Managing soil microorganisms to improve productivity of agro-ecosystems

Critical Reviews in Plant Sciences, 23(2):175–193 (2004)Copyright C© Taylor and Francis Inc.ISSN: 0735-2689DOI: 10.1080/07352680490433295

Managing Soil Microorganisms to Improve Productivityof Agro-Ecosystems

Gregory E. WelbaumDepartment of Horticulture, Virginia Polytechnic Institute and State University, Saunders Hall,Blacksburg, VA 24061, USA

Antony V. SturzPEI Department of Agriculture & Forestry, Charlottetown, Prince Edward Island, Canada C1A 7N3

Zhongmin DongDepartment of Biology, Saint Mary’s University, Halifax, Nova Scotia, Canada B3H 3C3

Jerzy Nowak∗Department of Horticulture, Virginia Polytechnic Institute and State University, Saunders Hall,Blacksburg, VA 24061, USA

Referee: Dr. Paul C. Struik, Crop & Weed Ecology, Wageningen University, Bodenumber 71, Bornsesteeg 47, 6708 PD Wageningen,The Netherlands

Table of Contents

I. INTRODUCTION .............................................................................................................................................. 176A. Overview ...................................................................................................................................................... 176B. Some Definitions ........................................................................................................................................... 176

II. SOIL AGRO-ECOSYSTEM AND MICROBIAL COMMUNITIES .................................................................... 177A. Soil Microbial Diversity and Functionality ....................................................................................................... 177B. Plant-Engineered Root Zone Communities ...................................................................................................... 177C. Beneficial and Detrimental Microbial Allelopathies ......................................................................................... 178

III. NITROGEN-FIXING AND HYDROGEN-GAS–OXIDIZING BACTERIA ......................................................... 178A. Nitrogen-Fixing Bacteria in Soil ..................................................................................................................... 178B. Hydrogen-Gas–Utilizing Bacteria in the Rhizosphere ....................................................................................... 179

IV. SOIL AGRO-ECOSYSTEM MANAGEMENT ................................................................................................... 180A. Tillage Effects ............................................................................................................................................... 180B. Bacterial Endophytes and Crop Rotations ........................................................................................................ 180C. Soil Ethylene and Crop Development .............................................................................................................. 180D. Feeding Soil Microbes ................................................................................................................................... 181

V. PRECISION MANAGEMENT OF A SUSTAINABLE AGRO-ECOSYSTEM—PROGRESS AND FUTURE ...... 183A. Plant–Microbial Ecosystems ........................................................................................................................... 184B. Soil Priming .................................................................................................................................................. 184C. Biopriming Plant Propagules .......................................................................................................................... 185D. “Microbial Precision” Production Systems: The Development of the “Smart Field” Concept ................................ 185

REFERENCES .......................................................................................................................................................... 186

∗Corresponding author: Department of Horticulture, Saunders Hall (0327), Virginia Polytechnic Institute and State University, Blacksburg,VA 24060, USA. E-mail: [email protected]

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176 G. E. WELBAUM ET AL.

Historically, agricultural production has relied on practices de-signed to manage nutrients, water, weeds, and crop diseases. Pre-cision agriculture and integrated pest management programs havegone one step further by recognizing the need to target inputs wherethey are required in the field. The major objective of these programshas been to minimize adverse environmental impacts of intensiveagriculture practices and reduce per unit production costs. Thisreview surveys the literature, examining the manipulation of mi-crobial (primarily bacterial) populations as linked to agriculturalproduction, and discusses new approaches that involve the pre-cision management of microorganisms in the agro-ecosystem. Itis proposed that our understanding of plant–soil interactions canbe greatly refined through the development of “smart” field tech-nology, where real-time, computer-controlled electronic diagnosticdevices can be used to monitor rhizosphere and plant health. Wesubmit that “smart field” generated information could be used todevelop a prescription for timely and low-level production interven-tions that will avoid the traditional inundative approaches to cropmaintenance and soil husbandry. Consequently, a lesser impact onthe agricultural soil environment is envisioned. The maximizationof production efficiencies will also involve the development of cropcultivars that are bred specifically to capitalize on beneficial plant–microbial associations.

Keywords soil microbial communities, diversity, management,plant-microbial interaction, feeding microbes

I. INTRODUCTION

The times have changed; the face of the country is changed; thequality of the soil has changed; and if we will live as well, and becomeas rich and respectable as our fathers, we must cultivate their virtues;but abandon their farming system.

- The Farmers Manual (1819)

A. OverviewMismanaging soil health and fertility is not a prerogative of

twenty first century agriculture. In the early part of the nineteenthcentury commentators had already noticed the occurrence of soilexhaustion and fertility loss, the consequences of overworkingfarmland and a general failure to manage nutrient flow correctly(Spafford, 1812).

Unfortunately, the choice between soil improvement or aban-donment usually resulted in the latter course, with settlers mov-ing on to clear new land and repeat the same managementmistakes, and reap the inevitable consequences. As a result,the pattern of American land colonization throughout the nine-teenth century was one of eastern farmers pushing west, leavingin their wake a ruined rural landscape, stripped of its forests anddepleted of its fertile topsoil (Strickland, 1801). Accordingly,one of the most intractable problems in American agriculture inthe 1800s became managing the relationship between yields andsoil nutrient balance. For although farmers understood that fer-tility could be taken away, few understood the best methods forreturning it.

In his treatise on the history of soil regeneration practices inearly America, Stoll (2002) outlines a number of the systems

that more enlightened farmers used to conserve and improvetheir soils, maintain tilth, and increase productivity. This wasnot new knowledge; pioneers in land experimentation had theirroots in Great Britain, where Jethro Tull’s The Horse-HoeingHusbandry (1733) promoted what today might be described asa system of sustainable soil management.

Such calls to farming practices, which espoused the main-tenance or improvement of the land base, were taken up bysuccessive sets of producers who praised the benefits of soilconditioning based on “closed” nutrient cycles and soil micro-bial rejuvenation. These practices were principally the result ofreincorporating into farmland carefully mixed manure prepara-tions as a standard part of their land husbandry practice.

During the aftermath of World War II the recognition offood as a strategic resource led to the drive for national secu-rity through self-sufficiency in food production and the ascen-dancy of agrichemical systems of crop production. Chemicalfertilizers came to supplant organic farming systems and the“natural” accumulation of soil nutrients and soil microflora thatproduced them. Newly developed classes of plant cultivars be-came increasingly reliant upon the support of agrichemistry. Atthe same time, the yield potential of agricultural soils began todecline as the biological processes that maintained their healthand quality became overtaxed (Greenland and Szabolcs, 1994;Pankhurst et al., 1997). Accordingly, an environmental price waspaid for a food security system based upon technological andagrichemical innovation and the exploitation of nonrenewableenergy reserves. Most notably, in the 1970s, 1980s, and 1990s thescientific literature became filled with reports of “soil-fatigue,”“soil degradation,” and “soil loss.”

B. Some DefinitionsDespite its importance, it is only relatively recently that mi-

crobial ecologists have begun to consider those complex interac-tions between plants and the microbial components in soil thatsustain them. And while the physical and biological benefitsof manures and composts have been quantified (Brady, 1974;Hoitink and Boehm, 1999), the microbial mechanisms that un-derpin their effectiveness are still little understood. Similarly,relatively little is known about the processes that maintain “soilquality,” “soil resilience,” and “soil health,” or that conserve “soilstability” above and beyond the application of chemical fertil-izers and certain well-established systems of crop rotation andresidue management.

