Mechanical Signals in Plant Development: A New Method for Single Cell Studies

Lynch, Timothy M.; Lintilhac, Philip M.

doi:10.1006/dbio.1996.8462

Cited by 125 publications

(77 citation statements)

References 0 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…When tension in the plant has been altered experimentally by applying external force (Hernandez and Green, 1993;Lynch and Lintilhac, 1997) or altering expansin levels (Fleming et al, 1997;Cho and Cosgrove, 2000), cell division, organ initiation, and organ fate are affected, and abnormal development results. WAKs are expressed in the meristem and, because they are linked to pectin, one might speculate that they function there as tension sensors.…”

Section: Waks and Developmentmentioning

confidence: 99%

Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion

Wagner¹,

Kohorn²

2001

The Plant Cell

105

180

View full text Add to dashboard Cite

The mechanism by which events in the angiosperm cell wall are communicated to the cytoplasm is not well characterized. A family of five Arabidopsis wall-associated kinases (WAKs) have the potential to provide a physical and signaling continuum between the cell wall and the cytoplasm. The WAKs have an active cytoplasmic protein kinase domain, span the plasma membrane, and contain an N terminus that binds the cell wall. We show here that WAK s are expressed at organ junctions, in shoot and root apical meristems, in expanding leaves, and in response to wall disturbances. Leaves expressing an antisense WAK gene have reduced WAK protein levels and exhibit a loss of cell expansion. WAKs are covalently bound to pectin in the cell wall, providing evidence that the binding of a structural carbohydrate by a receptor-like kinase may have significance in the control of cell expansion. INTRODUCTIONIn animal, fungal, and algal systems, the physical connection and the communication between the extracellular matrix (ECM) and the cell plays a fundamental role in cell growth and division (Fowler and Quatrano, 1997;Lukashev and Werb, 1998;Tsai, 1998). Similarly, the plant cell wall forms an ECM of carbohydrate and protein that provides structure for individual cells and whole organs. The cell wall must be dynamic as cells divide and elongate, and modulation of its composition and architecture is required during its synthesis and after it has been deposited (Cosgrove, 1997;Reiter, 1998). The wall must therefore be considered in the context of modulating plant development (Kohorn, 2000). Communication between the cytoplasm and the cell wall is necessary and evident because events like cell expansion (Cosgrove, 1997) and pathogen infection (Hammond-Kosack and Jones, 1996) lead to altered biosynthesis and modification of cell wall components and downstream cytoplasmic events such as systemic acquired resistance. How the dynamics and synthesis of the cell wall are coordinated with cytoplasmic events is largely uncharacterized.Developing cells have walls that are composed of cellulose, hemicellulose, pectin, and proteins. Cellulose is directly secreted by cellulose synthase into the ECM, where it assembles with hemicelluloses and pectins, which are produced in the endomembrane system and secreted by vesicles. The cell wall also includes endoglucanases (Hayashi et al., 1984; Zuo et al., 2000), xyloglucan endotransglycosylases (Fry et al., 1992;Vissenberg et al., 2000), expansins (McQueen-Mason et al., 1992; Cho and Cosgrove, 2000), and a number of other glycosyl transferases that alter carbohydrate linkages and modify secreted cell wall components. Other cell wall proteins, some of which are heavily glycosylated, have been proposed as structural cell wall components or have been implicated in mediating multiple aspects of plant development (reviewed in: Showalter, 1993; Cosgrove, 1997;Kohorn, 2000). These include the families of proline-rich proteins, glycine-rich proteins, hydroxyprolinerich glycoproteins, and arabinogalactan proteins...

show abstract

Section: Waks and Developmentmentioning

confidence: 99%

Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion

Wagner¹,

Kohorn²

2001

The Plant Cell

105

180

View full text Add to dashboard Cite

show abstract

“…It is not clear whether the instantaneous direction of cell growth or the longer-term average (e.g., as measured over a significant fraction of a cell generation) is more directly relevant to forming the division plane. Under compression, single cells tend to divide in a plane perpendicular to the principal axis of the stress tensor (11), which could indicate a mechanical basis for cell wall placement.…”

mentioning

confidence: 99%

Analysis of cell division patterns in the Arabidopsis shoot apical meristem

Shapiro

Tobin

Mjolsness

et al. 2015

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

View full text Add to dashboard Cite

The stereotypic pattern of cell shapes in the Arabidopsis shoot apical meristem (SAM) suggests that strict rules govern the placement of new walls during cell division. When a cell in the SAM divides, a new wall is built that connects existing walls and divides the cytoplasm of the daughter cells. Because features that are determined by the placement of new walls such as cell size, shape, and number of neighbors are highly regular, rules must exist for maintaining such order. Here we present a quantitative model of these rules that incorporates different observed features of cell division. Each feature is incorporated into a "potential function" that contributes a single term to a total analog of potential energy. New cell walls are predicted to occur at locations where the potential function is minimized. Quantitative terms that represent the well-known historical rules of plant cell division, such as those given by Hofmeister, Errera, and Sachs are developed and evaluated against observed cell divisions in the epidermal layer (L1) of Arabidopsis thaliana SAM. The method is general enough to allow additional terms for nongeometric properties such as internal concentration gradients and mechanical tensile forces.cell division | computer modeling | live imaging | Arabidopsis T he Arabidopsis shoot apical meristem (SAM) is a structure at the tip of the shoot that is responsible for generating almost all of the above-ground tissue of the plant (1). Its epidermal and subepidermal cells are organized into layers with very few cells moving between layers (2, 3). When these cells expand they do so laterally, pushing other cells toward the periphery of the meristem. Division in these cells is anticlinal such that each layer remains one cell thick. The underlying mechanism determining the location of new cell walls is unknown but the qualitative properties of meristematic cell division are well documented (4-8). Perhaps the best known summary is Errera's rule, derived following observations of soap bubble formation. In the modern interpretation, the plane of division corresponds to the shortest path that will halve the mother cell. Errera, in fact, wrote that the wall would be a surface "mit constanter mittlerer Krümmung (= Minimalfläche) [with constant mean curvature (= minimal area)]" (4). Because this does not specify a location for the new cell wall, more recent authors have added to this that the mother cell divides evenly (9, 10). With this modification, Errera's rule is easily quantifiable.A second observation is Hofmeister's rule: New cell walls usually form in a plane normal to the principal axis of cell elongation (5). This rule is more difficult to quantify, because the principal axis of cell elongation is often confused with the direction of growth. Cells are asymmetrical and hence a principal direction of cell elongation can easily be calculated (e.g., the principal axis of inertia or principal component of a segmentation). The assumption is often made that because the cell is more elongated in one direction...

show abstract

“…At one extreme, a molecular geneticist would point to DNA-regulated control of cell division, elongation and differentiation, and exchange of genetic information between cells, and suggest that this would be sufficient to regulate morphogenesis. At the other extreme, a biophysicist might point to the work of Green and others (6), suggesting that tissue buckling might provide a physical basis for organogenesis, where Lintilhac and co-workers have shown that simple application of stress to protoplasts induced cell divisions in directions constrained by the applied force (7,8). These conflicting viewpoints represent extremes that have been formalized in cellular and organismal theories of morphogenesis (9).…”

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.

126

107

View full text Add to dashboard Cite

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

show abstract

Mechanical Signals in Plant Development: A New Method for Single Cell Studies

Cited by 125 publications

References 0 publications

Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion

Wall-Associated Kinases Are Expressed throughout Plant Development and Are Required for Cell Expansion

Analysis of cell division patterns in the Arabidopsis shoot apical meristem

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

Contact Info

Product

Resources

About