Chapter 11: Understanding and managing the rhizosphere in agroecosystems 

Laurie E. Drinkwater1 and Sieglinde S. Snapp2		

1Associate Professor
 Department of Horticulture
 Cornell University
 Ithaca, New York 14853
 607-255-9408
 led24@cornell.edu

2Associate Professor
  Department of Crop and Soil Sciences
 Soils and Cropping System Ecologist
 440A Plant and Soil Sciences Building
 Michigan State University
 East Lansing, MI 48824-1325
517-282-5644
 snapp@msu.edu
I.  Introduction
	Agricultural systems represent the major form of land management, covering 5 billion hectares of the global terrestrial land area. The unintended consequences of agriculture extend well beyond agricultural landscapes and include environmental degradation and social displacement (Hambridge 1938; Vitousek et al. 1997; Friedland et al. 1991). Many have advocated the adoption of an ecosystem-based approach that would incorporate multifunctionality as an agricultural goal and entail broad application of fundamental ecological principles to food production (Dale et al. 2000; Drinkwater and Snapp 2005). This approach would aim to reduce external inputs and environmental degradation by increasing the capacity for internal, ecological processes to support crop production while contributing to other ecosystem services (Dale et al. 2000). 
	Most efforts devoted to managing the rhizosphere in agricultural systems have emphasized processes that contribute directly to maximizing yield within the context of resource-intensive cropping systems. Several excellent reviews are available covering the role of rhizosphere biology in promoting crop growth under the nutrient rich conditions of high input agriculture (cf. Pinton et al. 2001; Lynch 1990). In particular, the biology of important root pathogens and plant-microbial N-fixing symbioses have been extensively studied within this context (Spaink et al. 1998; Whipps 2001). A smaller amount of rhizosphere research has focused on achieving modest improvements in yields under severe nutrient or water limitations that are commonly found in low-input, subsistence agroecosystems of the developing countries where farmers do not have access to purchased fertilizers and pesticides (Lynch 1990).
	In this chapter we will assess the current ecological understanding of the rhizosphere in agroecosystems and broaden the scope of rhizosphere contributions to encompass a variety of ecosystem functions beyond those directly related to maximizing crop growth and yields. Our aim is to examine the potential for rhizosphere processes and plant-microbial interactions to restore agroecosystem functions to reduce input dependancy and environmental degradation. We begin with an inventory of how conventional, high input management has altered the soil environment and biota in agroecosystems with particular emphasis on the consequences for the rhizosphere habitat. We then survey a range of rhizosphere processes and examine how current management practices enhance or hinder the process and evaluate the potential for improved functionality. Finally, we look ahead and discuss how management of the rhizosphere and plant-microbial interactions could be approached within multifunctional, ecologically-sound agricultural systems of the future.  
II.	Intensive agriculture: deliberate and inadvertent consequences for the rhizosphere
	The soil environment in agroecosystems reflects the legacy of the native ecosystem and past management combined with current management practices. In early farming systems, human modification was limited to altering plant species composition. As agriculture has evolved, the degree of intervention has grown steadily, culminating with the current, resource intensive “Green Revolution” production systems where management interventions are often the dominant force shaping agroecosystem structure and function. Intentional management of the rhizosphere has focused mainly on biological control of root pathogens and enhancing obligate mutualisms and will be discussed later in this chapter. Here we briefly survey key modifications of the soil environment that result from a broad suite of management practices and their unintentional consequences for the rhizosphere habitat. In practice, farming systems fall along a continuum of intensity as depicted in Figure 1 and have varying impacts on rhizosphere processes. Our discussion will emphasize the situation in conventional, high input annual systems since these production systems supply a substantial portion of food on a global basis, are continuing to expand in developing countries and also have the greatest impact on the environment (Tilman 1999). 
A. Tillage and soil structure
	 Use of tillage in agricultural production began with the development of the plow (~ 4,000 BC in Mesopotamia and Egypt), which permitted large plots of soil to be intensively mixed and planted to a monoculture (Pryor 1985). Tillage remains a ubiquitous feature of nearly all annual cropping systems. A variety of tillage technologies have been developed, however most primary tillage involves mixing the top 15-25 cm of soil in preparation for planting. In addition to the periodic disruption of the soil environment, other consequences of tillage include radically altered pore volume and pore structure, reduced vertical stratification, destruction of biopores from past roots and hyphae, dispersal of microbial communities and fungal hyphae networks and accelerated decomposition of soil organic matter (SOM; Buyanovsky and Kucera 1987; Douds et al. 1995; Baer et al. 2002). Following tillage, the soil tends to settle so that porosity is reduced compared to the original conditions of the native pre-tillage ecosystem. For example, the pore volume (% of soil volume occupied by air or water) in native prairies of the Midwestern US is approximately 60-70% compared to 45-50% in cultivated prairie soils (Baer et al. 2002). Thus, the reliance on tillage profoundly alters the soil environment in terms of atmospheric and water relations (drainage and water holding capacity) while also disrupting processes that are influenced by legacy effects of former roots and fungal hyphae. No-tillage agricultural systems have been developed for annual crops such as the Midwestern grain systems of the United States. Even short periods without tillage extend the influence of root and hyphal remnants in soil (Douds et al. 1995).  A recent study (Williams and Weil 2004) using a minirhizotron to monitor root growth discovered that root channels are recycled in annual rotations where the cash crop was planted without tillage following a Brassica cover crop (Fig. 2). In practice very few fields are maintained in continuous no-till beyond several years (c.f. Drinkwater and Snapp 2005) so only perennial agricultural systems such as pastures and some orchards maintain soil environments that approximate the native state in terms of the degree of physical disturbance and pore structure (Fig. 1).