In the general context of this review, we define soil quality interms of its “suitability for chosen uses” (Warkentin and Fletcher,1977), usually for the purpose of sustaining plant and animalproductivity to support human health and habitation (Sparling,1997). Soil health, by contrast, is understood to be the com-petence with which soil functional processes (e.g., nutrient cy-cling, energy flow) are able to support viable, self-sustaining(micro)faunal and (micro)floral ecosystems that make up a “liv-ing soil” (O’Neill, 1991, p. 39). Soil stability relates to struc-tural integrity and describes the capacity of “soil to retain its

MANAGING SOIL MICROBES 177

arrangement of solid and void space when exposed to differentstresses” (Kay, 1990). We define soil resilience as the capa-bility of a soil (population or system) to return to its preper-turbation condition, as opposed to any intrinsic capacity to re-sist displacement from that initial equilibrium state (Eswaran,1994).

Though it is often considered that soil microbes play a keyrole in soil quality and health (Pankhurst et al., 1997; Karlenet al., 1997; Vessey, 2003), a general dearth of information ex-ists when it comes to categorizing the assembly of species thatassure soil fertility, the critical forces that govern their com-munity structure and function. What has become clear is thatthe interaction between root zone microflora and plants involvesa continuum of colonization events that are initiated at seedgermination and traverse the rhizosphere to the rhizoplane, tothe endoroot via the root epidermis and apoplast, directly to theshoots (Petersen et al., 1981; Kloepper et al.,1992; Van Bruggenet al., 2002). Consequently, phyto-microbial relationships canbecome extremely intimate, extending over the life-cycle andgrowth habit of the plant, and involving both exo- and endo-plant environments (Wardle, 2002). In this review we focus onmethods to create sustainable agro-ecosystems of crop produc-tion through the selective management of phyto-microflora.

II. SOIL AGRO-ECOSYSTEM AND MICROBIALCOMMUNITIES

A. Soil Microbial Diversity and FunctionalityIt is still unclear whether (bacterial) species diversity is, as

is often proposed, critical to the integrity and long-term sustain-ability of soil ecosystems (Altieri, 1995; Pankhurst et al., 1996;Wardle, 2002), or if it is merely evidence of a built-in “func-tional redundance” (Bianchi and Bianchi, 1995; Bardgett andShine, 1999). The extent to which species diversity and asso-ciated metabolic versatility within the soil community is in ex-cess of that required for ecosystem maintenance and functionalstability—in response to perturbation—remains an unresolvedquestion (Pankhurst, 1994).

While several studies have shown that a reduction in species-abundance relationships—measured, for example, by speciesrichness (total species) and species evenness (defined by the rel-ative frequency within a community)—can precede decliningecosystem processes (Naeem et al., 1995; Knops et al., 1999;Wilsey and Potvin, 2000), there is little conclusive evidence tosupport the hypothesis that ecosystem function depends uponthe “full complement of diversity within sites” (Schwartz et al.,2000). Accordingly, the importance of biodiversity in determin-ing ecosystem stability and resilience remains a matter of debate(see reviews by Chapin et al., 2000; Pimm, 1984; Waide et al.,1999). This is especially so in the microbial sciences, wherestudies of biodiversity can often become confounded by diffi-culties associated with the recovery and identification of suitabletaxonomic units necessary to describe species (O’Donnell et al.,1994; Pankhurst et al., 1996).

Part of the difficulty in resolving soil microbial communitystructure is our limited ability to examine soil ecosystems in realtime. The current trend of community-based analysis using PCRextraction does provide a new insight into the enormous diversityof bacterial strains in the soil environment (Kent and Triplett,2002). However, these techniques are not without their limita-tions (Niemi et al., 2001; Wilson et al., 1997; Sessitsch et al.,2002). As a result, only a fraction of that continuum of popula-tion events is captured in time (season) and space (root zone),and this for a restricted number of taxonomic units (species).Consequently, total species diversity can often appear to remainconstant, when in effect a continuous process (e.g., organic mat-ter decomposition) is occurring, driven by the sequential colo-nization of consortia of niche specialists that utilize the differ-ent substrates that present themselves over time (Walker, 1992).Thus, a duality in community variability occurs, namely thatof changes in compositional variability (relative abundance ofcomponent species) juxtaposed with that of aggregate variability(those changes involving total properties as overall abundance,biomass, and or production; Micheli et al., 1999).

The stability of populations at any given microsite, the rate ofturnover of species within an ecosystem, and the accumulationof biological diversity over time, if any, is subject to a number ofrate-governing variables, the degree and direction of which re-main largely unpredictable (Swift and Anderson, 1993; Lawton,1994; Micheli et al., 1999). Ecologists have long suggested thatenvironmental perturbations will increase the variability of eco-logical systems (Odum et al., 1979; Underwood, 1991). Whetherthis variability leads to increasing species diversity—thus pro-moting increased productivity and stability within ecosystems—becomes the basis for an interesting discussion (Cottinghamet al., 2000; Johnson et al., 1996; Kennedy and Smith, 1995;Naeem and Li, 1997).

B. Plant-Engineered Root Zone CommunitiesWhile it is a truism that soil agro-ecosystems are extremely

complex, the plant root system is a rationalizing force that im-poses a class of order on the chaos that is functional agriculturalsoil. The vast surface area provided by roots is an extraordinarilydiverse habitat for a huge assortment of microorganisms rangingfrom transient epiphytic saprophytes to epiphytic commensals,mutualistic symbionts, endophytes, and pathogens.

The biogeography of the habitats comprising the root systemare defined by physical and chemical characteristics such asincreased exposure to light, water, aeration, plant photosynthateleakage, root architecture, and root longetivity (Andrews andHarris, 2000; McCully, 1999). However, it is primarily throughthe general release of carbon-rich material in the form of rootborder cells (Hawes and Brigham, 1992; Hawes et al., 1998),or alternatively via the selective exudation of specific sugars,carboxylic, and amino acids (Grayston et al., 1998; Jaeger et al.,1999; Siciliano et al., 1998; Lugtenberg, 2001; Ryan et al., 2001)that plants are able to “load-up” the root zone environment withsubstrates that encourage the development of cultivar-specific,


plant-beneficial, microbial communities (Chanway et al., 1988;Lugtenberg, 2001).

This is by no means a one-way process, and plant “en-gineered” rhizomicrobial communities can likewise initiatechanges in the root biochemistry (Darrah, 1993; Hinsinger,1998; Parmar and Dardarwal, 1999; Lugtenberg, 2001; Pattenand Glick, 2002; Vessey, 2003), inducing a root exudation re-sponse in the host plants that fostered them (Bolton et al., 1993;Merharg and Killham, 1995). Thus root growth leads to substrateloading in the root zone, which in turn promotes rhizobacte-rial proliferation, leading to further root growth, a concomitantincrease in root exudation that leads to substrate loading, andso on.

All such root–microbial exchanges can be considered a formof allelopathy (Barazani and Friedman, 1999) and include thosebiochemical interactions, both inter- and intraspecifically, thatinvolve microbial- or plant-produced secondary metabolites (al-lelochemicals) that influence growth and development of bi-ological systems in the soil. Consequently, phyto-microbiallygoverned plant growth is a form of beneficial allelochemical re-sponse that shares many of the characteristics of a “feedback”system. The plant initiates an allelopathic cascade of which itis also the final recipient. An analogous process can be foundin autotoxicity, where phytochemical autoinhibitors collect inthe root zone and inhibit same or nonsame species’ growth anddevelopment (Singh et al., 1999).

Since this can involve ecological phenomena at the trophiclevel (Romeo, 2000), such allelopathic events will, by default,be involved in the regulation of ecosystem health and biodiver-sity (Wardle et al., 1998; Malik, 2000). Availability of substratedetermines reversible transition between active and dormant mi-crobial states and differentially affects microbial communitystructure (Stenstrom et al., 2001). Understanding these changes,both in the root zone and in the top- and subsoil, becomes criti-cal to soil health and fertility management in a sustainable soilagro-ecosystem (Taylor et al., 2002).

