Below-ground habitat construction by plant roots

The presence and activities of plant roots powerfully shape the physical, chemical, and biological processes that create and condition the roots' external environment, the soil (reviewed by Hinsinger et al. 2009; Philippot et al. 2013). In recognition of this organism-environment complex, the relatively shallow soil zone in which physiologically active plant roots occur is termed the "domain of roots" or rhizosphere (a term coined in 1904 by the German botanist and soil ecologist Lorenz Hiltner, as discussed by Hartmann et al. 2008). As Hiltner emphasized, this small volume of soil comprises a dynamic milieu which supports an extraordinary abundance and diversity of invertebrate, fungal, and bacterial soil inhabitants along with the plant roots with which they interact: a single gram of soil can contain 1010 bacteria, 104 unicellular eukaryotes, 104 nematode worms, and up to 25 km of fungal hy- phae (references in Hinsinger et al. 2009). Recent work has revealed highly complex rhizosphere "signal traffic" between roots and soil microorganisms or fauna, between roots within a single plant's root system, and between the roots of one plant and those of others (Philippot et al. 2013). The functional key to this hidden ecosystem is the soil matrix, with its enormous surface area, complex pore structure, and transient patches of water, air, and minerals. These critical soil properties, which strongly influence the morphology, deployment, and physiological activities of roots (see Chapter 4, Section 4.3.2), are in turn strongly influenced by active root systems. In addition to simply taking up nutrients and water, plant roots alter their physical, chemical, and biotic soil environment in ways that feed back to affect their own function, both directly and via complex effects on the soil community.

First, roots physically stabilize and compact soils, reducing the size of the pores that hold air, water, and nutrient solutes (references in McCully 1999). These structural changes determine the physiological availability of these soil resources to the root system itself, as well as to other soil organisms. They also determine the mechanical pressure required for growing roots to penetrate the soil (Hinsinger et al. 2009). The physical soil environment is further shaped by the channels formed by now-dead roots of current and previously living plants in the same location, which often form sites of greater organic matter and microbial density (Bundt et al. 2001).

Second, active roots influence soil moisture patterns and, consequently, the distribution of dissolved mineral ions (Marschner 1995; Hodge 2009; and references therein). By taking up water at different rates in different microsites, plant roots generate heterogeneity in soil water and nutrient content (Fitter and Hay 2002; Hinsinger et al. 2009). In addition, roots of many species redistribute water from wetter to drier soil patches at night, when transpiration ceases and a steeply negative water potential gradient occurs that brings water from roots into their immediate soil environment (Caldwell et al. 1998).

Third, growing roots change soil chemistry in several ways. Roots regulate the uptake and efflux of protons so as to maximize the availability of scarce mineral ions and avoid heavy metal toxicity (Marschner 1995; Hinsinger et al. 2009). Active roots also change soil chemistry by depleting oxygen and releasing substantial amounts of carbon dioxide through respiration (Nye 1981; Philippot et al. 2013). Because microbial communities are powerfully influenced by soil pH, this increase in soil acidification feeds back to influence the soil biota and, consequently, the plants interacting with it (Fierer and Jackson 2006). Another habitat-constructing chemical effect of roots is the addition of atmospheric oxygen into waterlogged and consequently anaerobic soils. This often critical environmental remediation is effected by individuals of the many wetland species that produce an anatomically distinctive, axially continuous porous tissue known as aerenchyma. Aerenchyma channels conduct oxygen from shoot organs, which are in contact with the aerial environment, down to buried roots, from which some of the oxygen is emitted into the rhizosphere (Blossfeld and Gansert 2007 and references therein). Interestingly, the ability of aerenchymatous plants to oxygenate the soil by releasing oxygen from their roots varies, for instance, among different cultivars of rice (references in Marschner 1995).

Roots also continuously shape the physical, chemical, and biotic properties of their surrounding soil zone by synthesizing and releasing into it a broad array of compounds with important habitat-constructing properties (reviewed by Walker et al. 2003; Philippot et al. 2013). These root exudates consist largely of organic compounds such as sugars, amino acids, and phenolics; it is estimated that 5%-21% of all photosynthetically fixed carbon is transferred to the rhizosphere through root secretion (Marschner 1995). Plant roots also synthesize and secrete high molecular weight compounds such as proteins and the polysaccharides found in mucilage. The primary sites of root secretion, as well as of water and nutrient uptake, are the very fine, ephemeral "feeder roots" that (together with their even finer epidermal root hairs) constitute much of the enormous surface area through which plant root systems interface with soil (Badri and Vivanco 2009). Mucilage and other exudates are synthesized and secreted by cells at the tips and sides of the root caps of these tiny roots, as well as by the surface bacteria associated with the roots (Humphries et al. 2005).

These secretions lubricate the root as it passes between soil particles (McCully 1999); plants increase production of these secretions in response to dry or compacted soil (Badri and Vivanco 2009).

