nutritional information. Here, we show that sugar signals influence SAM function by altering the protein levels of SHOOT MERISTEMLESS (STM), a key regulator of meristem maintenance. STM is less abundant in the inflorescence meristems of plants grown or treated under limiting light conditions, with lower STM levels correlating with lower sugar content in these meristems. Additionally, sucrose but not light is sufficient to sustain STM accumulation in excised inflorescences. Plants overexpressing the 1-subunit of SUCROSE-NON-FERMENTING1-RELATED KINASE 1 (SnRK1) accumulate less STM protein under optimal light conditions, despite higher sugar accumulation in the meristem. Furthermore, SnRK11 interacts physically with STM, suggesting a direct local repression. Surprisingly, silencing SnRK1 in the meristem leads to reduced STM expression and severe developmental phenotypes previously associated with STM loss-of-function. Altogether, we demonstrate that sugars promote STM accumulation and that the SnRK1 sugar sensor plays a dual role in the SAM, limiting STM abundance under unfavorable conditions but being required for overall meristem organization and integrity. This highlights the importance of sugars and SnRK1 signaling for the proper coordination of meristem activities.

plant biology↗

An ABA-GA bistable switch can account for natural variation in the variability of Arabidopsis seed germination time

Genetically identical plants growing in the same conditions can display heterogeneous phenotypes. Whether this phenotypic variability is functional and the mechanisms behind it are unclear. Here we use Arabidopsis seed germination time as a model system to examine phenotypic variability. We show extensive variation in seed germination time variability between Arabidopsis accessions, and use a multi-parent recombinant inbred population to identify two loci involved in this trait. Both loci include genes implicated in ABA signalling that could contribute to seed germination variability. Modelling reveals that the GA/ABA bistable switch underlying germination can amplify variability and account for the effects of these two loci on germination distributions. The model predicts the effects of modulating ABA and GA levels, which we validate genetically and by exogenous addition of hormones. We confirm that germination variability could act as a bet hedging strategy, by allowing a fraction of seeds to survive lethal stress.

plant biology↗

Nitrate modulates stem cell dynamics by regulating WUSCHEL expression through cytokinins

The shoot apical meristem (SAM) is responsible for the generation of all of the aerial parts of plants1. Given its critical role, dynamical changes in SAM activity should play a central role in the adaptation of plant architecture to the environment2. Using quantitative microscopy, grafting experiments and genetic perturbations, we connect the plant environment to the SAM, by describing the molecular mechanism by which cytokinins signal the level of nutrient availability to the SAM. We show that a systemic signal of cytokinin precursors3 mediates the adaptation of SAM size and organogenesis rate to the availability of mineral nutrients by modulating the expression of WUSCHEL, a key regulator of stem cell homeostasis4. In time-lapse experiments, we further show that this mechanism allows meristems to adapt to rapid changes in nitrate concentration, and thereby modulate their rate of organ production to the availability of mineral nutrients within a few days. Our work sheds new light on the role of the stem cell regulatory network, by showing that it does not only maintain meristem homeostasis but also allows plants to adapt to rapid changes in the environment.

plant biology↗