Enrico Coen - Academia.edu (original) (raw)

Papers by Enrico Coen

Nature communications, Mar 27, 2024

Plants exhibit reproducible timing of developmental events at multiple scales, from switches in c... more Plants exhibit reproducible timing of developmental events at multiple scales, from switches in cell identity to maturation of the whole plant. Control of developmental timing likely evolved for similar reasons that humans invented clocks: to coordinate events. However, whereas clocks are designed to run independently of conditions, plant developmental timing is strongly dependent on growth and environment. Using simplified models to convey key concepts, we review how growth-dependent and inherent timing mechanisms interact with the environment to control cyclical and progressive developmental transitions in plants.

eLife, Nov 28, 2017

How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified sh... more How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified shape changes during mouse heart looping, from 3D reconstructions by HREM. In combination with cell labelling and computer simulations, we propose a novel model of heart looping. Buckling, when the cardiac tube grows between fixed poles, is modulated by the progressive breakdown of the dorsal mesocardium. We have identified sequential left-right asymmetries at the poles, which bias the buckling in opposite directions, thus leading to a helical shape. Our predictive model is useful to explore the parameter space generating shape variations. The role of the dorsal mesocardium was validated in Shh-/mutants, which recapitulate heart shape changes expected from a persistent dorsal mesocardium. Our computer and quantitative tools provide novel insight into the mechanism of heart looping and the contribution of different factors, beyond the simple description of looping direction. This is relevant to congenital heart defects.

Science Advances, Apr 21, 2023

Peltate organs, such as the prey-capturing traps of carnivorous plants and nectary-bearing petals... more Peltate organs, such as the prey-capturing traps of carnivorous plants and nectary-bearing petals of ranunculaceous species, are widespread in nature and have intrigued and perplexed scientists for centuries. Shifts in the expression domains of adaxial/abaxial genes have been shown to control leaf peltation in some carnivorous plants, yet the mechanisms underlying the generation of other peltate organs remain unclear. Here, we show that formation of various peltate ranunculaceous petals was also caused by shifts in the expression domains of adaxial/abaxial genes, followed by differentiated regional growth sculpting the margins and/or other parts of the organs. By inducing parameters to specify the time, position, and degree of the shifts and growth, we further propose a generalized modeling system, through which various unifacial, bifacial, and peltate organs can be simulated. These results demonstrate the existence of a hierarchical morphospace system and pave the way to understand the mechanisms underlying plant organ diversification.

Nature Plants

Grass leaves develop from a ring of primordial initial cells within the periphery of the shoot ap... more Grass leaves develop from a ring of primordial initial cells within the periphery of the shoot apical meristem, a pool of organogenic stem cells that generates all of the organs of the plant shoot. At maturity, the grass leaf is a flattened, strap-like organ comprising a proximal supportive sheath surrounding the stem and a distal photosynthetic blade. The sheath and blade are partitioned by a hinge-like auricle and the ligule, a fringe of epidermally derived tissue that grows from the adaxial (top) leaf surface. Together, the ligule and auricle comprise morphological novelties that are specific to grass leaves. Understanding how the planar outgrowth of grass leaves and their adjoining ligules is genetically controlled can yield insight into their evolutionary origins. Here we use single-cell RNA-sequencing analyses to identify a ‘rim’ cell type present at the margins of maize leaf primordia. Cells in the leaf rim have a distinctive identity and share transcriptional signatures with...

Plant development depends on coordination of growth between different cell layers. Coordination m... more Plant development depends on coordination of growth between different cell layers. Coordination may be mediated by molecular signalling or mechanical connectivity between cells, but evidence for genetic control via direct mechanics has been lacking. We show that a brassinosteroid-deficient dwarf mutant of the aquatic plantUtricularia gibbahas twisted internal tissue, likely caused by a mechanical constraint from a slow-growing epidermis creating tissue stresses. This conclusion is supported by showing that inhibition of brassinosteroid action in anArabidopsismutant compromised for cell adhesion, enhances epidermal crack formation, an indicator of increased tissue tension. Thus, genes driving brassinosteroid synthesis can promote growth of internal tissue by reducing mechanical epidermal constraint, showing that tissue mechanics plays a key role in coordinating growth between cell layers.One-Sentence SummaryInternal twists in a mutant carnivorous plant reveal how genes control growth...