As a plant's roots push through the soil, they leave a trail of mucilage that contributes to soil structure by binding soil aggregates to each other (Read et al. 2003; Hinsinger et al. 2009); at the same time, the sloughed-off root cap cells with their mucilage provide food for soil microbial communities (Humphries et al. 2005). Mucilage also contains powerful phospholipid surfactants that, even in small amounts, alter the biophysical properties of the rhizosphere, making a given amount of soil moisture easier for roots to extract and increasing the availability to plants of dissolved nutrients such as phosphate (Read et al. 2003; Hinsinger et al. 2009). Mucilage and other root exudates also interact chemically with the soil to help regulate plant uptake of mineral ions and to prevent the entry of heavy metal toxins (McCully 1999). The production of specific root exudates can be closely regulated by the plant's immediate soil conditions. Specific types of nutrient deficiency increase the secretion of metabolites that increase the availability for uptake of the limiting nutrients; similarly, in response to aluminum stress, plants secrete organic acids that detoxify aluminum in soil (Badri and Vivanco 2009 and references therein).

For individuals of many grass species, mucilage secretion results in the formation of a distinctive plant-environment phenotype. The roots of these plants encase themselves in stable, close-fitting soil sheaths that are formed by the expansion and subsequent contraction of mucilages around soil particles during cycles of soil wetting and drying (McCully 1999). Interestingly, the mucilages involved in producing these rhizosheaths are secreted jointly by root cells and associated root-epidermal bacteria (Watt et al. 1994). Rhizosheaths create a moist zone immediately around the root and thus are believed to facilitate nutrient uptake in dry soils (Watt et al. 1994). Field observations support the view that sheath formation is a response to dry soil: the rhizosheaths that form during midsummer, when the soil is dry, are thicker and more strongly adherent to the root than sheaths that form in moist soil; plants in dry soil also produce mucilage that is more highly adhesive than that produced in moist soil (Watt et al. 1994). The roots of many southern hemisphere plants (including rushes in the Restoniaceae family and perennial desert grasses) form similar sand sheaths in dry soils, but by means of a different mechanism. These plants have long root hairs which develop lignin-encrusted walls that keep them in place; these root hairs trap sand particles close to the root in a thick sheath. This structural sheath comprises a transition zone that facilitates the uptake of water and nutrients from the soil and may also provide physical protection from herbivores (Shane et al. 2011).

The chemical impact of root exudates on the rhizosphere environment occurs largely through effects on soil cohabitants (possibly including competing plant individuals; see de Kroon 2007). Secreted compounds that contain proteins and readily available carbon support soil microorganisms that directly promote plant growth, such as symbiotic mycorrhizae (root-associated fungi; Philippot et al. 2013 and references therein; Figure 5.6). Other root exudates indirectly benefit plants by inducing spore germination of beneficial mycorrhizal fungi (Marschner 1995). Root exudates also promote rhizobacterial populations that suppress plant pathogens by outcompeting them, by producing specific antibiotic compounds, or by inducing systemic resistance in the plant itself (Humphries et al. 2005). It has also been suggested that roots secrete into the rhizosphere defensive compounds that mimic or block bacterial signals involved in collective pathogenic activity (Walker et al. 2003). These complex interactions are not yet well understood, although, intriguingly, the protein secretion profiles of plant roots and soil bacteria are known to change in response to each other's presence (Badri and Vivanco 2009). Indeed, the potential utility of manipulating root exudates as means of biological pathogen control is a subject of ongoing investigation (Humphries et al. 2005). Signaling molecules secreted by plant roots mediate other complex rhizosphere interactions. For example, attacks by larvae of the Western corn rootworm, Diabrotica virgifera, on the leaves of corn, Zea maize, induce the plants' roots to synthesize and secrete fi-caryophyllene, which attracts a nematode that is pathogenic to the insects (Rasmann et al. 2005). The roots of plants in the legume family increase rhizosphere nitrogen content

Plant root systems shape conditions in the rhizosphere in ways that feed back to affect plant function

Figure 5.6 Plant root systems shape conditions in the rhizosphere in ways that feed back to affect plant function. Carbon-rich root exudates support symbiotic mycorrhizal fungi that enhance plant growth and induce fungal spores to germinate. This micrograph shows the intimate relationship between a beneficial mycorrhizal fungus and the corn root on which it is growing. The threadlike filaments around the root are fungal hyphae, and the round bodies are spores. photo by Sara Wright, Courtesy of USDA_ARS.

by exuding compounds that initiate a symbiosis with nitrogen-fixing bacteria (references in Walker et al. 2003; see Section 5.4.2).

The release of habitat-constructing root exudates into the rhizosphere can play a tactical role in plant invasions, in part because the soil biota will lack coevolved responses (Broz et al. 2007). The roots of certain invasive plants release compounds that suppress the fungal symbionts of native species and thus allow the invaders to more easily outcompete their neighbors (references in Hodge 2009). A dramatic example of root-mediated habitat construction is that of the introduced allelopathic plant Centaurea maculosa. For over a century, this Eurasian member of the sunflower family has been aggressively displacing the native flora in western North America to form extensive monospecific stands. Early experiments using activated carbon to adsorb organic exudates showed that Centaurea roots released a substance that was toxic to other types of plant (references in Ridenour and Callaway 2001). Recent work has revealed this root-secreted toxin to be a particular molecular form of the plant secondary metabolite catechin (Bais et al. 2002; Walker et al. 2003). In addition, compounds that leach from Centaurea leaf litter suppress the germination and growth of neighboring plants (Ridenour and Callaway 2001). The chemical impact of both the leaves and the roots of this formidable invader creates a soil environment that native plants cannot inhabit.

This altered rhizosphere is also inhospitable to native soil fungi: a molecular phylotype study showed that the presence of Centaurea plants both reduced the abundance of soil fungi and changed the composition of the soil fungus community (Broz et al. 2007).

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