The role of polyp-stolon junctions in the redox signaling of colonial hydroids Neil W. Blackstone 1, *, Kimberly S. Cherry 1 & David H. Van Winkle 2 1 Department of Biological Sciences, Northern Illinois University, DeKalb IL 60115, USA 2 USDA – ARS, University of Nebraska, East Campus, 344 Keim Hall, Lincoln, NE 58583, USA (*Author for correspondence: Tel.: +1-815-753-7899, Fax: +1-815-753-0461, E-mail: neilb@niu.edu) Key words: epitheliomuscular cell, mitochondria, Podocoryna, Podocoryne, reactive oxygen species Abstract An encrusting colonial hydroid can be regarded as a network of polyps or ‘mouths’ connected by tube-like stolons. The success of the colony crucially depends on putting these mouths where the available food is. Feeding-related perturbations may provide important signals in this regard. After feeding, polyps contract regularly, dispersing food throughout the colony via the gastrovascular fluid. Mitochondrion-rich epithe- liomuscular cells concentrated near polyp-stolon junctions likely drive these contractions. Putatively, the redox state of these cells may influence colony-level form. For instance, the metabolic demand associated with feeding-related contractions results in mitochondria that have relatively oxidized electron carriers and produce lesser amounts of reactive oxygen species (ROS). ROS or other redox-sensitive molecules emitted from polyp-stolon junctions into the gastrovascular fluid may provide stolons with signals influencing elongation, branching, and regression. Treatments of colonies with anti-oxidants cause peripheral stolon tips to rapidly regress. This regression appears to be an active process involving a flux of locally produced peroxides and cell and tissue death. At the same time, polyps and stolon tips in the center of treated colonies remain healthy. ‘Sheet-like’ growth of short, branched stolons ensues. Signals that inhibit the outward growth of stolons may lead by default to the concentrated growth of stolons and polyps in food-rich areas. ROS may mediate signaling mechanisms involving nitric oxide, programmed cell death, a variety of redox- regulated proteins, or all of these. Introduction For a heterotrophic organism, a mouth is a major innovation. A mouth allows feeding on relatively large prey items and the sequestration of large amounts of energy. Nevertheless, to be useful, mouths must be effectively deployed. If the supply of prey items is temporally or spatially variable, this problem is especially acute, particularly for a sessile organism such as a colonial hydroid that relies on prey items for reduced carbon substrate. In such organisms, signaling provided by the food itself may greatly simplify the difficulties of mouth placement. While there are a number of potential mechanisms by which food-related signaling could be achieved (Blackstone, 2001), the polyp con- tractions that begin shortly after feeding (Dudgeon et al., 1999) will be the focus here. These con- tractions seem to be driven in large part by mito- chondrion-rich epitheliomuscular cells (EMCs) concentrated near polyp-stolon junctions (Black- stone et al., 2004). The metabolic demand associ- ated with feeding-related contractions leaves these mitochondria relatively oxidized and diminishes the formation of reactive oxygen species (ROS; Blackstone, 2001, 2003). Here hypotheses will be developed for potential mechanisms linking redox state and ROS to colony-level form. If the mitochondrion-rich EMCs at polyp-sto- lon junctions are involved in colony-wide pat- terning, signals must be transmitted from these junctions to actively growing stolons, for it is the Hydrobiologia 530/531: 291–298, 2004. D.G. Fautin, J.A. Westfall, P. Cartwright, M. Daly & C.R. Wyttenbach (eds), Coelenterate Biology 2003: Trends in Research on Cnidaria and Ctenophora. Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands. 291