(A-D) Data from cells amenable to tracking in the time-lapse experime... more (A-D) Data from cells amenable to tracking in the time-lapse experiment shown in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g001" target="_blank">Fig 1</a> and <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g006" target="_blank">Fig 6</a>. Data points are colour coded according to leaf width at the beginning of each time interval, as detailed in legend to <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g001" target="_blank">Fig 1</a>. (A) Epidermal cells in the lamina. (B) Subepidermal cells in the lamina. (C) Epidermal cells in the midline. (D) Subepidermal cells in the midline. (E-H) Output from epidermal and subepidermal models. (E) v-cells in the lamina of the epidermal model. (F) v-cells in the lamina of the subepidermal model. (G) v-cells in the midline of the epidermal model. (H) v-cells in the midline of the subepidermal model. Model data points are colour coded according to leaf width at equivalent stages to the data. (I-J) Areal growth rates of tracked cells in the lamina (Lam) and midline (Mid) regions, according to whether they were competent to divide or not competent to divide for the (I) epidermis and (J) subepidermis. Data are grouped according to tracking interval (as in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g001" target="_blank">Fig 1</a>); colours represent leaf widths at the start of each interval (as for A-D). Boxes represent the central 50% of the data, with top and bottom at the 25% and 75% quantiles of the data. Central red lines represent the median of the data, and two medians are significantly different (at a 5% significance level) if their notches overlap. Outliers are shown as red crosses. Data with a sample size less than 15 are omitted. Source data are available from <a href="https://figshare.com/s/b14c8e6cb1fc5135dd87" target="_blank">https://figshare.com/s/b14c8e6cb1fc5135dd87</a>. Lam, lamina; Mid, midline; v-cell, virtual cell.</p

(A, B) Model outputs when leaf has grown to a widt... more (A, B) Model outputs when leaf has grown to a width of about 0.5 mm (see horizontal line in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.s014" target="_blank">S14A Fig</a>). (A) Epidermal model used to generate <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g008" target="_blank">Fig 8G</a>, corresponding to growth in a chamber. (B) Output from epidermal model tuned to match spch growth on plates (by slowing growth by 40% and physiological time by 45%). (C) Leaf grown in a bio-imaging chamber when width has attained 0.46 mm (8DAS). (D) Leaf grown on plates when width has attained 0.48 mm (13 DAS). (E) Enlargement of region indicated by magenta square in C. (F) Enlargement of region indicated by orange square in D. (G,H) Segmented cells from leaves shown in C,D. Cell area colour coded as heat map for A,B. (I) Enlargement of segmented region indicated by magenta square in G; average cell area 123.3 ± 6.4 μm2 (n = 184). All cells with their centroid falling within the square were taken into account. (J) Enlargement of segmented region indicated by orange square in H; average cell area 199.8 ± 17.3 μm2 (n = 111). (K,L) Cell complexity from leaves shown in C,D, quantified through the CD of the LOCO-EFA components of each individual cell’s shape, normalised for cell area (see <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#sec019" target="_blank">Materials and methods</a>). Heat map range corresponds to zero for perfect circular or elliptical shapes, ranging to 5 as more LOCO-EFA harmonics are needed to describe the shape (dimensionless measure). (M) Enlargement of region indicated by magenta square in K. (N) Enlargement of region indicated by orange square in L. Scale bar = 100 μm. Source data are available from <a href="https://figshare.com/s/b14c8e6cb1fc5135dd87" target="_blank">https://figshare.com/s/b14c8e6cb1fc5135dd87</a>. CD, cumulative difference; DAS, days after stratification; LOCO-EFA, Lobe-Contribution Elliptic Fourier Analysis; spch, speechless.</p