C. Beneficial and Detrimental Microbial AllelopathiesThe term allelopathy was originally introduced to describe

the injurious effects of one plant upon the other (Molisch, 1937).However, the term has now been generally accepted to includeboth inhibitory and stimulatory effects, and the definition hasbeen extended to include “any process involving secondarymetabolites produced by plants, microorganisms, viruses andfungi that influence the growth and development of agriculturaland biological systems (excluding animals), including positiveand negative effects” (Torres et al., 1996, p. 278).

As a class of relationship between organisms, allelopathyis considered to be one where no direct contact occurs, theeffect of any interaction being a consequence of some indi-rect event controlled by an allelochemical. Thus in its broad-est sense “plant-directed” microbial communities can providethe host plant with a distinct ecological advantage throughthe cultivation of beneficial allelopathies (Sturz and Christie,

2003). Microbially generated secondary metabolites have beenshown to aid plant growth (Glick et al., 1999; Patten and Glick,2002; Mathesius, 2003), increase availability of minerals andnutrients (Murty and Ladha, 1988; Darrah, 1993; Marschenerand Romheld, 1994; Hinsinger, 1998), improve nitrogen econ-omy (Ladha et al., 1997; Reinhold-Hurek and Hurek, 1998;Yanni et al., 2001), change plant susceptibility to frost dam-age (Xu et al., 1998), enhance plant health through the directbiocontrol of phytopathogens (Weller et al., 2002; Van Bruggenet al., 2002), induce systemic forms of plant disease resistance(Van Loon et al., 1998; van Wees et al., 1999), and secureplant establishment (Lazarovits and Nowak, 1997; Burd et al.,1998).

By contrast, detrimental allelopathies occur where bacte-rially produced secondary metabolites adversely affect plantgrowth and development. These detrimental effects occur inthe absence of any pathogenic symptomology (Schippers et al.,1987; Barazani and Friedman, 2001), although affected plants,in their weakened state, can subsequently become susceptibleto phytopathogen attack (Frederickson and Elliot, 1985). Ac-cordingly, such organisms have been termed deleterious rhi-zosphere microorganisms (DRMO) and include the deleteriousrhizobacteria (DRB).

Notwithstanding the above, the use of functional groupings—beneficial, detrimental, or neutral–are deceptive (Nehl et al.,1996), as microbial–plant effects will vary according to a vari-ety of factors, including: plant developmental age (Pilet et al.,1979), environment (Hassink et al., 1991; Bensalim et al., 1998),host species (Astrom and Gerhardson, 1988; Grayston et al.,1998), and accompanying mycorrhizal status (see review byAzcon-Aguilar and Barea, 1992). Sturz et al. (1997) showedthat bacterial strains, which individually inhibit plant growth,can stimulate plant growth when applied as coinoculants. Sim-ilarly, the order in which bacterial populations form consortiaand become established in the root zone can affect subsequentplant growth responses (Sturz and Christie, 1995).

For a more comprehensive overview of the involvement ofplant and microbial secondary metabolites in ecosystem func-tioning (including allelopathy), please see Hadacek (2002) andBarazani and Friedman (2001).

III. NITROGEN-FIXING ANDHYDROGEN-GAS–OXIDIZING BACTERIA

A. Nitrogen-Fixing Bacteria in SoilThe amount of N present on this planet as dinitrogen is ap-

proximately 4 × 1015 tons in the atmosphere and about 20 timesthat bound in sedimentary and primary rocks beneath the sur-face (Gallon and Chaplin, 1987). None of these sources is ac-cessible to plants until it is fixed, i.e., converted to ammo-nia. Dinitrogen can be fixed by industrial processes (Haber-Bosch process), or biologically, by some prokaryotes. Althoughsignificant amounts of nitrogen are derived from industrialfertilizers, most of the fixed nitrogen present in the world’s


soil and water ecosystems comes from biological N2 fixation(Hernandez, 2002).

Nitrogen-fixing bacteria can be symbiotic, free-living, or as-sociative, forming casual associations with other organisms, i.e.,plants. The associative diazotrophs colonize the rhizosphere andoften enter the root and/or shoot interior, occupying intercellularspaces (the so-called diazotrophic endophytes). Free-living N2

fixers contribute only small amounts of N to plants. SymbioticN2-fixing bacteria can contribute directly to the productivity ofplants at a high rate, while less direct contributions may be madeto the growth of plants by associative bacteria. Although theirnitrogen contribution is minuscule, the associative diazotrophsenhance plant growth (Sevilla et al., 2001; Baldani et al., 2000;Bastian et al., 1999; Jacoud et al., 1998; Hurek et al., 2002;Dobbelaere et al., 2003). These results have encouraged a waveof investigations into associative endophytic diazotrophs in non-legume plants (Riggs et al., 2002).

The rhizobia–legume symbiotic relationship is the mostwidely studied and utilized of plant–microbe interactions(Sprent, 2001). Rhizobia residing inside nodules of legumeplants take N2 from air and reduce it to plant-available nitrogen.The host plant develops nodule structure, regulates O2 tension,and provides organic carbon to the bacteria, while the bacteriaprovide the plant with the nitrogen it needs. Moreover, nonsym-biotic/associative N-fixing bacteria normally live in the rhizo-sphere, where they can exchange fixed nitrogen with the plant fororganic carbon. In this system, microbial populations respondto plant exudates, and plant exudation follows from microbialactivity in the rhizosphere.

The organic carbon exuded from plant roots into the rhizo-sphere promotes microbial population development around theroots. Studies have shown that root exudation is positively re-lated to soil inorganic N pool, its subsequent uptake by plantsand its final accumulation in leaves (Hamilton and Frank, 2001).Although no N fixation was shown in that study, it was clearlydemonstrated that plants were capable of promoting soil micro-bial populations through nutrient delivery, especially nitrogennutrient supply. Direct soil deposition of plant-derived nitro-gen, including rhizodeposits (decaying roots), functions as asource of nutrients for the surrounding bacteria (Høgh-Jensenand Schjoerring, 2001). Retaining crop residues increase thenumber of N-fixing bacteria in soil by a factor of 100 and theiractivity by more than 10 (Roper, 1983). For a detailed overviewof the nitrogen fixation by the associative diazotrophs, and rootexudation, see the review by Jones et al. (2003).

B. Hydrogen-Gas–Utilizing Bacteria in the RhizosphereIt is well known that intercropping legumes with nonlegumes,

or crop rotation involving legumes and nonlegumes, can leadto significant increases in the growth and yield in the non-legume crop. However, only about 25% of the increase inthe growth of the nonlegume crop can be attributed to im-proved N nutrition. The remaining 75% of the effect have

eluded explanation (Bolton et al., 1976; Hesterman et al., 1986;Fyson and Oaks, 1990; Zanetti et al., 1996; Høgh-Jensen andSchjoerring, 2001). Recent studies showed that the H2 producedas a by-product of N2 fixation by legume nodules is responsi-ble for a substantial portion of the growth- or yield-enhancingeffects of legume soils. Antibiotic and/or fungicide treatmentshave demonstrated that the H2 uptake and plant growth promo-tion effects were both bacterial in nature (McLearn and Dong,2002; Irvine et al., 2003).

Hydrogen gas is a byproduct of the N2-fixing enzyme nitroge-nase, claiming about 33% of the energy that flows to the enzyme(the other 67% is used to reduce N2) (Hunt and Layzell, 1993). Inmost free-living diazotrophs and some symbioses, the bacteriaalso produce an enzyme called an uptake hydrogenase (HUP),which is able to oxidize the H2 and thereby extract chemicalenergy from it. However, many legume symbioses, includingmost of the rhizobia used in agricultural production, lack thisuptake hydrogenase (Uratsu et al., 1982). Thus the H2 producedby the nitrogenase diffuses out of the nodule into the soil. TheH2 production represents an energy source equivalent to 5 to7% of the crop’s net photosynthesis (Dong and Layzell, 2001).This H2 loss from nodule to soil is traditionally believed to bea disadvantage of HUP− over HUP+. But the evolutionary pro-cess, plant breeding of agricultural crops, or selection of optimalN2-fixing bacteria have not reduced this energy loss in legumes.This leads to the hypothesis that H2 released by legume nodulesmay change the soil fertility directly to the benefit of the plant.

