Ulrike Mathesius and Michelle Watt
1 Introduction 126
2 Examples for the Roles of Rhizosphere Signals Under Controlled Conditions 127
2.1 Plant Signals Regulating Interactions with Soil Microbes 127
2.2 Perception and Response to Microbial Signals by Plants 133
2.3 Plant Interference with Rhizosphere Signals 139
2.4 Bacterial Interference with Rhizosphere Signals 140
2.5 Adaptation of Signals for Multiple Purposes and Cross-Signaling 141
3 Signaling in Field Rhizospheres 143
3.1 Time, Distances, and Diffusivities Determine Chance of Signal Exchange 144
3.2 Surfaces and Epitopes for Signal Binding Are Constantly Changing 147
3.3 How Do Root Cells Perceive and Respond to the Rhizosphere Microorganism Community? 149
4 Future Approaches 150
Abstract This review presents an analysis of rhizosphere signals important in plant-microbial interactions that have been studied in controlled conditions and how they may function on field-grown roots. We define rhizosphere signals to be molecules on or emitted from microorganism or root cells that are recognized by other cells and trigger a response. A well-known example are the flavonoids from legume roots, which bind to transcriptional activators in rhizobia bacteria triggering the release of Nod factors (lipochitin oligosaccharides) that bind to root hairs or cortical cells initiating nodule development. Many other signals are reported, e.g.,
ARC Centre of Excellence for Integrative Legume Research, Division of Plant Science, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia e-mail: [email protected] M. Watt
CSIRO Plant Industry, Black Mountain Laboratories, GPO Box 1600, Canberra, ACT 2601, Australia
DOI 10.1007/978-3-642-13145-5_5, © Springer-Verlag Berlin Heidelberg 2011
phytohormones, quorum sensing signals (QSS) and their mimics, strigolactones, and exopolysaccharides. Some are involved in infection of roots by symbionts or pathogens; others in growth, physiological, and immune responses caused by commensal organisms that do not invade the root. The signals have so far been largely studied in the classical host-microbe framework in controlled conditions. Field rhizospheres, however, are host-microbe communities that change in space and time. Root surfaces, and thus binding sites for signals, change as the root ages and differentiates, as do chemicals released, which may be energy substrates, signals, or toxins to soil microorganisms in a local patch of soil. The nutritional status and disease susceptibility of the plant and the soil properties are also changing with space and time in the field. These dynamics explain in part why it has been so difficult to translate laboratory effects of signals to the field. Our analysis suggests that signal function in field rhizospheres would depend on (1) compatibility between microorganism populations and root tissue age and cell surfaces for signal-receptor binding, (2) proximity to the root, (3) moisture, and (4) plant nutrition and predisposition to response to microorganisms due to biotic or abiotic factors. These ideas need to be tested. Two major gaps in knowledge are the microorganisms that colonize the rhizosphere and their signals - only a small percentage have been sequenced, and how the plant genetics is regulating the perception and response to the diverse signals that may bind successfully to the root surfaces in the field.
Soil grown plants are surrounded by a myriad of soil microorganisms, some of which have evolved to form symbiotic or pathogenic relationships. Other organisms are commensals living on root substrates such as exudates, mucilages, and dead plant material. While the soil environment is relatively nutrient-poor, the rhizo-sphere can contain high concentrations of nutrients from the root. It has been estimated that up to 20% of the carbon fixed by the shoot could be transferred into the rhizosphere (Knee et al. 2001), and thus microbial numbers, as well as their signals, can be high around the root surfaces. In addition to exudation of nutrients, vitamins, and minerals, the plant also exudes various secondary metabolites, many of which act as signals (Walker et al. 2003a) or as compounds inhibitory to the growth and functioning of microorganisms or roots called allelochemicals (Bertin et al. 2003). Before plants make physical contact with microbial partners, chemical signal exchange has often preceded their interaction and prepared the partner for a successful interaction. This rhizosphere signaling is necessary to coordinate bacterial behaviors, to signal the presence of microbial partners to plant hosts, and to elicit specific responses in hosts and microbial partners that contribute to symbiotic and pathogenic interactions and to commensal interactions (Hirsch et al. 2003).
The rhizosphere has a very wide range of signal molecules from the root or microorganisms that have diverse chemical structures and functions (Table 1;
Fig. 1). We consider in this review signals to be molecules that occur on the surface of, or are released from the cell of one organism, and to bind to another cell, triggering a response. They can be highly specific to cell partners and processes. The identity, function, and response to a number of rhizosphere signals have been well described, e.g., Costacurta and Vanderleyden (1995); Hirsch et al. (2003); Somers et al. (2004), and this review will concentrate on some of the best characterized rhizosphere signals to highlight recent progress as well as gaps in our knowledge about the function and potential application of rhizosphere signals to improve crop plant performance. We will consider the role of rhizosphere signals in specific signaling processes like recognition, attraction of partners, elicitation of host responses, and coordination of bacterial behaviors. We will highlight that signals are not just used for the purpose they might have originally been intended for. There are examples of eavesdropping, signal mimicry, signal interference, and nonsignaling function of "signaling" molecules. In addition, the functioning of rhizosphere signals depends on soil and root properties (Watt et al. 2006b). Signal breakdown can be a physicochemical process, but it can also actively be influenced by hosts and soil microorganisms. An important aspect of rhizosphere signaling is the dependence of signaling on spatial properties of the root, including surface properties and developmental zones, as well as the rhizosphere composition. This paper will review the modes of action of a few key signals in controlled conditions and consider field rhizospheres and the factors that would favor signal exchange to improve crop performance.
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