B.  Nutrient availability and soil chemistry
	Manipulation of soil chemistry began with the advent of liming to raise soil pH in early Roman agriculture and has grown to be a major component of soil fertility management in conventional agriculture so that soil pH is usually more neutral relative to native soils. In general, soil chemistry management aims to optimize the supply of nutrients to the crop. For the past 50 years, intensive agriculture has focused on supplying soluble, plant available forms of major nutrients combined with manipulation of soil pH and additions of micronutrients as indicated by soil tests (Drinkwater and Snapp 2005). In wealthier, industrialized countries major nutrients are generally supplied in surplus quantities as soluble, inorganic fertilizers resulting in cropping systems which are maintained in a state of nutrient saturation, particularly when the cash crop is present. Compared to unmanaged terrestrial systems, the concentrations of soluble, inorganic forms of major nutrients such as N and P in these agricultural systems are often several orders of magnitude greater. In contrast, agroecosystems of poorer developing countries do not have access to manufactured fertilizers and are often producing crops in soils that have depleted nutrient pools from long histories of farming without adequate nutrient return to fields.
C. Carbon flow and soil organic matter
	The use of tillage has major consequences for C distribution and turnover. Tillage eliminates the O horizon and accelerates litter decomposition rates by mixing newly introduced litter with soil (Buyanovsky and Kucera 1987). Furthermore, the advent of fertilizers and herbicides made it unnecessary to grow cover crops and forages in rotation with cash crops and permitted the widespread adoption of the simplified crop sequences that are prevalent today (Drinkwater and Snapp 2005). These rotations typically include bare fallow periods (when land is maintained without any growing plants) in between cash crops. As a result, the time frame of actively growing plants in annual agriculture is commonly limited to 4-6 months per year, decreasing the rhizosphere habitat, C-fixation and inputs of labile C in space and time. Tillage, combined with soluble N additions and the relatively labile composition of crop residues returned to the soil, fosters rapid turnover of particulate organic soil C pools (Buyanovsky and Kucera 1987) while decomposition of the humified fraction may decrease (Neff et al. 2002), shifting the distribution of C pools so that labile, particulate OM is proportionately reduced compared to humified OM (Wander 2004). The reduction in total SOM combined with the disproportionate impact on labile C pools increases the severity of C-limitation in bulk soil and exacerbates the tendency for nutrient saturation while also modifying microbial habitat distribution. 
D.  Consequences for the soil biota and the rhizosphere community
	The abiotic changes outlined above restructure the distribution and frequency of microbial soil habitats (i.e. rhizosphere, aggregates, particulate organic matter and biopores) in agroecosystems and lead to shifts in species abundance and richness of the soil biota.  Management interventions such as tillage, crop species composition and soil amendments act in concert with the background soil environment to alter the indigenous biota in bulk soil (Guemouri-Athmani et al. 2000), and to influence rhizosphere community composition (c.f. Buckley and Schmidt 2003; da Silva et al. 2003 ; Buenemann et al. 2004). Studies comparing the resident microbial community composition across managed ecosystems suggest that soil type is the most important factor, followed by land use and management history (Salles et al. 2004; Bossio et al. 2005). In the short-term, the influence of plants is most significant for the plant-associated habitats such as the rhizosphere and rhizoplane (Salles et al. 2004) however, as the longevity of crop cultivation increases, plant species impacts on microbial community become more detectable (Guemouri-Athmani et al. 2000; Schloter et al. 2000). The effects of cultivation on microbial community structure in bulk soil appear to be long-lasting and can still be detected years after agricultural management has ended (Buckley and Schmidt 2003). 
	It is clear that under intensified agriculture, the rhizosphere community is faced with a unique soil environment that differs substantially from the one in which plant-microbial interactions originally evolved. Ecosystem services that were once supplied by plants and associated soil organisms are now largely provided through a variety of inputs. Biotic functional diversity has been replaced by increased intervention including tillage, and the use of soluble fertilizers and pesticides (Drinkwater and Snapp 2005). In essence, it is the management system that has created the dependence upon many of the agricultural inputs that target the belowground system in agriculture, similar to the pesticide treadmill that was first proposed in the 1960's to describe the increased dependence on insecticides created by chemical control of aboveground herbivorous arthropods (Smith and van der Bosch 1967). The use of tillage necessitates the need for continued tillage due to diminished SOM and degraded soil structure (Topp et al. 1995). The high concentrations of plant-available nutrients in space and time may reduce the role of mutualist rhizosphere organisms since energetics favor plant acquisition of these soluble nutrients which are supplied in quantities surpassing crop needs (see Johnson and Gehring, this volume). Finally, alterations in the soil environment combined with simplified rotations often increase the frequency and severity of pathogen infections leading to dependence on broad spectrum fungicides such as methyl bromide (Cook 1993; Abawi and Widmer 2000).

III.  Rhizosphere processes and agroecosystem function
	It is against this backdrop of a highly modified soil environment and the cascading effects on soil biota that we examine the rhizosphere in agriculture and consider how to redirect management to restore rhizosphere processes and agroecosystem function. Rhizosphere microorganisms and their associated primary producers contribute both directly and indirectly to a wide range of ecosystem functions (Figure 3). Processes such as aggregation, nutrient cycling, hydrology and C storage are jointly mediated by plants and soil organisms through interactions in the rhizosphere, although the significance of rhizosphere contributions has generally been diminished in agroecosystems by inputs and other interventions (Figure 1). 
E. Rhizosphere-mediated aggregation
	Soil aggregation determines the pore structure and dispersion resistance of soil and is a fundamental driver of soil and ecosystem functioning. The proportion of soil particles sequestered in aggregates contributes to the movement and storage of water, soil aeration, and species composition and distribution of soil organisms. These factors interact with one another and influence numerous ecosystem processes including: 1) water holding capacity, infiltration and erosion, 2) temporal and spatial distribution of anaerobic conditions 3) growth of plant roots and fungal hyphae, and 4) the cycling and storage of nutrients and carbon (Angers and Caron 1998). The process of aggregate formation is particularly important in agroecosystems where tillage periodically disrupts soil structure and accelerates the breakdown of macroaggregates and physically-protected labile SOM. While parent material and clay surface chemistry regulate micro-aggregate formation, plants and soil organisms are the major drivers of macro-aggregate formation (Tisdall and Oades 1982). As a result, the feedbacks between plants, soil organisms and soil structure are key regulators of productivity and biogeochemical functioning of agroecosystems. In soils with a high proportion of fine silt and clay particles, aggregation is a prerequisite for life because most plants require some level of aggregate structure to create pores for aeration and water flow in order to grow in these soils.