The H2 released is rapidly oxidized by soil microorgan-isms within a few centimeters of the legume nodules (La Favreand Focht, 1983), resulting in an increase in rhizobial biomass(Popelier et al., 1985), and greater rates of O2 consumption andchemoautolithotrophic CO2 fixation (Dong and Layzell, 2001).A recent study showed that this H2 uptake in H2-treated soilsand soil around HUP− nodules is promoted by bacterial activity(McLearn and Dong, 2002). Since the H2 released by nodules isoxidized by bacteria in the adjacent soils, it has been proposedthat the soil microfloral community structure is changed by theH2 released into the soil, and this microbial alteration influencesplant growth. Plant growth studies showed that H2-treated soilpromoted soybean, barley, and canola growth by 10 to 20, andspring wheat by 20 to 30% (Dong and Layzell, 2002). Theseexperiments indicate that a considerable amount of energy istransferred to the rhizosphere microbial population in a HUP−

legume field in the form of H2, and in return the energy-enrichedsoils promote plant growth. These discoveries could help to ac-count for the beneficial effects of legumes used in rotations withcereals and other crops. We can speculate that H2 produced asa by-product of N2 fixation in legumes enhances certain micro-bial populations in soil and improves the growth and yield ofthe subsequent crop. This hypothesis would also account forthe evolutionary questions surrounding why HUP− symbioseshave thrived when there are genes (in many cases within thesame genus and species) for the more energetically efficientHUP+ symbioses (Uratsu et al., 1982). Perhaps the plant growth


advantages of the HUP− symbioses offset the greater energy ef-ficiency of the HUP+ symbioses.

IV. SOIL AGRO-ECOSYSTEM MANAGEMENT

A. Tillage EffectsThe use of tillage techniques in seed bed preparation and land

use management not only impose a physical stress on the soilstructure but also on the soil microbial communities that inhabitthat soil (Doran and Linn, 1994; Elliot and Stott, 1997). In aneffort to minimize such stresses, modern arable farming systemsare attempting to reduce excessive cultivation in favor of limitedor strategic tillage practices (Masse et al., 1994).

Here we define a conventional tillage system as a prelimi-nary deep primary operation followed by some secondary tillagesystem for seedbed preparation (Soil Conservation Society ofAmerica, 1976). In contrast, conservation, or reduced tillage,can encompass any tillage practice that reduces loss of soil andwater as compared to unridged or clean tillage. This can include(1) minimum tillage, considered to be the minimum amount oftillage required for seed bed preparation and plant establish-ment; (2) notillage/zero tillage/direct drilling, which involvesno seedbed preparation other than chemical preparation and soilopening for seed placement (Baeumer and Bakerman, 1973);and (3) high-residue mulched beds (Morse, 1999, 2000)

Compared to conventional tillage systems, reduced-tillagepractices offer not only long-term benefits from soil stability,reduced soil erosion, and sustainable agriculture (Anderson andGregorich, 1983; Lal, 1991; Larson and Pierce, 1991), but theycan also enhance soil microbial diversity (Davis et al., 2002;Hassink et al., 1991; Lupwayi et al., 1998; Magdoff and vanEs, 2000; Phatak, 1998; Phatak et al., 2002; Wander et al.,1995). Thus, minimizing the mechanical upheaval associatedwith tillage operations tends to maximize soil microbial diver-sity because the disruption of food substrate at the trophic level,desiccation and soil compaction are reduced, and optimum porevolume is maintained (Giller, 1996).

Paradoxically, fallow periods in a crop rotation can reducesoil microbial diversity (Zelles et al., 1992), an effect proba-bly associated with food substrate depletion over time. Thus,heterogeneity in soil microbial populations tends to coincidewith heterogeneity of food resources, which is often greatest incrops under conservation or zero tillage management, where theresidue of the preceding year’s crops adds sequentially to thevariety of food substrates available for utilization.

Clearly, while the act of mixing soil during tillage increasesseedbed homogeneity, it will simultaneously destroy the diver-sity of trophic microsites that occur down the soil profile togetherwith the assemblages of soil microorganisms that occupy them.The result is a reduction in both the structural and functional di-versity of the soil microbial community (Beare et al., 1995) andthe efficiency of those microbially mediated processes that sus-tain the agricultural productivity of soils, e.g., nutrient recycling,degradation of toxic residues, maintenance of soil structure, andaggregation (Sparling, 1997).

For a recent overview of the soil-borne disease managementapproaches under a direct seeding system (no till), see Paulitzet al. (2002).

B. Bacterial Endophytes and Crop RotationsA continuous apoplastic pathway exits from the root epi-

dermis to the shoot, which appears sufficient for movement ofmicroorganisms from the root cortex into the xylem and fromthere throughout the plant (Petersen et al., 1981). Consequently,many bacterial endophyte communities are the product of a col-onizing process initiated by rhizobacteria in the root zone. Inthis regard, the plant host offers the microbial endophyte a rela-tively homeostatic, spatially diverse environment that is suitablefor biotrophic mutualists, benign commensals, and necrotrophicpathogens alike (Chanway, 1996: Stone et al., 2000).

Where plant–endophyte populations are complementary, twobroad categories of beneficial effect are found in the literature,namely (1) plant growth promotion (e.g., Frommel et al., 1991,1993; Pillay and Nowak, 1997; Glick et al., 1998, 1999) and(2) disease control based on postinfection pathogen suppression(Benhamou et al., 1996; Sturz et al., 1999). Recently, increasedinterest has been expressed in further defining and exploitingthis relationship (Turner et al., 1993; Hallman et al., 1997;Sturz et al., 2000; Kobayashi and Palumbo, 2000; Lodewyckxet al., 2002; Mathesius, 2003), especially in those situationswhere endophytes are able to mitigate plant responses to en-vironmental stress, such as those found as a result of drought(Nowak et al., 1999), transplantation (Nowak et al., 1995) andheat (Bensalim et al., 1998). However, where plant–endophytepopulations are noncomplementary, inhibitory allelopathic ef-fects can result (Sturz and Christie, 1996).

It soon becomes clear that a fundamental source of potentialendophytes is to be found in the soils and organic debris of previ-ous crop plantings. Thus, by extension, complementarity amongrotation crops will involve a microbial compatibility between thenewly planted crop and the resident autochthonous soil popula-tion. Consequently, it has been proposed that the yield benefitsfrom complementary cropping systems involving, for example,legume rotations—and often attributed solely to residual nitro-gen and improved soil structure—may also include an additionalbenefit from the carryover of the residual populations of endo-phytically competent bacteria able to promote plant growth andinhibit disease development (Sturz et al., 1998). These relation-ships between crops in complementary rotations can be cultivarspecific (Sturz et al., 1999, 2003). Accordingly, crop rotationselection criteria should include an evaluation of the effects ofrhizobacteria and their associated endoplant-competent bacte-rial communities when considering the long-term consequencesof those crop choices, since the benefits to soil health and qualityof such choices are likely to be cumulative.

C. Soil Ethylene and Crop DevelopmentWhile the details and significance of soil ethylene (C2H4)

have only recently become appreciated, some repercussions


have already been recognized. Soil ethylene can affect plantgrowth and is certainly a significant factor in field productionof agricultural crops. Soil is itself a source of ethylene, and theamount generated can vary widely depending on the type and de-gree of soil amendment and other related factors (Smith, 1976a;Arshad and Frankenberger, 1988, 1990a, 1990b, 1990c, 1991;Zechmeister-Boltenstern and Smith, 1998). While both biologi-cal and chemical processes contribute to ethylene accumulationin soil (Arshad and Frankenberger, 2002), most soil ethylene isproduced by microbes.

