Purdue plant biologists solve major cell puzzle on the way to leaf engineering


epidermal-tissue
This patch of leaf epidermal tissue shows a mosaic of living, computer-modeled cells. Image data of living cells were obtained using plasma membrane marker proteins (magenta) and microtubules (green). Mechanical finite element models of cells show tensile force models. (Photo provided by Dan Szymanski)
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WEST LAFAYETTE, Ind. – The leaves are the main plant organs responsible for photosynthesis. Their size, shape, and angles – all affected by cell structure and growth – can also expose more of their surface to the sun, increasing energy reserves and grain production in crops. The epidermal cells on the outer surface of the leaf control the growth of the organ and form in very convoluted, puzzle-like shapes. Understanding how plant cells control these complex cell sizes and shapes is a major goal of plant biology.

In an article on computer modeling and cell biology in the journal Natural plants, Purdue Dan Szymanski, professor at the Department of botany and phytopathology, have discovered that tensile force patterns in thin, pressurized cell walls carry information that shapes the morphogenesis of cells and tissues. The results reveal a conserved cellular basis of plant growth and are essential for understanding leaf architecture and potentially modifying it in the future to improve plants.

“The epidermis of the leaves is like an exoskeleton, the growth of which determines the size and shape of organs,” Szymanski said. “We show how groups of cells can function as dynamic building blocks for the organ. Patterns of tensile force in the cell wall are decoded by a cytoskeleton-cell wall system that determines how cells in the tissue interact and grow at peak rates. These cell growth patterns can be maintained for days to affect tissue and organ morphology.

Szymanski, in collaboration with Joseph turner, professor of mechanical and materials engineering at the University of Nebraska-Lincoln, showed that cells have areas of high tensile force in their walls. The magnitude and direction of these forces are detected and reflected by the microtubule cytoskeleton.

Microtubules, hollow tubes made from proteins, model the synthesis of cellulose fibers in the cell wall. Extracellular fibers accumulate and orient in these high pressure areas to create cell expansion patterns that maintain tissue integrity and allow rapid expansion of thin-bladed sheets.

Lobed morphology in the inner cell types of the leaf allows efficient gas exchange for photosynthesis, and this cellular trait affects the yield of major crop species. Szymanski’s group discovered a general mechanism of lobe formation in any type of plant cell.

Realistic mechanical computational models of the cell wall have shown that the microtubule system reflects the magnitude and direction of wall tensile forces. Szymanski said.

“We have shown quantitatively that the forces in the wall are continuously detected by the microtubule system,” he said.

These microtubules, which were analyzed in real time by Samy Belteton, a graduate student at Szymanski’s lab, using living cell imaging, model the movement of cellulose synthase machines that make extracellular fibers that locally strengthen the domains of the cell wall. This allows the tissue to adaptively grow within the expanding sheet.

Szymanski and coworkers first identified the location and magnitude of large tensile forces and the identity of the subset of microtubules controlling cell shape. This work provides important information on how mechanical signaling at the periphery of the cell occurs and how it dictates local growth behaviors.

Szymanski’s group will continue to determine how these cellular-level events work at the organ level to define leaf traits. Understanding how these cellular building blocks of leaves acquire their sizes and shapes provides a basis for designing optimal leaf architectures for crop productivity.

The National Science Foundation’s Division of Molecular and Cellular Biosciences supported this research.

Writer: Brian Wallheimer; 765-532-0233; [email protected]

Source: Dan Szymanski; 765-494-8092; [email protected]


ABSTRACT

Real-time conversion of tissue-scale mechanical forces into an interdigital growth model

Samuel A. Belteton, Wenlong Li, Makoto Yanagisawa, Faezeh A. Hatam, Madeline I. Quinn, Margarete K. Szymanski, Mathew W. Marley, Joseph A. Turner,
Daniel B. Szymanski

doi.org / 10.1038 / s41477-021-00931-z

The leaf epidermis is a dynamic biomechanical shell that integrates growth across spatial scales to influence organ morphology. The pavement cells, the fundamental unit of this tissue, irreversibly transform into highly lobed cells which cause the flat sheets to expand. Here, we define how tissue-scale cell wall tensile forces and microtubule-cellulose synthase systems model interdigital growth in real time. A morphologically potent subset of cortical microtubules spans the periclinal and anticlinal cell faces to form cellulose fibers that generate anisotropic wall plaque. The result is polarized local growth that is mechanically coupled to the adjacent cell via a pectin-rich middle coverslip, resulting in the formation of lobes. Finite element pavement cell models have revealed cell wall tensile stress as an upstream structuring element that links biomechanical parameters at the cellular and tissue scale to interdigital growth. Cell lobing in leaves is evolutionarily conserved, occurs in several cell types, and is associated with important agronomic traits. Our general mechanistic models of lobe formation provide a basis for analyzing the cellular basis of leaf morphology and function.

Agricultural communications: 765-494-8415;

Maureen Manier, Head of Department, [email protected]

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