	The potential for agricultural plants and their associated rhizosphere organisms to foster aggregate formation has been studied since the early 1980's (Reid and Goss 1981; Tisdall and Oades 1982) and is recently reviewed by Angers and Caron (1998). Most of this research has focused on the effect of different plant species on water stable aggregation in bulk soil which reflects root litter and rhizosphere processes. In general, perennial forage crops and annual legumes and grasses tend to increase water stable aggregation compared to cash crops or bare fallow (Reid and Goss 1981, Angers and Caron 1998). These are the agricultural plants that have been removed from most rotations in favor of simplified rotations enabled by modern agriculture. Maize, tomato and wheat actually decreased aggregate stability while growth of perennial ryegrass and alfalfa tended to increase it. Rhizosphere mediated impacts on aggregate stability in bulk soil accrue over time and have been related to plant parameters such as total root biomass or root length (Rillig et al. 2002), microbial polysaccarhides produced in the rhizosphere (Reid and Goss 1981), and more recently, fungal populations associated with the rhizosphere (Haynes and Beare 1997; Rillig et al. 2002) or fungal products such as glomalin (Wright et al. 1996). 
	The role of plant-microbe symbiosis in aggregate formation is most extensively documented for arbuscular mycorrhizal fungi (AMF) which are an important biotic regulator of water stable aggregation in bulk soil. The discovery of glomalin, a collection of iron-containing glycoproteins produced by AMF (Wright et al. 1996), has provided an unprecedented opportunity to study the ecology of biotic aggregate formation. To date, glomalin has been found in virtually all soils tested for the glycoprotein although the quantity can vary from up to 100 mg g soil-1 in tropical forest soils to 3-4 mg g soil-1 in temperate agricultural soils (Wright and Anderson 2000; Rillig et al. 2001). Glomalin is a moderately stable component of the SOM, with a mean turnover time reported to range from 6-40 years. The structure of glomalin has not been characterized so the true function of the glycoprotein remains unresolved and is an active area of research.
	More recently, the role of rhizosphere bacteria in promoting aggregation of soil within close proximity to roots, i.e. rhizosphere or root-adhering soil, has been investigated. Several rhizosphere organisms that foster aggregate formation through production of exopolysaccharides (EPS) have been identified and linked to improved soil structure of root-associated soil (Gouzou et al. 1993;  Alami et al. 2000). The EPS-producing bacteria Paenibacillus polymyxa (strain CF43), an N-fixing bacteria endemic to the wheat (Triticum aestivum L.) rhizosphere fosters significant increases in the aggregation and water-holding capacity of soil adjacent to roots (Gouzou et al. 1993). In a study of sunflower (Helianthus annuus L.) and an EPS-producing Rhizobium sp (Strain YAS34) isolated from the sunflower rhizosphere, inoculation with this organism resulted in increased abundance in the rhizosphere, modified soil structure and water holding capacity around the root system, and a corresponding improvement in the drought resistance of the plant (Alami et al. 2000). This type of localized modification of soil structure through the production of EPS appears to be important for non-irrigated agricultural systems at the scale of individual plants. It is likely to be most significant for short term modifications of water movement and storage since these polysaccharides are readily decomposed and probably have a much shorter mean residence time than glomalin-type substances.
	Questions about the function of these compounds, their evolutionary significance and the mechanisms that control their production remain unanswered. This information coupled with a greater understanding of the extent to which cultivar selection, tillage and other interventions may have inadvertently influenced crop-microbial interactions that foster aggregate formation is crucial for intentional management of biotic aggregation. The promotion of aggregation through production of complex, extracellular polymers has often been viewed as a secondary consequence of release of these substances in the environment. Clearly, bacterial production of EPS is a widespread phenomenon occurring across microbial habitats associated with the formation of biofilms (Morris and Monier 2003). However, given the prevalence of organisms that are able to release copious amounts of these compounds into the soil and the benefits that accrue through improvements in soil structure, it is possible that under certain conditions soil structure modification is the major function of these compounds. Although a systematic study of the abundance of EPS-producing species across ecosystems that vary in terms of clay content has not been conducted, some evidence suggests that at least within bacterial species, strains that are present in high-clay soils tend to produce significant amounts of EPS (Achouak et al.1999) and promote aggregate formation (Gouzou et al. 1993). One in vitro experiment demonstrated that glomalin production by Glomus intraradices is extremely plastic and appears to respond to environmental conditions such as pore structure (Rillig and Steinberg 2002). In this study, the production of glomalin was increased under unfavorable growing conditions simulating a soil structure lacking sufficient pores. These findings are intriguing, however more research is needed to conclusively determine the primary function of these extracellular compounds.
F.  Decomposition and net mineralization of nutrients
	Plant-mediated decomposition and corresponding mineralization of nutrients via the rhizosphere (“microbial loop” or “priming effect”, see Cheng and Gershenson, Griffiths et al., this volume) is not considered to be important in conventional agriculture and hence, deliberate management of this process has not been attempted. While some plants are able to produce and secrete enzymes required for P mineralization (Vance et al. 2003), release of nutrients from organic compounds is largely carried out by heterotrophic microorganisms through the production of  extracellular enzymes that can attack polymers and release small, soluble molecules. The role of plant microbial interactions in accessing organic nutrient pools is considered to be of central importance in organically-managed systems (Drinkwater 2004). Although SOM pools are not generally the target of conventional soil fertility management, it is clear that the microbial loop may serve as a significant source of nutrients, particularly N, even in cropping systems receiving large fertilizer additions. Despite application of luxurious amounts of N and use of refined best management practices, crops still acquire 40-80% of their N from endogenous soil reserves and an average of 50% of the N applied is lost from agricultural landscapes (Tilman 1999). 