(A) Cell areas (heat map) of wild-type (left) and spch</i... more (A) Cell areas (heat map) of wild-type (left) and spch (right) leaves at similar developmental stages. (B-D) Cells amenable to tracking from time-lapse imaging of a wild-type leaf (expressing pSPCH:SPCH-GFP, not shown) at approximately 1-h intervals over 2.5 d (0–57 h, last time point in series not shown). Data are visualised over about 12-h intervals and shown on first time point (underlined) for each interval. Leaf widths for first time point (left to right) are 0.17, 0.23, 0.28, 0.39, and 0.42 mm. (B) Cells amenable to tracking that were competent to divide (green) and either executed division during the interval (light green) or divided in a later interval (dark green). Cells that did not divide (black). (C) Non-stomatal divisions coloured as for (B). Stomatal lineage divisions that executed division during the interval (yellow) or divided in a later interval (orange). (D) Cellular areal growth rates (heat map) for each tracking interval. Leaf outline indicated by dotted black line. The petiole-lamina boundary was defined as described in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.g001" target="_blank">Fig 1</a>. Grey boxes are aligned to the petiole-lamina boundary and extend to 150 or 300 μm. Cells within the magenta lines were assigned as being destined to form the midline according to their position and shape in the final image. Scale bars = 100 μm. See also <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.s012" target="_blank">S12 Fig</a>, <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.s013" target="_blank">S13 Fig</a>, and <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.2005952#pbio.2005952.s014" target="_blank">S14 Fig</a>. Source data are available from <a href="https://figshare.com/s/b14c8e6cb1fc5135dd87" target="_blank">https://figshare.com/s/b14c8e6cb1fc5135dd87</a>. GFP, green fluorescent protein; spch, speechless.</p

Constitutive equations, details of the GFtbox models, complications of remeshing, and the mathema... more Constitutive equations, details of the GFtbox models, complications of remeshing, and the mathematical solution of spherically symmetric growth that is compared with the finite element solution in Figure 6.

Development, 1995

We show that the flowering sectors on plants mutant for floricaula (flo), a meristem identity gen... more We show that the flowering sectors on plants mutant for floricaula (flo), a meristem identity gene in Antirrhinum majus, are periclinal chimeras expressing flo in either the L1, L2 or L3 cell layer. Flower morphology is almost normal in L1 chimeras, but altered in L2 and L3 chimeras. Expression of flo in any one cell layer results in the expression of organ identity genes, deficiens (def) and plena (ple) in all three cell layers of the chimeras, showing that flo acts inductively to promote gene transcription. The activation of both def and ple is delayed, and the expression domain of def is reduced, accounting for some of the phenotypic properties of the chimeras. Furthermore, we show that flo exhibits some cell-autonomy with respect to autoregulation.

Journal of Public Health, 2020

Background There is a high prevalence of COVID-19 in university-age students, who are returning t... more Background There is a high prevalence of COVID-19 in university-age students, who are returning to campuses. There is little evidence regarding the feasibility of universal, asymptomatic testing to help control outbreaks in this population. This study aimed to pilot mass COVID-19 testing on a university research park, to assess the feasibility and acceptability of scaling up testing to all staff and students. Methods This was a cross-sectional feasibility study on a university research park in the East of England. All staff and students (5625) were eligible to participate. All participants were offered four PCR swabs, which they self-administered over two weeks. Outcome measures included uptake, drop-out rate, positivity rates, participant acceptability measures, laboratory processing measures, data collection and management measures. Results 798 (76%) of 1053 who registered provided at least one swab; 687 (86%) provided all four; 792 (99%) of 798 who submitted at least one swab had...