Interestingly, although all major groups of bacteria, actino-mycetes, fungi, and algae are capable of producing ethylene(Arshad and Frankenberger, 2002; Hodges and Campbell, 1998;Cherneys and Kende, 1996; Osborne et al., 1996), according toSmith and Cook (1974) spore-forming bacteria living in anaer-obic microsites are the primary ethylene producers. However,microbial generation of ethylene varies greatly with soil environ-ment, the nature of substrates present in native soil organic mat-ter, and/or soil amendments (Arshad and Frankenberger, 2002).Smith (1976b) proposed that the “microbial nutrient status” ofsoils could be screened by measuring O2 utilization and CO2 evo-lution and then could be correlated to soil ethylene production.This was recently confirmed by Zechmeister-Boltenstern andSmith (1998) after conducting experiments on six different soils.

In soil, the ethylene “atmosphere” may exceed 10 µl L−1

(Perret and Koblet, 1984; Meek et al., 1983; Campbell andMoreau, 1979; Smith and Dowdell, 1974), sufficiently high tocause physiological changes in plants (Smith, 1976a; Primrose,1979; Arshad and Frankenberger, 1991, 1998; Muromtsev et al.,1995; Bibik et al., 1995; Zahir and Arshad, 1998). As a gaseousplant hormone ethylene can, in very small concentrations, af-fect plant release from dormancy, shoot and root growth anddifferentiation, adventitious root formation, leaf and fruit ab-scission, floral induction, female flower formation, flower andleaf senescence, and fruit ripening, to mention a few of the better-characterized responses.

Consistent with its classification as a secondary metabolite,microbial ethylene may also function as a signaling compoundin plant–microbial interactions—in plant microbial-cross talk(Arshad and Frankenberger, 2002)—and may also play a sig-nificant role in rhizobacteria-mediated induced systemic resis-tance (ISR) in plants against specific pathogens via the jas-monate/ethylene signal-dependent pathway (Ton et al., 2002).Ethylene is involved in the determination of root system mor-phology, plant responses to abiotic and biotic stresses, and de-velopment of legume–rhizobia symbiotic associations (Nayaniet al., 1998; Grichko and Glick, 2001a, 2001b; Penrose andGlick, 2001; Penrose et al., 2001; Ma et al., 2002, 2003; Stearnsand Glick, 2003; Grossman and Hansen, 2001; Ton et al., 2002).It may also affect the rate of root infection by phytopathogensthat produce ethylene during early stages of infection (Whipps,1990).

Besides soil microorganisms, plant roots contribute signifi-cant amounts of ethylene or its precursor, 1-aminocyclopropane-

1-carboxylic acid (ACC), to the soil, particularly under stress(Abeles et al., 1992; Hyodo, 1991; Campbell and Thomson,1996; Grichko and Glick, 2001a; Stearns and Glick, 2003;Nayani et al., 1998; Ma et al., 2002). Upon exposure tostress, plants produce “stress ethylene,” which can be low-ered by associated bacteria able to produce 1-aminocyclopane-1carboxylate deaminase (ACC-deaminase) (Grichko and Glick,2001a, 2001b; Stearns and Glick, 2003). The ACC-deaminasecleaves ACC to α-ketobutyrate and ammonia (reviewed in Maet al., 2002). ACC-deaminase commonly occurs in soil bac-teria (Li and Glick, 2001; Gosh et al., 2003), including thepseudomonads (Campbell and Thomson, 1996), and in rhizo-bia (Shah et al., 1998), where it stimulates the formation of rootnodules in leguminous plants upon infection (Ma et al., 2002).

Thus it is not beyond the bounds of possibility to modify cropgrowth by manipulation of soil ethylene level via managementof ACC-deaminase–containing bacterial communities.

D. Feeding Soil MicrobesThe symbiosis that exists between plants and soil microbes

is much more highly evolved and extensive than was first real-ized. For decades, the use of amino acid supplements, sugars,humic acids, and various gaseous materials remained outside themainstream of agriculture in the U.S. because the scientific basisof such amendments was poorly understood. However, it is in-creasingly apparent that many of these materials and treatmentsdirectly benefit or stimulate microbial populations by perform-ing functions that directly benefit plants. Tailoring amendmentsand cultural practices to promote beneficial soil microbes hasbeen an underappreciated area of crop production science thatoffers potential for increasing agricultural productivity in a nat-ural and sustainable manner.

It is already well established that sugars and amino acids arereleased by decomposing plant material and can serve as carbonsources for soil microbes. However, in modern crop productionmonocultures that rely on mineral fertilizers, carbon sources canbecome limited, especially where crop residues are removedfrom fields and soil organic matter is kept low. Consequently,the diversity of microbial activity is likely to be reduced.

This is not meant to imply that soil applications of N-P-Kprimarily intended to provide essential nutrients to crop plantsdo not also benefit soil microbes. The point is that traditionalfertilizer inputs are intended primarily for crop plants and notthe microbes that sustain them. Even when soil organic matteris low, relatively few agriculturalists would fertilize their fieldsspecifically to benefit soil microbes.

Even so, simple sugars, in the form of molasses, have oftenbeen added to compost to hasten decomposition, and on occasionthey are used in small quantities by agriculturalists as a soilamendment (Story, 1939; Schenck, 2001). The benefits of sugarsupplements have been reported for many years and includeno detrimental environment effects because they decompose insoil to CO2 and harmless organic products (Anonymous, 1939


in Schenck, 2001; Story, 1939). As such, molasses have beenused as a carbon source for microbes in bioremediation of soilcontaminants (Park et al., 2002).

Using sugar as a fertilizer was found to increase sugarcaneyields, particularly on soils low in potassium (Schenck, 2001).It has been suggested that molasses soil treatments effectivelyreduced crop damage by root parasites (Anonymous, 1939 inSchenck, 2001; Story, 1939). Vawdrey and Stirling (1997) ob-served a reduction in the severity of root galling in tomato whenmolasses was added without urea. Molasses applied to fieldplots at relatively high rates lowered nematode soil populationsand improved papaya tree growth and harvestable fruit, and inChinese cabbage fields it decreased the numbers of Heteroderanematode cysts following harvest (Schenck, 2001). Here it wasreasoned that the suppressive effects of sugar on nematodes weredue variously to antagonism by microorganisms in the soil thatwere stimulated by molasses, changes in oxygen concentrationcaused by microbial metabolism of molasses, or the release oftoxic compounds from decomposing molasses (Schenck, 2001).

Soils in wheat, ryegrass, bentgrass, and clover crops have allbeen amended with sucrose to mimic rhizosphere carbon inputs(Grayston et al., 1998). After treatment, microbial communitieswere extracted and analysed using the BIOLOG system to con-struct sole carbon source utilization profiles for these communi-ties. A clear discrimination between the carbon sources utilizedby microbial communities from the different plant rhizosphereswas shown (Grayston et al., 1998). Accordingly, different carbonsources may stimulate specific soil microbes so that microbialfertilization can be customized to benefit particular microbes andthus the crops associated with them. Carbohydrates, carboxylicacids, and amino acids were the substrates mainly responsiblefor this differentiation, suggesting that plants may differ in theselective exudation of these compounds (Grayston et al., 1998).

Optimal growth of the soil bacteria Bacillus megaterium oc-curred with 5% (w/v) date syrup or beet molasses supplementedwith NH4Cl (Omar et al., 2001). B. megaterium has the abil-ity to solubilize inorganic phosphate (Cakmakci et al., 1992),suppress Rhizoctonia root rot of soybean (Zheng and Sinclair,2000), and produce polysaccharides (Bishop and White, 1993).