	Clearly, greater reliance on plant-mediated mineralization for nutrient acquisition in agroecosystems would reduce the potential for nutrient losses due to the tight coupling between the release of soluble, potentially mobile nutrient forms and plant uptake in the rhizosphere. This could be particularly advantageous in the case of N which is highly susceptible to loss once it is converted to inorganic forms. Inorganic N pools can be extremely small while high rates of net primary productivity (NPP) are maintained if N-mineralization and plant assimilation are spatially and temporally connected in this manner. 
	We expect that during millions of years of co-evolution plant-microbial feedbacks have evolved to regulate this co-dependency. Until the advent of Haber-Bosch N, the presence of inorganic N was indicative of net mineralization (with the exception of soils where NH 4+ is present in clays). Thus, plants could increase their access to N through root proliferation and exudation of labile C to support decomposition when inorganic N patches were encountered. In split root studies, rhizodeposition is increased by roots exposed to greater concentrations of inorganic N compared to roots from the same plant that are under low inorganic N conditions (Paterson 2003). We believe it is safe to say that the feedback mechanisms regulating this exchange are not fully understood and that the coupling of plant-microbial nutrient flows has probably been unintentionally modified in high input agricultural systems. Furthermore, it is unclear how crop breeding, which has occurred primarily under nutrient saturated conditions, has affected the ability of crops to access these pools of organic N via this mechanism. While crops certainly stimulate microbial decomposition of SOM (Clarholm 1985; Paterson 2003), selection in soil environments where inorganic N and P are supplied in surplus quantities would tend to favor the development of cultivars that did not squander fixed C to obtain N or P. In fact, it is possible that the combination of a modified soil environment and crop selection for such an environment has undermined the capacity of some crops to access certain organic nutrient reserves.
	While we can speculate about the mechanisms regulating plant-microbial interactions that influence decomposition, many questions remain to be answered if we are to effectively manage this process in agroecosystems. In particular, it will be important to identify the SOM pools accessed by plant-mediated decomposition in order to manage agroecosystems to enhance these reservoirs without fostering increases in net N mineralization in the absence of plants. Our current understanding of decomposition energetics suggests that labile C is needed in order to support the breakdown of the large reservoirs of humus which consists of complex polymers with a C:N ratio of about 12:1. The importance of rhizosphere habitats in fostering decomposition of chemically recalcitrant substrates is supported by bioremediation studies which have demonstrated that decomposition of soil contaminants such as polycyclic aromatic hydrocarbons is accelerated in the rhizosphere (Siciliano et al. 2003). In addition to targeted management of SOM pools, other attributes such as food-web structure could also be influenced by management to optimize this process. 
G.  Rhizobial and mycorrhizal associations
	The specificity of the legume and rhizobia association has been exploited by farmers and agricultural scientists for centuries. Application of Rhizobia inoculum to the seeds of leguminous species is the most widely practiced, conventional agricultural technology used to deliberately manipulate rhizosphere microorganisms. This direct biological intervention has been credited with enhancing N fixation by 30 to 75% in grain legumes (Moawad et al. 1998). However, indigenous strains of Rhizobia are often more effective at colonizing nodules than inoculated strains, even if the seed is inundated with Rhizobia inoculum. The interaction of focal plant with the bacterial inoculum, and the outcome in terms of colonization and development of a symbiotic organ such as nodules are highly dependent on space and time. For instance the community of nodule inhabitants is significantly influenced by rhizosystem architecture in inoculated soybeans (Espinosa-Victoria et al. 2000). Nodules located near the central root system are developed through plant symbiotic interactions with inoculated Rhizobium species, while external nodules far from the central axis are likely to be inhabited by indigenous, and often ineffective, Rhizobium.
	Indigenous rhizosphere populations generally resist invasion by inoculated organisms in the absence of host-microorganism specificity. This is illustrated by the widespread failure of efforts to manage arbuscular mycorrhizae in agricultural systems through inoculation-based technologies (Hamel 1996). There are exceptions, usually involving inundation of young, uncolonized tissues in an environment with few established organisms. Examples include inoculation of seeds or mycorrhizal treatment of horticultural plantings at mine rehabilitation sites, containerized systems or seriously degraded and fumigated soils (Jeffries et al. 2003). With the notable exception of the legume-Rhizobia association, inoculation techniques have not led to consistent or persistent effects on nutrient availability in conventional agriculture. A promising area of research is to examine the potential to manage these mutualisms in low input and organic systems that provide an energetically and biologically favorable environment for displacing or augmenting indigenous micro flora and fauna, compared to conventional agriculture (Kumar et al. 2001). 
	Agricultural management practices have profound indirect consequences on these rhizosphere mutualisms. Reliance on soluble nutrients markedly alters community dynamics in the rhizosphere and may have inadvertently selected for ineffective mycorrhizal and legume-Rhizobium symbioses in modern agricultural systems. A case can be made that the evolution of plant-microsymbiont relationships has been mediated by agricultural practices, many of which favor parasitism over mutualism (e.g. Kiers et al. 2002). Mycorrhizal species composition in high nutrient input corn systems has been shown to favor ineffective strains (Douds et al. 1995), but there has been very limited research on the mutualist to parasitic role of microbial associations in agroecosystems. 
	The N balance in agricultural systems is profoundly influenced by the regulation of the N2-fixation process by soluble nitrogen. There is genetic variation in both plant host and Rhizobium bacteria for tolerance of the N2-fixation process to the presence of nitrate, but in the vast majority of cases the presence of nitrate is highly suppressive to symbiotic N2-fixation (c.f. Kiers et al. 2002). Indirect consequences of the suppression of N2-fixation by soil N may include suppression of mycorrhizal function since flavonoids that induce nodulation also stimulate hyphal growth of the AM fungi (Rengel 2002). 
