Root Exudation and Rhizosphere Biology

A, Representation of the complex interactions mediated by root exudates that take place in the rhizosphere between plant roots and other organisms. Organisms are not drawn to scale. QS, quorum sensing. B, In vitro culture of oca (Oxalis tuberosa) grown in sterile liquid medium under UV light exposure. C, Chemical structure of harmine as determined by1H and C13 NMR analysis. D, Fluorescent root exudates from O. tuberosa were observed bound to the blue germination paper under UV light exposure. E, Soil samples showing fluorescence obtained from greenhouse-grown oca plants. Samples were taken 5 cm from the stem girth of the plant, and the numbers (1–8) denote the depth by every 1 cm toward the top-layer soil. In vitro-grown oca plants and soil samples collected from oca's rhizosphere were visualized for blue-purplish fluorescence under UV light exposure with a short wave of UV approximately 254 nm. Although root exudation clearly represents a significant carbon cost to the plant, the mechanisms and regulatory processes controlling root secretion are just now beginning to be examined. Root exudates have traditionally been grouped into low- and high-M r compounds. However, a systematic study to determine the complexity and chemical composition of root exudates from diverse plant species has not been undertaken. Low-M r compounds such as amino acids, organic acids, sugars, phenolics, and various other secondary metabolites are believed to comprise the majority of root exudates, whereas high-M r exudates primarily include mucilage (high-M r polysaccharides) and proteins. The rhizosphere is a densely populated area in which the roots must compete with the invading root systems of neighboring plant species for space, water, and mineral nutrients, and with soil-borne microorganisms, including bacteria, fungi, and insects feeding on an abundant source of organic material (Ryan and Delhaize, 2001). Thus, root-root, root-microbe, and root-insect communications are likely continuous occurrences in this biologically active soil zone, but due to the underground nature of roots, these intriguing interactions have largely been overlooked. Root-root and root-microbe communication can either be positive (symbiotic) to the plant, such as the association of epiphytes, mycorrhizal fungi, and nitrogen-fixing bacteria with roots; or negative to the plant, including interactions with parasitic plants, pathogenic bacteria, fungi, and insects. Thus, if plant roots are in constant communication with symbiotic and pathogenic organisms, how do roots effectively carry out this communication process within the rhizosphere? A large body of knowledge suggests that root exudates may act as messengers that communicate and initiate biological and physical interactions between roots and soil organisms. This update will focus on recent advancements in root exudation and rhizosphere biology. Survival of any plant species in a particular rhizosphere environment depends primarily on the ability of the plant to perceive changes in the local environment that require an adaptive response. Local changes within the rhizosphere can include the growth and development of neighboring plant species and microorganisms. Upon encountering a challenge, roots typically respond by secreting certain small molecules and proteins (Stintzi and Browse, 2000;Stotz et al., 2000). Root secretions may play symbiotic or defensive roles as a plant ultimately engages in positive or negative communication, depending on the other elements of its rhizosphere. In contrast to the extensive progress in studying plant-plant, plant-microbe, and plant-insect interactions that occur in aboveground plant organs such as leaves and stems, very little research has focused on root-root, root-microbe, and root-insect interactions in the rhizosphere. The following sections will examine the communication process between plant roots and other organisms in the rhizosphere. In natural settings, roots are in continual communication with surrounding root systems of neighboring plant species and quickly recognize and prevent the presence of invading roots through chemical messengers. Allelopathy is mediated by the release of certain secondary metabolites by plant roots and plays an important role in the establishment and maintenance of terrestrial plant communities. It also has important implications for agriculture; the effects may be beneficial, as in the case of natural weed control, or detrimental, when allelochemicals produced by weeds affect the growth of crop plants (Callaway and Aschehoug, 2000). A secondary metabolite secreted by the roots of knapweed (Centaurea maculosa) provides a classic example of root exudates exhibiting negative root-root communication in the rhizosphere. Recently, Bais et al. (2002c) identified (±)-catechin as the root-secreted phytotoxin responsible for the invasive behavior of knapweed in the rhizosphere. Interestingly, (−)-catechin was shown to account for the allelochemical activity, whereas (+)-catechin was inhibitory to soil-borne bacteria (Bais et al., 2002c ). In addition to racemic catechin being detected in the exudates of in vitro-grown plants, the compound was also detected in soil extracts from knapweed-invaded fields, which strongly supported the idea that knapweed's invasive behavior is due to the exudation of (−)-catechin. Moreover, this study established the biological significance of the exudation of a racemic compound such as catechin, demonstrating that one enantiomer can be responsible for the invasive nature of the plant, whereas the other enantiomer can contribute to plant defense. Although studies have reported the biosynthesis of the common enantiomer (+)-catechin, little is known regarding the synthesis of (−)-catechin or (±)-catechin as natural products. One possibility is that (+)-catechin production is followed by racemization in the root or during the exudation process. Alternatively, there could be a deviation from th