In greenhouse studies, B. megaterium isolated from sugar-treated potting soils displayed improved soil particle aggrega-tion and increased water-holding capacity, which was considereddue to his same exopolymer (G. Welbaum, personal communica-tion) (see Figure 1). Similarly, soils amended with molasses hadgreater moisture retention in a pawpaw field study in Australia,although the authors did not speculate on a possible mecha-nism (Vawdry et al., 2002). Sugars may also directly impact soilproperties in ways not related to microbial activity. Molassesand gypsum, applied either alone or combined, improved thestructural stability of two sodic soils by decreasing dispersionand/or slaking (Suriadi et al., 2002).

Apart from their trophic role, sugars also have a hormone-like function as primary messengers in signal transduction inplants and certain microbes (Koch, 1996; Smeekens, 2000;

FIG. 1. Changes in the water content of Sunshine Mix growing media av-eraged from 3 12-celled trays without plants in a growth chamber following asingle treatment with 8 mL of water or 50, 60, 80, or 100 mM sucrose. Watercontents were determined from fresh and oven dry weights. Sterilization of me-dia in an autoclave for 20 min prior to sugar treatment resulted in no increasein water-holding capacity. Staining with alician blue, a carbohydrate-specificstain, revealed positive staining beginning 48 h after treatment. Bacteria fromtreated soils were cultured on high sucrose media and genetically identified asBaccillus megaterium, a known producer of extracellular polysaccharide. Errorbars represent ± SE.

Rolland et al., 2002; Leon and Sheen, 2003). The concept ofsugars as central signalling molecules is relatively novel. Hex-okinase (HXK) has been found to be a glucose sensor that mod-ulates gene expression and multiple plant hormone-signallingpathways (Sheen et al., 1999; Smeekens, 2000; Leon and Sheen,2003). Diverse roles of SNF1-related protein kinases (SnRKs)in carbon metabolism and sugar signalling are also emerging(Halford and Hardie, 1998; Hardie et al., 1998). Recent molec-ular analyses have revealed direct, extensive glucose control ofabscisic acid biosynthesis and signalling genes that partially an-tagonizes ethylene signalling during seedling development un-der light (Leon and Sheen, 2003). Glucose and abscisic acid pro-mote plant growth at low concentrations but act synergistically toinhibit growth at higher concentrations (Leon and Sheen, 2003).

Sugar molecules modulate many vital processes that arealso controlled by hormones during plant growth and develop-ment (Smeekens, 2000; Leon and Sheen, 2003). For example,trehalose (∝-D glucopy-ranosyl-[1,1]-∝-D-glucopyranoside),a nonreducing disaccharide common in fungi and bacteriathat does not accumulate in plants but is involved in the


regulation of plant growth and stress responses (Godjin and vanDun, 1999; Ho et al., 2001). Transgenic plants expressing theEscherichia coli or Saccharomyces cerevisiae genes for tre-halose synthesis (Holstrom et al., 1996; Romero et al., 1997;Pilon-Smits et al., 1998), exhibited strong developmental alter-ations, such as stunted growth (Goddijn et al., 1997; Romeroet al., 1997).

The mechanisms by which trehalose metabolism alters plantdevelopment are not entirely known. Seedling growth has beeninhibited after treatment with 25 µM trehalose (Aeschbacheret al., 2000). Similarly, Shen and Welbaum (2004) foundthat 15 mM trehalose reduced both root and hypocotyl growthof alyssum and muskmelon by approximately 15%. Thus, mi-crobially derived trehalose may similarly affect plant growthand development. The fact that sucrose, trehalose, and othersugars are not just simple molecules providing carbon and en-ergy source but are also involved in sensing and signallingpathways both in plants and microbes (Goddijn and Smeekens,1998; Smeekens, 2000; Rolland et al., 2002) adds a fur-ther degree of complexity to the functioning of the agro-ecosystem.

Techniques have been developed to map the availability ofsugars and amino acids along live roots in an intact soil–rootmatrix with native microbial soil flora and fauna present. Jaegeret al. (1999) genetically engineered Erwinia herbicola 299R tocontain a promoterless ice nucleation reporter gene, driven byeither of two nutrient-responsive promoters, for use as a biosen-sor. Both biosensors exhibited up to 100-fold differences in icenucleation activity in response to varying substrate abundancein culture (Jaeger et al., 1999).

Plants leak nutrients that nourish soil bacteria, which inturn benefit plants by protecting then from disease (Zheng andSinclair, 2000; Vessey, 2003), stimulating plant growth, increas-ing nutrient availability (Cakmakci et al., 1992), or, in the caseof B. megaterium, secreting polysaccharides (Bishop and White,1993; Gandhi et al., 1997) that help both the bacteria and plantsavoid drought stress (G. Welbaum, personal communication)(Figure 1).

The polymer produced by B. megaterium (Bishop and White,1993; Gandhi et al., 1997) is an example of microbial extracel-lular polysaccharides (EPS) that are apparently produced by awide range of soil microbes (Roberson et al., 1995). EPS con-tribute to the stability of soil aggregates and are important factorsaffecting soil structure in cultivated soils. In studies of tomatoproduction in California, it was demonstrated that EPS produc-tion could be effectively managed primarily by manipulating N(Roberson et al., 1995).

Glomalin is another example of a beneficial microbial prod-uct produced by arbuscular mycorrhizal fungi in the taxonomicorder Glomales (Wright and Upadhyaya, 1996). Glomalin isthought to seal and solidify the outside of the fungi’s hyphae thattransport water and nutrients, particularly phosphate, to plants.As roots grow, glomalin sloughs off into the soil, where it im-proves aggregation of soil particles. It can also serve as a sink

for soil carbon and increases soil water-holding capacity whileretaining soil structure and aeration, and soil stability to resisterosion (Rillig et al., 2001).

Glomalin levels can be maintained or increased by using no-till, cover crops, reduced phosphorus inputs (Wright et al., 1999).Higher CO2 levels in the atmosphere also stimulate arbuscularfungi to produce more glomalin. Thus at CO2 levels of 670 µLL−1 arbuscular mycorrhizal hyphae grew longer and producedfive times as much glomalin as fungi on plants grown underambient levels (370 µL L−1) (Rillig et al., 2000).

Many biostimulants have been offered for sale commercially(Ferrini and Nicese, 2002; Kelting et al., 1998). Although mostof these products are advertised as enhancing plant growth, orincreasing stress tolerance, the stimulation of bacterial growthmay be an inadvertent outcome of foliar feeding (Holland, 1997).Humic substances (HS) have generally formed the major com-ponents of the mixture of materials that comprise soil organicmatter. Much of the humic acid research has dealt with its cre-ation, function, and longevity in soils. Relatively few studieshave examined its effects on plant growth when used as a bios-timulant (Kelting et al., 1998). Humic acid may also be an im-portant source of organic carbon for microbial populations, sincehumin is often broadly used to describe a mixture of materialsthat are insoluble in aqueous systems and that contain nonhu-mic components such as long-chain hydrocarbons, esters, acids,and even relatively polar structures of microbial origin, such aspolysaccharides.

Tailoring inputs to feed soil microbes has not beenwidely practiced. As our knowledge of soil microbial com-munities progresses, more precise rhizosphere managementpractices—enhancing soil and plant health and the overall cropproductivity—can be developed.

V. PRECISION MANAGEMENT OF A SUSTAINABLEAGRO-ECOSYSTEM—PROGRESS AND FUTURE

In general, agricultural production tends to focus on practicesdesigned to manage nutrients, water, weeds, and crop diseases.Precision agriculture and integrated pest management programshave gone one step further by recognizing the need to targetinputs where they are required in the field. Here the objectivehas been to lower the adverse environmental impacts of inten-sive agriculture practices and reduce per unit production costs.However, this undoubtedly successful approach can be furtherrefined by the development and integration of new technolo-gies, including new crop cultivars that capitalize on the holisticmanagement of the agro-ecosystem.