	Nutrient input level is a major regulator of plant-mycorrhizal symbiosis (see Johnson and Gehring, this volume). Application of inorganic P has been widely shown to directly suppress mycorrhizal infection of roots (Jasper et al. 1979), and to suppress function of the plant-mycorrhizal symbiosis in maize and soybean (McGonigle et al. 1999). Disturbance from tillage is another factor that reduces the presence of mycorrhizal symbiosis (Galvez et al. 2001).  Further study of the intermediate and longer term consequences of agricultural management practices on plant symbioses is urgently required.
H.  Biological control and community ecology of the rhizosphere
	In general, conventional agricultural practices stimulate facultative saprophytic pathogens and increase crop susceptibility to disease. The edaphic environment is modified as shown in Figure 1, with high inorganic nutrient availability and low diversity carbon inputs associated with conventional agricultural systems. This profoundly influence substrate, habitat availability and microbial community dynamics (Hoitink and Boehm, 1999). These environmental modifications in conjunction with short rotations are the root of many soil-borne disease problems. This is evident in intensively managed, high value vegetable crops where reliance on fumigation, multiple tillage operations and high rates of fertilizer is often associated with compacted soils, low levels of soil microbial activity and recurring root health problems (Abawi and Widmer 2000).	
The use of inoculation with beneficial, biological control organisms that will colonize the rhizosphere shows some promise as a means to suppress plant disease (Cook et al.1993). Successful application has been rare, although a notable exception is inoculation of plant habitats with limited colonization such as seeds and emerging radicle. For example, application of Pseudomonas fluorescens to tomato seeds reduced development of the pathogen Pythium ultimum. Suppressive capacity was linked to siderophore production and established presence of P. fluorescens (Hultberg et al. 2000).	
Efforts to reduce soil borne diseases by modifying the soil environment have also met with some success. Management that augments the time frame of living cover and diversity of carbon inputs is associated with enhanced activity and presence of soil microorganisms. If non-pathogenic rhizosphere organisms are well-established, this will tend to suppress soil-borne disease organisms through mechanisms such as competition for resources and habitat (Whipps 2001), antagonistic compounds (Robleto et al. 1998), degradation of pathogenicity factors or pathogen cell walls, promotion of vigorous, healthy roots (Snapp et al. 1991; 2003) and induction of systemic resistance in the target plant against the pathogen (van Wees et al. 1999). Soilborne phytopathogens encounter antagonism from rhizosphere microorganisms before, during and after primary infection and secondary spread within the root. Readers are refereed to recent reviews which focus on the mechanisms of suppressive soils (e.g. Sturz and Christie 2003).
A well-studied example of rhizosphere occupants and consequences for soil-borne disease is take-all (Gaeumannomyces graminis var. tritici) in wheat, one of the most important, devastating fungal diseases in cereal production around the world (Cook 1993). Wheat is a rare case where temporal monoculture has proven beneficial to pathogen suppression. Generally, after initially severe outbreaks, the disease is suppressed in continuous wheat monocultures through a phenomenon known as take-all decline. Altered population dynamics of rhizosphere bacteria are consistently associated with suppression of take-all, and most recently, Pseudomonads that secrete 2, 4-diacetylphloroglucinol (2,4-DAPG), a compound that directly inhibits G. graminis var. tritici have been identified as the major antagonists (Gardener et al. 2001; Mazzola 2004). As the longevity of a continuous wheat monoculture increases, 2,4-DAPG producing Pseudomonads become more abundant (Gardner et al. 2001). The control of G. graminis in wheat by 2,4-DAPG strains has been documented in disparate geographical regions and can be enhanced by management practices (i.e. no-till enhances the development of suppressive populations of Pseudomonads, Mazzola 2004). Finally, wheat cultivars play a role in determining the particular Pseudomonad strains that will become most abundant (Mazzola et al. 2004). This case can serve as a model example of the potential for rhizosphere ecology to be applied in managing complex plant-microbial interactions so that chemical controls are not needed.
I.  Plant species and cultivar effects on rhizosphere processes
	It is well-known that plants exert an influential role on rhizosphere community composition (Hawkes et al., this volume), and that the selection for particular microbial assemblages in the rhizosphere eventually impacts the microbial community structure in bulk soil (Schloter et al. 2000). This is important in the context of agricultural systems because it suggests that crop rotations can be intentionally designed to manage the resident microbial and rhizosphere communities. Indeed, this strategy has been employed in agriculture in a rudimentary fashion though the use of rotation to reduce the severity of soil borne diseases even before the identity of the pathogens was known (Cook 1993). Hawkes et al. (this volume) have reviewed the literature on the role of plant species in determining rhizosphere microbial community composition. Here we examine plant influences on rhizosphere communities in an agricultural context with particular emphasis on the consequences of crop breeding and the role of plant intraspecific genotypic variation in regulating rhizosphere microbial community composition. 
	Plant selection in the last half-century has occurred almost entirely under management regimes that include fumigated soils with luxurious additions of nutrients and sufficient water (Boyer 1982). This strategy of reducing environmental variation by providing ample resources reduces gene by environment interaction, and enhances the power of selection for specific traits (Boyer 1982). Growing evidence suggests that this approach has altered belowground function in crops and may have selected against traits that allow crops to maintain productivity in environments that differ from those created by high input systems (Jackson and Koch 1997; Bertholdsson 2004). While this is an interesting hypothesis, it has yet to be proven. In many cases, the underlying phenotypic alterations that have contributed to improving yield potential under these high input conditions have not generally been identified (Boyer 1982) however, there are a few examples where modification of belowground plant traits of modern cultivars has been demonstrated (Jackson 1995; Bertholdsson 2004; Briones et al. 2002). In lettuce, plant breeding approaches have altered root architecture and the ability of root branching to respond to soil environmental conditions such as nutrient limitation (Jackson 1995; Jackson and Koch 1997). A study comparing 137 barley cultivars representing a time span of 100 years of crop selections found that allelopathic abilities resulting from root exudates are reduced in modern hybrids compared to older varieties (Bertholdsson 2004). In this study, alleopathic activity of roots decreased by 32-85% in modern hybrids compared to the older cultivars. Finally, in wheat and barley, increased plasticity in root hair length has been linked to improved capacity to acquire soluble P (Gahoonia et al. 1999).
