To shape a cell: an inquiry into the causes of morphogenesis of microorganisms.

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  • 1 December 1990
    • journal article
    • review article
    • Vol. 54  (4) , 381-431
Abstract
We recognize organisms first and foremost by their forms, but how they grow and shape themselves still largely passes understanding. The objective of this article is to survey what has been learned of morphogenesis of walled eucaryotic microorganisms as a set of problems in cellular heredity, biochemistry, physiology, and organization. Despite the diversity of microbial forms and habits, some common principles can be discerned. (i) That the form of each organism represents the expression of a genetic program is almost universally taken for granted. However, reflection on the findings with morphologically aberrant mutants suggests that the metaphor of a genetic program is misleading. Cellular form is generated by a web of interacting chemical and physical processes, whose every strand is woven of multiple gene products. The relationship between genes and form is indirect and cumulative; therefore, morphogenesis must be addressed as a problem not of molecular genetics but of cellular physiology. (ii) The shape of walled cells is determined by the manner in which the wall is laid down during growth and development. Turgor pressure commonly, perhaps always, supplies the driving force for surface enlargement. Cells yield to this scalar force by localized, controlled wall synthesis; their forms represent variations on the theme of local compliance with global force. (iii) Growth and division in bacteria display most immediately the interplay of hydrostatic pressure, localized wall synthesis, and structural constraints. Koch's surface stress theory provides a comprehensive and quantitative framework for understanding bacterial shapes. (iv) In the larger and more versatile eucaryotic cells, expansion is mediated by the secretion of vesicles. Secretion and ancillary processes, such as cytoplasmic transport, are spatially organized on the micrometer scale. The diversity of vectorial physiology and of the forms it generates is illustrated by examples: apical growth of fungal hyphae, bud formation in yeasts, germination of fucoid zygotes, and development of cells of Nitella, Closterium, and other unicellular algae. (v) Unicellular organisms, no less than embryos, have a remarkable capacity to impose spatial order upon themselves with or without the help of directional cues. Self-organization is reviewed here from two perspectives: the theoretical exploration of morphogens, gradients, and fields, and experimental study of polarization in Fucus cells, extension of hyphal tips, and pattern formation in ciliates. Here is the heart of the matter, yet self-organization remains nearly as mysterious as it was a century ago, a subject in search of a paradigm.