A better understanding of the dynamic nature of the plant–microbial ecosystem, the development of stable/beneficial as-sociations between existing and newly bred crop cultivars andtheir associated microflora, the introduction of the new waysof microbial population management, and the development ofreal-time monitoring and diagnostic devices, will favor timelyproduction interventions.


A. Plant–Microbial EcosystemsCertainly from the above discussion there is support for the

view that the functional biodiversity of soil organisms can belinked with the maintenance of soil functional processes. As a re-sult, the study of soil food webs—the interrelationship betweenbiological activity (Mikola and Setala, 1998), soil microflora(Hungate et al., 2000; Setala, 2000), plant community structure(Gange and Brown, 2002; Wardle et al., 1999), and soil man-agement practices (Brussaard, 1994; Moore, 1994) has been thefocus of intense interest in recent years. Even so, our knowl-edge of the interaction between soil food web decomposers andtheir effects on nutrient cycling is generally sparse (Ruess et al.,2002).

Perhaps even less well understood are the physiological, bio-chemical, plant–microbial and microbial–microbial interactionsthat occur in real time over changing agro-physical and agro-chemical environments (Mathesius, 2003). What are the molec-ular determinants of nutrient sequestration giving specific ad-vantages to groups of different microbial consortia in variousniches? What signal molecules are involved in nutrient sensingand how are they exchanged between plants and their coloniz-ing microflora? How do plants recognize beneficial microor-ganisms and differentiate them from pathogens? Suppression ofplant defenses in early stages of the rhizobia–legume symbio-sis development (Mithofer, 2002) and in mycorrhizal infection(Garcia-Garrido and Ocampo, 2002) indicates that such differ-entiation is indeed possible.

Developments in genomics, proteomics, and metabolomicsprovide new tools that will allow us to study genotype × en-vironment molecular interactions (Bouchez and Hofte, 1998;Briggs, 1998; Phillips and Freeling, 1998; Sommerville andSommerville, 1999; Delseny et al., 2001; Lagudah et al., 2001).These tools are currently being used on model plant species,but their application to a broader range of crops is essentialif we are to develop new approaches to the management ofagro-ecosystems.

Breeding plants for sustainable agricultural production sys-tems will incorporate newfound disease resistance genes (seereviews by McDowell and Woffenden, 2003; Staples, 2003).However, we must also consider beneficial plant–microbial asso-ciations in our breeding programs. Discovery of new small signalmolecules in plant responses to environmental stresses, e.g., tre-halose (Schiraldi et al., 2002), linear ß-1,3 glucans (Klarzynskiet al., 2000), fatty acid-derived compounds (Ongena et al., 2002;Weber, 2002), and microbial metabolic networks (Wackett,2003) on one hand, and advances in microbial (Hopwood, 2003;Wackett, 2003) and plant (Britt and May, 2003; Morandini andSalamini, 2003) genome sequencing, functional genomics (e.g.,Askenazi et al., 2003), and in silico interaction of metabolicnetworks modeling (Price et al., 2003) on the other, will in-crease the number of breeding options and selection criteriaavailable to plant breeders. Certainly communities of microor-ganisms and their host plants could benefit from closer geneticlinks (Lugtenberg et al., 2001). Interaction between soil particles

and microorganisms has been recognized as one of the key de-terminants in a functioning terrestrial ecosystem (Huang et al.,2002; Sessitsch et al., 2001). The introduction of certain my-corrhizal fungi–rhizobacteria combinations can not only affectplants but also influence rhizomicrobial composition (Probanzaet al., 2001) and soil structure, enhancing, for example, the pro-portion of water-stable aggregates (Bethlenfalvay et al., 1997).

Only a small proportion of naturally occurring microorgan-isms can be cultured using traditional microbiological tech-niques (Hugenholtz and Pace, 1996). Soil- and plant-associatedbacteria can also switch between culturable and unculturableforms (Hurek et al., 2002). Fortunately, molecular methods al-low the monitoring of both bacteria forms (Sessitsch et al., 2001)and can distinguish between active and dormant constituents inany population (Sessitsch et al., 2002). Moreover, a combina-tion of molecular techniques and electron and epifluorescencemicroscopy have opened up possibilities to study bacteriophagesin natural ecosystems (Asheford et al., 2003). These bacterialviruses may play a significant role in the management of bacte-rial populations, as their numbers seem to be much higher thanestimated before and may reach, on average, 1.5 × 108 g−1 ofsoil (approximately 4% of the bacterial population) (Ashefordet al., 2003). Such powerful analytical tools will enable us tobetter address agro-ecosystem management processes at the mi-crobial level and link them to the development microbial utiliza-tion methods in plant production systems. In this regard, find-ing new ways of establishing stable associations between plantsand beneficial organisms and understanding the molecular andbiochemical mechanisms of signal recognition and transductionthat occur in plant–microbial interactions under different envi-ronments are most challenging study elements.

B. Soil PrimingSoil structure, its overall health, and crop yield potential can

be modified by cultural practices. However, the concept of “soilpriming,” which we interpret as setting the “readiness” of aspecific soil to receive a selected crop, is still new (Yunasaand Newton, 2003). For example, the design composition ofa cover crop in a heavy life-mulch/no-till production system(Morse, 1999) can include “primer plants” with deep, thick,and fast-decomposing roots, providing channels (biopores) forthe establishment of soil microbial communities (Yunasa andNewton, 2003). Integration of legumes, which secrete com-pounds recognized as signal molecules by rhizobacteria, intolife-mulch will induce the bacterial production of Nod factors(lipochitooligosaccharides) essential for the establishment suc-cessful N2-fixing legume–rhizobia symbiosis (Prithiviraj et al.,2003). Submicromolar concentrations of these compounds in-duce physiological changes in both host (legume) and an array ofnonhost plants by enhancing seed germination and early seedlinggrowth (Prithiviraj et al., 2003). Moreover, nodules of severallegumes produce high levels of hydrogen gas, which stimulatesproliferation of beneficial bacteria in the rhizosphere, improving


growth of cereals in rotation (Dong and Layzell, 2001; McLearnand Dong, 2002). Recent interest in the hydrogen-producing mi-croorganisms has been motivated by the potential for the bio-logical production of hydrogen gas for fuel (Kalia et al., 2003),and options also exist for their use in conventional agriculture.

C. Biopriming Plant PropagulesDespite decades of extensive investigation of seed inoculation

with beneficial microorganisms (seed biopriming) (McQuilkenet al., 1998; Dobbelaere et al., 2003; see reviews by Bennettet al., 1992; Callan et al., 1997) and tuber (Burr et al., 1978;Burr and Caesar, 1984; Lynch, 1990), the full potential for theutilization of these natural allies has never been achieved.

A promising new area is that of induced-resistance responsesin host plants mediated by selected strains of rhizosphere bac-teria. These appear to protect plants by activating general inter-nal defense responses (Pieterse et al., 2001). This phenomenon,phenotypically similar to pathogen-induced systemic acquiredresistance (SAR), is referred to as rhizobacteria-mediated ISR(Van Loon et al., 1998). SAR in plants is induced by a va-riety of necrotizing pathogens and depends on salicylic acid(SA) accumulation in infected plants. Similar to SAR, some rhi-zobacteria induce the SA-dependent signaling pathway by pro-ducing nanogram amounts of SA in the rhizosphere (De Meyerand Hofte, 1997; De Meyer et al., 1999). Other rhizobacteriaactivate plant defences via an SA-independent signaling path-way involving jasmonic acid and ethylene (Ton et al., 2002).SA-independent ISR has been well characterized in the modelplant Arabidopsis thaliana, using Pseudomonas fluorescencestrain WCS417r as the inducer (Pieterse et al., 1996; van Wees,2000; Ton et al., 2002).

