MOLECULAR CONTROL POINTS IN RHIZOSPHERE FOOD WEBS

Abstract

Plant roots play diverse roles in the rhizosphere. They function as organs responsible for structural support, for acquisition of mineral and water resources, and for fostering of symbiotic bacteria and fungi. They also sustain a complex food web of prokaryotes and eukaryotes in, on, and near the root. In addition to these well-known functions, roots have a recently discovered role with potentially profound coevolutionary implications for the rhizosphere food web, as well as for terrestrial ecological communities in general. Roots are both a source and a receptor of molecular signals important for mutualistic bacteria and perhaps other soil organisms. Fluid-borne rhizosphere compounds flow in the opposite direction from airborne signals that emanate from plant shoots. The powerful transpiration stream around roots naturally concentrates molecular data in a cafeteria of information about the surrounding soil. These molecular signals, such as N-acylated homoserine lactones and phenazines produced by bacteria, can be interpreted simultaneously by multiple species as well as by the root. We propose a model of multitrophic molecular signals in the rhizosphere that implies multiple roles of roots, as hosts, regulators, and sustainers of terrestrial productivity. We suggest a framework of regulation in the rhizosphere that functions through molecular “control points.” We define control points as regulatory elements that are operated on by selection processes to confer fitness on individual organisms and thereby have effects that propagate through other trophic levels. Identification of a control point creates a hypothesis that can be tested to assess the quantitative significance of that regulatory element. Some control points may transmit or perceive signals between organisms, but others probably integrate changing environmental conditions or external resources into individual life histories and community functions. The promise of understanding the new molecular signals is that genes must closely underlie these control points. This could offer ecology access to the power of molecular biology and allow a deep understanding of the evolutionary significance of these phenomena. One major strength of rhizospheres for addressing these issues is that realistic ecological interactions can be examined in a restricted microcosm under environmentally controlled conditions with organisms whose genomes have been completely defined and/or partially modified. Corresponding Editor: R. B. Jackson. For reprints of this Special Feature, see footnote 1, p. 815