Development, 1995

Flower meristems comprise several distinct cell layers. To understand the role of cell interactio... more Flower meristems comprise several distinct cell layers. To understand the role of cell interactions between and within these layers, we have generated plants chimeric for a key floral homeotic gene, floricaula (flo). These chimeras arose in Antirrhinum by excision of a transposon, restoring flo gene function. Activity of flo in a subset of cell layers gives fertile flowers with an abnormal morphology. This shows that flo can act non-autonomously between layers, although some aspects of its function are impaired. In addition, we show that flo exhibits some cell-autonomy within layers.

eLife, Nov 28, 2017

How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified sh... more How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified shape changes during mouse heart looping, from 3D reconstructions by HREM. In combination with cell labelling and computer simulations, we propose a novel model of heart looping. Buckling, when the cardiac tube grows between fixed poles, is modulated by the progressive breakdown of the dorsal mesocardium. We have identified sequential left-right asymmetries at the poles, which bias the buckling in opposite directions, thus leading to a helical shape. Our predictive model is useful to explore the parameter space generating shape variations. The role of the dorsal mesocardium was validated in Shh-/- mutants, which recapitulate heart shape changes expected from a persistent dorsal mesocardium. Our computer and quantitative tools provide novel insight into the mechanism of heart looping and the contribution of different factors, beyond the simple description of looping direction. This is relev...

The Plant Cell, 1996

In many plant species, self-incompatibility (SI) is genetically controlled by a single multiallel... more In many plant species, self-incompatibility (SI) is genetically controlled by a single multiallelic S locus. Previous analysis of S alleles in the Solanaceae, in which S locus ribonucleases (S RNases) are responsible for stylar expression of SI, has demonstrated that allelic diversity predated speciation within this family. To understand how allelic diversity has evolved, we investigated the molecular basis of gametophytic S I in Antirrhinum, a member of the Scrophulariaceae, which is closely related to the Solanaceae. We have characterized three Antirrhinum cDNAs encoding polypeptides homologous to S RNases and shown that they are encoded by genes at the S locus. RNA in situ hybridiration revealed that the Antirrhinum S RNases are primarily expressed in the stylar transmitting tissue. This expression is consistent with their proposed role in arresting the growth of self-pollen tubes. S allelesfrom the Scrophulariaceae form a separate group from those of the Solanaceae, indicating that new S alleles have been generated since these families separated (-40 million years). We propose that the recruitment of an ancestral RNase gene into SI occurred during an early stage of angiosperm evolution and that, since that time, new alleles subsequently have arisen at a low rate.

Science, 1997

Flowering plants exhibit one of two types of inflorescence architecture: indeterminate, in which ... more Flowering plants exhibit one of two types of inflorescence architecture: indeterminate, in which the inflorescence grows indefinitely, or determinate, in which a terminal flower is produced. The indeterminate condition is thought to have evolved from the determinate many times, independently. In two mutants in distantly related species,terminal flower 1inArabidopsisandcentroradialisinAntirrhinum, inflorescences that are normally indeterminate are converted to a determinate architecture. TheAntirrhinumgeneCENTRORADIALIS(CEN) and theArabidopsisgeneTERMINAL FLOWER 1(TFL1) were shown to be homologous, which suggests that a common mechanism underlies indeterminacy in these plants. However, unlikeCEN,TFL1is also expressed during the vegetative phase, where it delays the commitment to inflorescence development and thus affects the timing of the formation of the inflorescence meristem as well as its identity.

Science

Growth coordination between cell layers is essential for development of most multicellular organi... more Growth coordination between cell layers is essential for development of most multicellular organisms. Coordination may be mediated by molecular signaling and/or mechanical connectivity between cells, but how genes modify mechanical interactions between layers is unknown. Here we show that genes driving brassinosteroid synthesis promote growth of internal tissue, at least in part, by reducing mechanical epidermal constraint. We identified a brassinosteroid-deficient dwarf mutant in the aquatic plant Utricularia gibba with twisted internal tissue, likely caused by mechanical constraint from a slow-growing epidermis. We tested this hypothesis by showing that a brassinosteroid mutant in Arabidopsis enhances epidermal crack formation, indicative of increased tissue stress. We propose that by remodeling cell walls, brassinosteroids reduce epidermal constraint, showing how genes can control growth coordination between layers by means of mechanics.