 	Studies comparing the role of intraspecific genetic variation on rhizosphere microbial community composition have reported varying results. Some report little or no detectable cultivar effect ( c.f. Devare et al. 2004) while others find substantial differences in microbial community composition in the various plant-associated habitats (Germida and Siciliano 2001; Briones et al. 2002; da Silva et al. 2003; Mazzola et al. 2004). Many of these studies do not include information about the degree of genotypic variation among the cultivars studied making it difficult to interpret contradictory results. Since the development of genetically-modified crops, there have been numerous studies investigating the effect of these new genotypes on plant-associated soil microbes. Studies comparing the original non-GMO hybrid to the GMO version in terms of root associated microbes report variable results, however single gene modifications that are expressed in belowground functions frequently do result in detectable modifications of rhizosphere community composition (cf. Dunfield and Germida 2004). Comparisons across cultivars with noticeable phenotypic variability in systemic growth characteristics have detected significant differences in rhizosphere community composition (da Mota et al. 2002; da Silva et al. 2003; Mazzola et al 2004). In a study comparing Pseudomonad rhizosphere populations in five wheat cultivars, Mazzola et al. (2004) reported that the cultivars differed in their capacity to select for populations of 2,4 DAPG producing Pseudomonas species. Comparisons of traditional or pre-industrial cultivars to modern, highly-selected varieties frequently detect differences in rhizosphere community composition (Germida and Siciliano 2001; Briones et al. 2002; 2003). As more sophisticated molecular techniques become widely available, a picture is emerging which suggests that more closely related cultivars will have greater similarities in rhizosphere community composition compared to more distantly related cultivars (Schloter et al. 2000; da Mota et al. 2002; da Silva et al. 2003). 
	Although it is becoming well accepted that intraspecific differences in plant genotypes influence rhizosphere community composition, the consequences for rhizosphere function are rarely understood. An excellent example linking plant genotypic and phenotypic differences to rhizosphere processes occurs in ammonia-oxidizing bacteria (AOB) populations in the rhizosphere of traditional versus modern rice cultivars (Briones et al. 2002; 2003). Efficient management of N in rice paddies is particularly challenging because rice paddies are typically maintained under flooded conditions and are essentially anoxic below the soil-water interface and AOB abundance is significantly enhanced in the rice rhizosphere (Briones et al. 2002). Using fluorescence in situ hybridization (FISH) with rRNA-targeted probes specific for the AOB to characterize AOB populations in the rhizosphere and on the rice root surface, Briones et al. (2002) reported differences in the total abundance and species composition of the rhizoplane microbial communities across cultivars (Table 1). The greater abundance of the faster-growing Nitrosomonas spp. can be partially attributed to the increased secretion of O2 by cv IR63087-1-17 compared to cv. Mahsuri (Briones et al. 2002). Shifts in the dominant AOB population were accompanied by greater abundance of heterotrophic bacteria in the rhizoplane of cv. Mashuri suggesting that other factors such as differences in root exudates and N dynamics (i.e. NH4+ assimilation by the plants and heterotrophs in the rhizosphere) may also contribute to the observed distributions of AOB species and nitrification rates (Briones et al. 2003). This case establishes the potential for deliberate management of biogeochemical processes through cultivar-microbe interactions while also illustrating the complexities involved in manipulating rhizosphere function.
	Finally, another area of interest from the standpoint of agriculture addresses the question of whether or not there are non-obligate, root-associated microorganisms that are endemic to the rhizosphere of particular plant species and the extent to which crops can modify these populations. Resolving this question could contribute to the development of breeding strategies that target crops and their associated microorganisms. The evidence that both interspecific and intraspecific composition of rhizophere associated assemblages are tightly coupled to the host plant genotype is increasing (Schloter et al. 2000; Mazzola et al. 2004). Wheat offers a particularly interesting system for consideration of this question since it is one of the oldest agricultural plants and is currently cultivated across a wide variety of climates and soil types. A number of microorganisms have consistently been found in rhizospheres of wheat growing in geographically dispersed soils from diverse environments (Schloter et al. 2000; Mazzola 2004). Paenibacillus polymyxa is a free-living N-fixer that has been found in the wheat rhizosphere in North America (Nelson et al. 1976), Europe (Heulin et al. 1994) and Africa (Guemouri-Athmani et al. 2000) and the rhizosphere populations of this organism appear to be adapted to the wheat rhizosphere (Guemouri-Athmani et al. 2000). One study conducted in Algerian soils that had been under wheat cultivation from 5- 2000 years, showed that the genetic composition of Paenibacillus polymyxa populations varied across the chronosequence (Guemouri-Athmani et al. 2000). The longevity of wheat cultivation was correlated with decreased phenotypic and genetic diversity and higher frequency of N-fixing strains of P. polymyxa in rhizosphere-associated soil. The rhizosphere assemblage consisting of the wheat pathogen Gaeumannomyces graminis var. tritici and the populations of 2,4 DAPH producing Pseudomonas spp. antagonists is also found in the wheat rhizosphere in widely distributed geographic locations (Mazzola 2004). These examples, while rather limited, demonstrate similarities in rhizosphere assemblages when plants of the same species are gown in a broad range of environments and supports the idea that plant genotype is the major driver influencing the formation of unique rhizosphere assemblages.  