ISR, is now considered a general plant defense phenomenon,and has been described in many plant species, including to-bacco, tomato, cucumber, bean, radish, and carnation. The ad-vantage of using ISR as a tool for promoting disease resistance inplants is that it provides a broad-spectrum resistance against sev-eral different types of pathogens. In Arabidopsis, for example,P. fluorescence strain WCS417r-induced ISR was effec-tive against fungal root pathogen Fusarium oxysporum, andoomycete leaf pathogen Peronospora parasitica, and bacterialleaf pathogens Pseudomonas syringae pv. tomato and Xan-thomonas campestris pv. armaraciae (Pieterse et al., 1996; vanWees et al., 1997; Pieterse et al., 2000).

Simple seed inoculation with beneficial organisms has notbeen successful (Dobbelaere et al., 2003), as such inoculantsmust compete with naturally occurring colonizers (both endo-phytic and epiphytic; Sturz et al., 2000). Tissue culture tech-niques provide a great opportunity for the uptake of selectedmicrobial strains and/or strain combinations by sterile (or rela-tively sterile) plant propagules. In vitro and ex vitro bacterizationand mycorrhization of vegetatively propagated material is cur-rently being explored as an efficient way to improve productionpractices of high value horticultural crops (reviewed in Nowak,1998; Nowak and Shulaev, 2003; Rai, 2001). The use of en-

dophytic bacteria seems to be particularly promising (Nowakand Shulaev, 2003). Such bacteria, when cocultured with plants,can be readily established in planta (e.g., Pillay and Nowak,1997) and managed accordingly (Sturz et al., 2000). The suc-cessful introduction of endophytic pseudomonads into tissueculture plantlets to improve transplant establishment (Nowaket al., 1999) and early vigor (Lazarovits and Nowak, 1997)has also been found to increase resistance to biotic (Sharmaand Nowak, 1998; Barka et al., 2002) and abiotic (Bensalimet al., 1998) stresses. Similar introduction of nitrogen-fixing en-dophytes (other than Rhizobia) into clonally propagated plantscould also significantly contribute to the development of sustain-able crop production systems (Dong et al., 1995; Sturz et al.,2000). Reis et al. (1999) has successfully inoculated sugar caneplantlets with Acetobacter diazotrophicus, in vitro; and thesebacteria were reisolated from plants thirty days after transplant-ing, demonstrating successful colonization.

The development of stable artificial associations betweenplants and nitrogen fixing diazotrophic bacteria have also beendescribed by Varga et al. (1994) and Preininger et al. (1997).Here, the authors were able to regenerate plantlets from a sym-biotic callus-bacteria culture system, which could fix nitrogen.Such associations have been established with carrot (Vargaet al., 1994), strawberries (Preininger et al., 1997), tomato,potato, wheat, sugar cane, and poplar, using 11 strains of 8Azotobacter species (Sz. S. Varga, personal communication). Inthe tomato system, the bacterium could be transmitted throughseeds; approximately 20% of seedlings derived from the seedsof Azotobacter beijerinckii-containing tomato demonstrated N2-fixing activity two months after germination (Sz.S. Varga, per-sonal communication).

Synergistic effects of VAM fungi and diazotrophic bacteriaon nutrition and growth of various crops have been demonstratedby Paula et al. (1991, 1992). This promising finding, combinedwith a substantial body of literature describing the presence of“mycorrhiza helper bacteria” in natural ecosystems (see reviewsby Garbaye, 1994; Founoune et al., 2002) needs to be exploredfurther.

The development of a defined coculture microbial–plant mi-croecosystem to study complex plant–microbial environmentinteractions (Nowak and Shulaev, 2003) would contribute to theoverall understanding of the plant growth ecosystem (Probanzaet al., 2001) and the development of new technologies for stressmanagement and yield enhancement in plants. In this way, thelarge-scale production of microbial propagules, seeds, tubers,cuttings, or grafted transplants containing endophytic and/orepiphytic microbial populations designed for specific plantingsites and/or crop rotations would contribute significantly to thecreation of sustainable agro-ecosystems.

D. “Microbial Precision” Production Systems: TheDevelopment of the “Smart Field” Concept

Precision agriculture became a popular term in the 1980s todescribe the use of the Global Positioning System (GPS) to tailor


inputs and map productivity to specific geographical locationswithin the field setting (Robert, 2002). With the continuing evo-lution of molecular genetic techniques, computer technology,and nanotechnology, it will be possible to precisely manage therhizosphere while monitoring soil and plant health, in real time.Although much progress has been made in understanding thosefactors that comprise a sustainable agro-ecosystem and the dy-namic interactions of microbial communities with soil/soil par-ticles (Huang et al., 2002; Passiora, 2002b) and plants (O’Neill,1991; Sturz and Nowak, 2000), much more needs to be done todesign “microbial precision” production systems.

Such a system would be based on the management of func-tional microbial communities—namely disease inhibitors, in-ducers of growth promotion and stress resistance responses inplants, and facilitators of nutrient/water uptake (Vessey, 2003)—and will require comparative studies to determine the interac-tion of cultural practices, soil amendments, and crop rotations inthe agro-ecosystem linked to soil and plant “health” (Passiora,2002a; Paulitz et al., 2002; Ryszkowski et al., 1998; Stine andWeil, 2002).

Today, genetically based microbial profiling (Sessitsch et al.,2001, 2002) allows us to link microbial population dynamics tosoil type and farming inputs and outputs. Most microbial ecologystudies on this topic focus on the management of rhizospherediseases, the beneficial effects of the phylloplane organisms, i.e.,methylobacteria (Holland and Polacco, 1994; Holland, 1997)and yeasts (Buck, 2002). The effects of soil and plant nutrition onresident microbial populations (both exo- and endoplant) haveonly begun to be considered (Kinkel, 1997; Andrews and Harris,2000).

Adaptation of environmental probes based on nanosensorsfor agro-ecosystem monitoring would allow the developmentof “smart fields.” In smart fields, simple though essential envi-ronmental factors such as temperature, pH, water, mineral nu-trients, and gas composition (e.g., oxygen, carbon dioxide, andethylene) could be monitored in real time and at multiple loca-tions in the field. Such probes could be integrated into arrays andlinked to a computer-based “monitoring/command” system thatturns on specifically prescribed response inputs to correct forimbalances that might arise. Changes to the rhizosphere couldbe rapidly made through a subsurface irrigation system (e.g.,http://www.irrigro.com/; http://www.gravityline.com/) buried toa depth of 15–25 cm. Diverse inputs, such as water, mineral nu-trients, microbial inoculants, crop protection chemicals, gases(e.g., O2, air, or H2) and organic nutrients (e.g., sugars and/orsignal molecules) that preferentially feed soil and plant benefi-cial microbes could readily be delivered, creating both benefi-cial rhizospheres and healthy plant stands. Much more attentioncould be paid to field site preparation prior to planting (soil prim-ing) to reduce soil-borne disease pressures and thus postplantinginputs.

Smart Field technology, combined with microbial popula-tion analyses, offers the possibility of (1) further improving ourunderstanding of interactions within the soil microbial–plant

ecosystem; (2) better enabling the identification of indicatorsof soil and plant health status, allowing for early interventionsand thus reducing the requirement for inundative system inputs;(3) creating a scientific “workshop” for the development of newsustainable technologies for accelerated soil improvement; and(4) provide impetus for discovery and the development of sim-ple diagnostic tools for the determination of soil and plant healthstatus parameters.

ACKNOWLEDGEMENTSThe authors would like to acknowledge the contribution of

Ms. Margaret Merrill, the College Librarian (College of Agricul-ture and Life Sciences, Virginia Polytechnic Institute and StateUniversity), to literature searches, and Mrs. Maura Wood’s helpwith manuscript preparation.

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Managing soil microorganisms to improve productivity of agro-ecosystems

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