The architecture of polarized cell growth: the unique status of elongating plant cells Frantis ˇ ek Balus ˇ ka, 1 * Przemyslaw Wojtaszek, 1,2 Dieter Volkmann, 1 and Peter Barlow 3 Summary Polarity is an inherent feature of almost all prokaryotic and eukaryotic cells. In most eukaryotic cells, growth polarity is due to the assembly of actin-based growing domains at particular locations on the cell periphery. A contrasting scenario is that growth polarity results from the establishment of non-growing domains, which are actively maintained at opposite end-poles of the cell. This latter mode of growth is common in rod-shaped bacteria and, surprisingly, also in the majority of plant cells, which elongate along the apical – basal axes of plant organs. The available data indicate that the non-growing end-pole domains of plant cells are sites of intense endocytosis and recycling. These actin-enriched end-poles serve also as signaling platforms, allowing bidirectional exchange of diverse signals along the supracellular domains of longitudinal cell files. It is proposed that these actively remodeled end-poles of elongating plant cells remotely resemble neuronal synapses. BioEssays 25:569–576, 2003. ß 2003 Wiley Periodicals, Inc. Introduction Physical forces shape our world. Hence, a sphere is the default shape for all cells. ‘‘Trypsinized’’ animal cells detached from their substratum, as well as fungal and plant protoplasts released from their surrounding walls, all are almost perfect spheres. However, most living cells do not conform to this apolar state but build some characteristic alternative shape by a process known as cytomorphogenesis. (1–4) Although the details of their interactions may vary between different groups of organisms, dynamic arrays of cytoskeletal elements, which are able to read external and internal cues and to interact with membraneous and exocellular matrix (ECM) molecules, are crucial in conferring the property of cellular polarity in all eukaryotic cells. Here, we compare the major regulatory principles and strategies that govern both the establishment and maintenance of cellular polarity in organisms ranging from simple prokaryotes to complex multicellular eukaryotes. The outcome of our comparison indicates that the mode of polari- zation of most plant cells deviates from that of the eukaryotic mainstream and bears some resemblance to the strategy adopted by rod-shaped bacteria in the polarizing of their cells. Polarity is an inherent feature of cellular life Polarity is understood as the ability of cells to organize their interiors and their external forms so that the physical tendency for spherical symmetry of the cell is broken and, as a first step, a new, cylindrical symmetry is established. Such cells now have the ability to grow differentially, either at their ends or along their sides. However, such a situation, although often loosely referred to as polarity, is really no more than unidirec- tional growth. A true polarity comes about when one end of the cylindrical cell differs from the other, just as the North and South poles of a bar magnet differ in the polarity of the magnetic flux. For instance, neurons are polarized cells, with dendrites acting as ‘‘entry ports’’ and axons as ‘‘output’’ channels for signaling molecules, specialized for rapid cell-to- cell communication. In higher plants, elongating plant cells are also polarized as one end of their end-poles shows an efflux whereas the opposite end shows an influx of signaling molecules like ions and the phytohormone auxin. (5) Cell polarity is often reinforced by a cytoskeleton that integrates cellular space. Directional or polarized growth is also modulated by biotic and abiotic signals, which lead to the assembly and disassembly of cytoskeletal elements through their altered interactions with membraneous compartments of the cell. Besides having a dynamic cytoskeleton,(for plants see Refs. 6–10) most cells also rely on mechanically stable, yet chemically interactive exocellular matrices for the main- tenance of diverse cell shapes. (for plants see Refs. 11,12) BioEssays 25:569–576, ß 2003 Wiley Periodicals, Inc. BioEssays 25.6 569 1 Institute of Botany, Department of Plant Cell Biology, Rheinische Friedrich-Wilhelms-University of Bonn, Germany. 2 Institute of Molecular Biology and Biotechnology, Adam Mickiewicz University, and Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poland. 3 School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK. Funding agencies: The authors are thankful to Alexander von Humboldt Foundation (Bonn, Germany) and the Deutsches Zentrum fu ¨r Luft- und Raumfahrt (Ko ¨ln, Germany) for support. *Correspondence to: Frantis ˇek Balus ˇka, Institute of Botany, Depart- ment of Plant Cell Biology, Rheinische Friedrich-Wilhelms-University of Bonn, 53115 Bonn, Germany. E-mail: baluska@uni-bonn.de DOI 10.1002/bies.10282 Published online in Wiley InterScience (www.interscience.wiley.com). Review articles