The coupling between both inter- and intraspecific genetic diversity of plants and their associated rhizosphere organisms, provides support for the extended phenotype concept (Dawkins 1982). This idea that a single, dominant species can influence community-scale evolutionary processes may be important in some ecosystems has been supported by recent studies of intraspecific genetic variability in plants and their associated aboveground arthropods (Whitham et al. 2003; Johnson and Agrawal 2005) and may also a useful concept to apply to agricultural systems where monocultures are the norm. Further understanding of evolutionary mechanisms governing rhizosphere populations and plant-microbial interactions will be crucial in the development of crop breeding strategies that target processes occurring in the rhizosphere. 
IV.  The future of the rhizosphere in ecological agriculture
	The management of biocomplexity to promote ecological processes and restoration of agroecosystem function will require the development and application of ecosystem-based management strategies. Ecosystem management is a land-management approach that 1) takes into account the full suite of organisms and ecosystem processes, 2) applies the concept that ecosystem function depends on ecosystem structure and diversity, 3) recognizes that ecosystems are spatially and temporally dynamic and 4) includes sustainability as a primary goal (Dale et al. 2000). Application of this approach will require that we redirect management practices to create a soil environment that is more conducive to supporting potential contributions from rhizosphere processes. Opportunities to redirect management include changes in the way we approach cultivar selection, repopulating annual systems with plants in space and time and integration of rotation, tillage and soil amendment practices. 
J.  Selection for plant-microbe consortia
	We see many opportunities for plant breeding to enhance plant-microbial interactions in ways that contribute to restored ecosystem functions. First, the traditional breeding framework views plants as single organisms, and as a result, selection of crops and mutualists is often conducted separately. This book supports the notion that plants are more accurately viewed as a consortium consisting of a primary producer and many species of associated microbes (or depending on your bias, microorganisms and their associated plants!). Agricultural breeding programs should select for well-adapted consortia that can achieve necessary levels of primary productivity while maintaining ecosystem services through optimization of plant-microbial collaborations. Second, crop breeding is typically conducted in environmental backgrounds receiving high levels of inputs, sometimes even greater than is economically viable for farmers (Boyer 1982). This has led to the selection of cultivars that are high yielding and dependent on these inputs. Breeding programs that select for plant consortia under in reduced input environments where internal ecosystem processes are enhanced will result in biotic assemblages which are adapted to these conditions.
	Limited efforts have applied interdisciplinary approaches to crop breeding that combine plant selection for multiple traits (including those related to belowground functions) with use of reduced input environments (Banziger and Cooper 2001; and Alves et al. 2003). A successful example of this approach is the soybean breeding program in Brazil where N fertilizers have been omitted from the soybean breeding programs since the 1960's (reviewed by Alves et al. 2003). More efficient Bradyrhizobium strains that support higher levels of biological nitrogen fixation (BNF) through the symbiosis were introduced and at first failed to compete against indigenous strains for nodule space (Nishi et al. 1996). Over ten years as these strains adapted to the soil environment, a few of the introduced strains developed improved competitive ability against less efficient indigenous strains for nodule space. One of these strains is now commonly used in the surrounding region as an inoculant in soybean. This observation suggests that selecting for desired plant traits under appropriate environmental conditions (in this case, improved N-fixing mutualism selected for under conditions of low soil N) has cascading effects on symbiont populations and selects for plant-microbial associations that function well in agricultural systems.  
	For the most part, selecting for cash crop species that are well-suited for ecologically complex production systems will require that yield-related traits (quantity and quality of harvestable crop) continue to be of primary importance while selection for specific rhizosphere functions serves a supporting role.  In contrast, rhizosphere function can serve as a primary trait in breeding for cover crops which support specific ecosystem services that are mediated by plant-microbial interaction in the rhizosphere. We believe that the development of plant-microbial consortia that can enhance specific ecosystem processes such as aggregation, nutrient bioavailability and retention, disease suppression and C storage is a reasonable goal.
K.  Using increased plant species biodiversity in space and time
	Plant species diversity can be increased either by introducing additional cash crops or non-cash crops (hereafter referred to auxiliary crops, cover crops or intercrops) selected to serve specific ecosystem functions. The benefits of management practices that expand plant presence in space and time have long been recognized (Hambridge 1938). Given the current understanding of belowground plant functions, intentional management of plant diversity based on the capacity of a species to enhance particular ecosystem processes is clearly feasible. Indeed, the potential for a single plant species and its associated microbes to significantly influence ecosystem function is large in agroecosystems since single species effects tend to be more pronounced in ecosystems with limited biodiversity (Chapin et al. 2000), particularly when a missing functional group is added (Naeem and Li 1997). 
	The prospect of increasing rotational diversity and replacing bare fallows with cover crops is generally deemed impractical mainly due to concerns about yield reductions, and the bulk of research evaluating diversified rotations has focused solely on yield assessments (Tonitto et al. 2006). There are several recent examples in which assessment expands to include the potential contributions of cover crops to a wide range of belowground agroecosystem services including aggregation (Haynes and Beare 1997), creation of biopores in compacted soils (Williams and Wiel 2004), P bioavailability (Oberson et al. 1999), disease suppression (Mazzola 2004) and N use efficiency (Tonitto et al. 2006). A recent meta-analysis of the cover crop literature suggests that yield penalties have been over emphasized in the past (Tonitto et al. 2006). Yields in diversified rotations employing cover crops varied from no detectable yield reductions to an average yield reduction of 10% in studies where corn was grown following a leguminous cover crop without added fertilizer N. Nitrate leaching, which was the only ecosystem service that had been sufficiently studied to include in the meta-analysis, was reduced by 70% on average. Further assessments of cropping systems where restored plant diversity replaces conventional inputs to provide ecosystem services are needed. Identifying a wider variety of species as well as modifying current cover crop species through breeding programs to fill particular niches could also greatly increase the potential for cover crop adoption and expand contributions from rhizosphere processes. 
