Analysis of surface growth in shoot apices

Dumais, Jacques; Kwiatkowska, Dorota

doi:10.1046/j.1365-313x.2001.01350.x

Cited by 102 publications

(114 citation statements)

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“…The software for computing average growth maps could also be used on growth pattern data sets collected using other methods (Dumais and Kwiatkowska, 2002).…”

Section: Ease Of Use and Wider Applicability Of The Methods And Compumentioning

confidence: 99%

Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions

Remmler

Rolland‐Lagan

2012

Plant Physiol.

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Growth patterns vary in space and time as an organ develops, leading to shape and size changes. Quantifying spatiotemporal variations in organ growth throughout development is therefore crucial to understand how organ shape is controlled. We present a novel method and computational tools to quantify spatial patterns of growth from three-dimensional data at the adaxial surface of leaves. Growth patterns are first calculated by semiautomatically tracking microscopic fluorescent particles applied to the leaf surface. Results from multiple leaf samples are then combined to generate mean maps of various growth descriptors, including relative growth, directionality, and anisotropy. The method was applied to the first rosette leaf of Arabidopsis (Arabidopsis thaliana) and revealed clear spatiotemporal patterns, which can be interpreted in terms of gradients in concentrations of growth-regulating substances. As surface growth is tracked in three dimensions, the method is applicable to young leaves as they first emerge and to nonflat leaves. The semiautomated software tools developed allow for a high throughput of data, and the algorithms for generating mean maps of growth open the way for standardized comparative analyses of growth patterns.

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“…The software for computing average growth maps could also be used on growth pattern data sets collected using other methods (Dumais and Kwiatkowska, 2002).…”

Section: Ease Of Use and Wider Applicability Of The Methods And Compumentioning

confidence: 99%

Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions

Remmler

Rolland‐Lagan

2012

Plant Physiol.

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“…At least in some environmental conditions, various bacteria (23,24) and budding yeast (8,25,26) grow at constant rates per unit size (constant relative growth rates) throughout the cell cycle, and metazoan lymphoblasts (27) and human osteosarcoma cells (28) grow at constant relative rates during certain cell cycle phases, whereas fission yeast has been reported to show bilinear growth (two distinct phases of a constant absolute growth rate) (29). In plant tissues where wall-wall contacts between cell neighbors impose additional growth constraints compared with single cells, constant relative growth rates have been tacitly assumed (12,14,30), but this assumption and whether growth rate varies through the cell cycle have not been tested experimentally.…”

Section: Significancementioning

confidence: 99%

“…As cells proliferate radially outward from the SAM's central zone into the peripheral zone, they remain fixed in position relative to one another, experience a gradient of the stem cell reporter CLAVATA3, initiate developmental programs, increase their growth rates, and decrease their interdivision times (11)(12)(13)(14)(15)(16). These tissue-level growth kinetics are common to several plant species (13,16,17).…”

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confidence: 99%

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Willis

Refahi

Wightman

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

187

217

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Cell size and growth kinetics are fundamental cellular properties with important physiological implications. Classical studies on yeast, and recently on bacteria, have identified rules for cell size regulation in single cells, but in the more complex environment of multicellular tissues, data have been lacking. In this study, to characterize cell size and growth regulation in a multicellular context, we developed a 4D imaging pipeline and applied it to track and quantify epidermal cells over 3-4 d in Arabidopsis thaliana shoot apical meristems. We found that a cell size checkpoint is not the trigger for G2/M or cytokinesis, refuting the unexamined assumption that meristematic cells trigger cell cycle phases upon reaching a critical size. Our data also rule out models in which cells undergo G2/M at a fixed time after birth, or by adding a critical size increment between G2/M transitions. Rather, cell size regulation was intermediate between the critical size and critical increment paradigms, meaning that cell size fluctuations decay by ∼75% in one generation compared with 100% (critical size) and 50% (critical increment). Notably, this behavior was independent of local cell-cell contact topologies and of position within the tissue. Cells grew exponentially throughout the first >80% of the cell cycle, but following an asymmetrical division, the small daughter grew at a faster exponential rate than the large daughter, an observation that potentially challenges present models of growth regulation. These growth and division behaviors place strong constraints on quantitative mechanistic descriptions of the cell cycle and growth control.cell size | cell growth | cell cycle | homeostasis | plant stem cells H ow cells coordinate growth and division to achieve a particular cell size remains a fundamental question in biology. Our understanding of this basic property of cells is limited, in part, by the lack of quantitative data on cellular growth and size kinetics over multiple generations, especially in higher eukaryotes (1). Classical studies of cell size homeostasis focused on whether division occurred upon reaching a critical size or after a fixed time period has elapsed (2, 3). However, time-lapse studies of single-celled organisms spanning a range of bacteria (4-7) and the yeast Saccharomyces cerevisiae (8) have recently indicated that cell size is regulated by the addition of a fixed volume increment between divisions. Identification of the size regulation behavior constrains the set of feasible molecular scenarios for how growth and division are coordinated with the cell cycle (8-10). In multicellular tissues, the loss of growth and division/cell cycle coordination could have an impact on the organism's development, yet, to the best of our knowledge, cell growth and size kinetics have never before been measured over generations in a tissue context. The experimental challenges are particularly acute because interdivision times are often on the order of tens of hours, cells have a diversity of shapes necessitating di...

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“…Numerous molecular and physical interactions between cells are required for the control of cell behavior, and gaining a quantitative description is difficult. In previous studies, image analysis tools have been used to process microscopy images and quantify deformation in tissues (11,12). Software models based on reaction diffusion systems have been used to describe molecular transport phenomena (13), gene regulatory networks have been employed to model the regulation of gene expression (14), and feedback-regulated models for polar auxin transport can predict canalisation of vascular tissues (15).…”

mentioning

confidence: 99%

Coordination of plant cell division and expansion in a simple morphogenetic system

Dupuy

Mackenzie

Haseloff

2010

Proc. Natl. Acad. Sci. U.S.A.

129

107

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Morphogenesis in plants arises from the interplay of genetic and physical interactions within a growing network of cells. The physical aspects of cell proliferation and differentiation are genetically regulated, but constrained by mechanical interactions between the cells. Higher plant tissues consist of an elaborate three-dimensional matrix of active cytoplasm and extracellular matrix, where it is difficult to obtain direct measurements of geometry or cell interactions. To properly understand the workings of plant morphogenesis, it is necessary to have biological systems that allow simple and direct observation of these processes. We have adopted a highly simplified plant system to investigate how cell proliferation and expansion is coordinated during morphogenesis. Coleocheate scutata is a microscopic fresh-water green alga with simple anatomical features that allow for accurate quantification of morphogenetic processes. Image analysis techniques were used to extract precise models for cell geometry and physical parameters for growth. This allowed construction of a deformable finite element model for growth of the whole organism, which incorporated cell biophysical properties, viscous expansion of cell walls, and rules for regulation of cell behavior. The study showed that a simple set of autonomous, cell-based rules are sufficient to account for the morphological and dynamic properties of Coleochaete growth. A variety of morphogenetic behavior emerged from the application of these local rules. Cell shape sensing is sufficient to explain the patterns of cell division during growth. This simplifying principle is likely to have application in modeling and design for engineering of higher plant tissues.biophysics | Coleochaete | dynamics | morphogenesis microscopy

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Analysis of surface growth in shoot apices

Cited by 102 publications

References 50 publications

Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions

Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions

Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche

Coordination of plant cell division and expansion in a simple morphogenetic system

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