Science, 2021

Shared systems in leaf development The long, narrow leaves of grasses look rather different from ... more Shared systems in leaf development The long, narrow leaves of grasses look rather different from the often shorter, flatter leaves of eudicot plants. Richardson et al . combined developmental genetics and computational modeling to reveal that these two types of leaves, which are widely separated by evolution, have more in common than expected. Expression of similar patterning genes in the primordial zone is confined to a wedge for the eudicot leaf but expanded to concentric domains in the grass leaf, driving development of the cylindrical, encircling sheath characteristic of grass leaves. Addition or removal of gene expression in a marginal zone contributes to the development of the broader leaf characteristic of eudicots. Thus, grass and eudicot leaves are diversified elaborations of shared toolkits. —PJH

(A) Canvas for divergent petal models with different DGRAD (terracotta region) activity ... more (A) Canvas for divergent petal models with different DGRAD (terracotta region) activity in promoting Kper. 100% activity corresponds to the wild-type model (as in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001550#pbio-1001550-g004" target="_blank">Figure 4C–E</a>), and 50% and 0% activity correspond to virtual mutant models in which the level of DGRAD is reduced to 50% or eliminated. Canvas is shown at 0 DAP (time of virtual clone induction), 2 DAP, and 12 DAP. (B) Flowers of jag-2 and jag-1 mutants. (C–D) Representative outlines of jag-1 petals at various stages of development. Width of petals shown: 87, 310, and 530 µm. (E) Petal length against width throughout petal development (in natural logarithm scale) for wild type (gray crosses) and jag-1 (black crosses). The blue and red lines are the linear regressions for the wild type and mutant, respectively. The gradient for jag-1 is 0.65 compared to 0.78 for wild-type petals, showing that jag petals grow less in width compared to length (see also <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1001550#pbio-1001550-g001" target="_blank">Figure 1D</a>). (F–G) JAG expression pattern at various stages of petal development as visualised with the jag-3 mutant line complemented with a JAG::JAG:VENUS construct. The widths for each DAP images are: 1.5 DAP (75 µm), 5.5 DAP (271 µm), 6.5 (363 µm), and 8.5 DAP (575 µm). For the image at 1.5 DAP the YFP channel is shown merged with the red channel (corresponding to the emission of chlorophyll autofluorescence) Scale bar, 10 µm (A) (0–2 DAP) (C), 20 µm (F), 100 µm (D, G), 500 µm (B), 1 mm (A) (12 DAP).</p

Nature communications, Mar 27, 2024

eLife, Nov 28, 2017

Science Advances, Apr 21, 2023

Nature Plants

Development, 1995

Journal of Public Health, 2020

Development, 1995

eLife, Nov 28, 2017

How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified sh... more How left-right patterning drives asymmetric morphogenesis is unclear. Here, we have quantified shape changes during mouse heart looping, from 3D reconstructions by HREM. In combination with cell labelling and computer simulations, we propose a novel model of heart looping. Buckling, when the cardiac tube grows between fixed poles, is modulated by the progressive breakdown of the dorsal mesocardium. We have identified sequential left-right asymmetries at the poles, which bias the buckling in opposite directions, thus leading to a helical shape. Our predictive model is useful to explore the parameter space generating shape variations. The role of the dorsal mesocardium was validated in Shh-/- mutants, which recapitulate heart shape changes expected from a persistent dorsal mesocardium. Our computer and quantitative tools provide novel insight into the mechanism of heart looping and the contribution of different factors, beyond the simple description of looping direction. This is relev...

The Plant Cell, 1996

Science, 1997

Science

Science, 2021