L. Integrated plant and amendment strategies
	Ecosystem-based approaches to soil fertility management targeting soil nutrient reservoirs with longer mean residence times that can be accessed by plants and their associated microbes has the potential to build soil productivity over time (Drinkwater and Snapp 2005). Integrated management of biogeochemical processes that regulate the cycling of nutrients and carbon, combined with increased reservoirs more readily retained in the soil, will greatly reduce the need for surplus nutrient additions in agriculture. This approach relies on numerous rhizosphere processes, and combines the use of organic amendments and small amounts of inorganic nutrients from sparingly soluble sources such as rock phosphate with inclusion of plant consortia that can access these sources. Greater understanding of the ecology and evolution of the microbial loop in the rhizosphere will be crucial to coupling N-mineralization with plant uptake so that N losses and plant-microbial competition for N are minimized. 
	Strategies need to be developed that combine P application with assimilation in biological sinks, through management and integration of species that augment levels of soil organic acids and phosphates. Application of sparingly-soluble sources of P to crops (e.g., most legumes) that can assimilate P into biological pools is an efficient strategy that has been underappreciated, and could be used to bypass desorption, precipitation and occlusion of P (Vance et al. 2003). Legumes are important vehicles to enhance P availability through diverse mechanisms, including modified roots, secretion of organic acids and enhanced P-solubilizing activity through microorganisms (Oberson et al. 1999). Similarly, targeted use of animal manures can facilitate plant and microbial uptake of P and enhance crop access to P (Erich et al. 2002). Manipulation of mycorrhizal populations to develop more efficient plant-symbiont combinations is in its infancy, but strategies that can be pursued include use of sparingly-soluble rock P, reduced tillage and integration of auxiliary plants that are highly mycorrhizal.
Conclusions
	Throughout this chapter we have emphasized interactions between the managed soil environment and the biota inhabiting plant-associated niches. Improved ecosystem-based strategies will require an understanding of the feedbacks among management, rhizosphere communities and the background soil environment at longer-temporal scales than current investigations tend to encompass. In particular, future research must address feedbacks between abiotic conditions and ecological and evolutionary processes that govern rhizosphere community structure and function. We believe that adoption of the ecosystem as a conceptual model will guide future research in these directions.
	We recognize that ultimately the transition to ecologically-sound, sustainable food production systems that meet human needs will be complex and will require fundamental changes in cultural values and human societies (Boyden 2004) as well as the application of ecological knowledge to agricultural management. It is our hope that application of current ecological understanding to the design of agricultural systems will provide the scientific know-how to promote the transition to sustainable food systems that supply a wide range of necessary ecosystem services. We believe there is a tremendous untapped potential for subterranean ecological processes to contribute to these sustainable food systems.

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Figure Legends
Figure 1.  Variation in management intensity and consequences for the rhizosphere.  Agricultural management systems are distinguished by the reliance on agrochemical inputs (fertilizers, pesticides, other agrochemicals) and tillage intensity. As the level of input dependance is reduced, the reliance on plant functional diversity generally increases as does the extent of the rhizosphere in space and time. Reduced dependence on tillage for annual crops (no-till) and perennial systems (pastures, agroforestry) are closest to unmanaged ecosystems in terms of soil physical environment and the presence of rhizosphere remnants as such as intact networks of root and hyphal pores (Williams and Weil 2004).  Conventional production systems rely on high inputs and intensive tillage.  Integrated pest management aims to substitute cultural practices and managed biodiversity for pesticides and has become a standard approach to managing insecticides efficiently in many cropping systems (Lewis et al. 1997).  Pesticide-free agriculture is a grower-initiated approach largely oriented toward filling consumer demand for foods that are free of pesticides (Ott 1990).  Integrated or low input systems combine agrochemical use with ecological or organic practices with the goal of reducing environmental impacts while achieving high yields (Reganold et al. 2001). Organic agriculture is the dominant from of ecologically-based food production in the US and seeks to minimize external inputs while avoiding all synthetic agrochemicals (National Organic Program 2005). Ecological and biodynamic systems originated in Europe and have an increased requirement for internalized N-fixation compared to US certified organic (International Federation of Organic Agricultural Movements 2005). 

Figure 2. Paired minirhizotron images showing roots of a canola cover crop (left) in compacted plowpan soil (spring) and soybean roots (right) observed at the same locations in the soil a few months later.  The roots can be seen to follow channels made by the preceding canola roots (after Williams and Weil 2004; with permission).

Figure 3. Rhizosphere processes contribute to a variety of ecosystem functions and services and are the outcome of plant-microbial collaborations. Some, such as and soil retention are strongly governed by plant species and others such as nitrification are largely controlled by microorganisms. 

Table 1. Comparison of rice cultivars, their rhizosphere composition and biogeochemical function (from Briones et al. 2002, 2003).

	Improved traditional	Modern hybrid	
Cultivar	 Mahsuri	IR63087-1-17	
Fertilizer use efficiency	Able to use either NH4 or NO3	Greater efficiency with NH4 application	
Rhizosphere environment	Roots are less permeable to O2	Roots leak more O2	
Rhizosphere community composition(1)               	Rhizoplane is dominated by heterotrophs	Heterotrophs may be less abundant compared to Mahsuri rhizoplane	
Most abundant ammonia oxidizing bacteria	Nitrosopira sp. (Able to grow at lower substrate concentrations, K strategist)	Nitrosomonas sp. (Fast growing, R strategist)	
Nitrogen cycling(2)	Nitrification is not detectable	Nitrification rate: 1.2 ug N g soil day-1	

(1)Detection and characterization of ammonia-oxidizing bacteria by PCR-DGGE targeting the amoA gene. Quantification of AOB in rhizosphere and rhizoplane was based on FISH.

(2)Based on in situ field experiments using the 15N pool dilution method.