Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE SYNTHASE INTERACTIVE1

Mollier, Corentin; Skrzydeł, Joanna; Borowska-Wykręt, Dorota; Majda, Mateusz; Bayle, Vincent; Battu, Virginie; Totozafy, Jean-Chrisologue; Dulski, Mateusz; Fruleux, Antoine; Wrzalik, R.; Mouille, Grégory; Smith, Richard S.; Monéger, Françoise; Kwiatkowska, Dorota; Boudaoud, Arezki

doi:10.1016/j.celrep.2023.112689

Cited by 8 publications

(5 citation statements)

References 88 publications

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“…We analyzed sepals from 4 genotypes in 2 culture conditions and at different developmental stages. In order to enable the comparison between several sepals that were imaged starting from different stages, we temporally aligned live imaging sequences along a common time frame using sepal width, building upon the approach developed in [40], see Datasets and Methods. The parameters that characterise growth fields in all these sequences are shown in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…To describe the impact of mutations or culture conditions on growth parameters, we compared tissues at equivalent developmental stages. We first synchronized all the live imaging sequences from a dataset by building upon the approach developed in [40]. We considered the time curves of organ width for every sepal and finding the time delays ensuring the best superposition between width vs. time curves, leading to a corrected time T t .…”

Section: Comparing Genotypesmentioning

confidence: 99%

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Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Fruleux,

Hong,

Roeder

et al. 2023

Preprint

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Living tissues display fluctuations -- random spatial and temporal variations of tissue properties around their reference values -- at multiple scales. It is believed that such fluctuations may enable tissues to sense their state or their size. Recent theoretical studies developed specific models of fluctuations in growing tissues and predicted that fluctuations of growth show long-range correlations. Here we elaborated upon these predictions and we tested them using experimental data. We first introduced a minimal model for the fluctuations of any quantity that has some level of temporal persistence or memory, such as concentration of a molecule, local growth rate, or mechanical properties. We found that long-range correlations are generic, applying to to any such quantity, and that growth couples temporal and spatial fluctuations. We then analysed growth data from sepals of the model plant Arabidopsis and we quantified spatial and temporal fluctuations of cell growth using the previously developed Cellular Fourier Transform. Growth appears to have long-range correlations. We compared different genotypes and growth conditions: mutants with altered response to mechanical stress have lower temporal correlations and longer-range spatial correlations than wild-type plants. Finally, we used a theoretical prediction to collapse experimental data from all conditions and developmental stages, validating the notion that temporal and spatial fluctuations are coupled by growth. Altogether, our work reveals kinematic constraints on spatiotemporal fluctuations that have an impact on the robustness of morphogenesis.

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Section: Resultsmentioning

confidence: 99%

Section: Comparing Genotypesmentioning

confidence: 99%

Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Fruleux,

Hong,

Roeder

et al. 2023

Preprint

Self Cite

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“…S6N), which aligns with our model predictions, suggesting that the epidermal layers are under compression. Since cell growth directions are also critical for determining organ shapes (42)(43)(44), we assessed the principal direction of maximal cell growth (PDGmax) in the wild type and as2-7D mutant. The wild type cells on both epidermal layers grow in a highly aligned manner along the sepal longitudinal axis (Fig.…”

Section: Aligned Of Cell Growth Orientation Between Epidermal Layers ...mentioning

confidence: 99%

Growth directions and stiffness across cell layers determine whether tissues stay smooth or buckle

Yadav,

Hong,

Klees

et al. 2023

Preprint

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From smooth to buckled, nature exhibits organs of various shapes and forms. How cellular growth patterns produce smooth organ shapes like those of leaves and sepals remains unclear. Here we show that unidirectional growth and comparable stiffness across both epidermal layers of Arabidopsis sepals are essential for smoothness. We identified a mutant with ectopicASYMMETRIC LEAVES 2(AS2) expression that exhibits buckles on the outer epidermis due to conflicting growth directions and unequal epidermal stiffnesses. Aligning growth direction and increasing stiffness restores smoothness. Furthermore, buckling generates outgrowth by influencing auxin efflux transporter protein PIN-FORMED 1 polarity, indicating buckling can initiate organogenesis. Our findings suggest that in addition to molecular cues influencing tissue mechanics, tissue mechanics can also modulate molecular signals, giving rise to well-defined shapes.One-Sentence SummaryThe keys to unlocking sepal smoothness are unidirectional growth and even stiffness; misplace them, it’s time to buckle up!

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“…Smaller cells are the product of frequent cell division, while giant cells result from early termination of cell division and subsequent endoduplication [4,13,14]. Giant cells are very long cells that can extend from the base to the tip of the sepal, and they are usually quite straight [15,16]. Despite the variability in cell sizes and growth rates, all cells experience a similar sigmoid curve where growth is initially slow, then 3 accelerate, and then slow down again, and they all reach the same maximum of growth rate, albeit at different times [17].…”

Section: Introductionmentioning

confidence: 99%

Sepal shape variability is robust to cell size heterogeneity in Arabidopsis

Trinh,

Lionnet,

Trehin

et al. 2024

Preprint

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How organisms produce organs with robust shapes and sizes is still an open question. In recent years, the Arabidopsis sepal has been used as a model system to study this question because of its highly reproducible shape and size. One interesting aspect of the sepal is that its epidermis contains cells with very different sizes. Previous reports had qualitatively shown that sepals with more or less giant cells exhibit comparable final size and shape. Here we investigate this question using quantitative approaches. We find that a mixed population of cell size modestly contribute to the normal width of the sepal, but is not essential for its shape robustness. Furthermore, in a mutant with increased cell and organ growth variability, the change in final sepal shape caused by giant cells is exaggerated, but the shape robustness is not affected. This formally demonstrates that sepal shape variability is robust to cell size heterogeneity.

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Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE SYNTHASE INTERACTIVE1

Cited by 8 publications

References 88 publications

Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Growth couples temporal and spatial fluctuations of tissue properties during morphogenesis

Growth directions and stiffness across cell layers determine whether tissues stay smooth or buckle

Sepal shape variability is robust to cell size heterogeneity in Arabidopsis

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