Critical Reviews in Plant Sciences, 23(2):175–193 (2004)

Copyright C Taylor and Francis Inc.

ISSN: 0735-2689
DOI: 10.1080/07352680490433295

Managing Soil Microorganisms to Improve Productivity

of Agro-Ecosystems

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

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

Zhongmin Dong
Department 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 .............................................................................................................................................. 176

A. Overview ...................................................................................................................................................... 176
B. Some Definitions ........................................................................................................................................... 176

II. SOIL AGRO-ECOSYSTEM AND MICROBIAL COMMUNITIES .................................................................... 177

A. Soil Microbial Diversity and Functionality ....................................................................................................... 177
B. Plant-Engineered Root Zone Communities ...................................................................................................... 177
C. Beneficial and Detrimental Microbial Allelopathies ......................................................................................... 178

III. NITROGEN-FIXING AND HYDROGEN-GAS–OXIDIZING BACTERIA ......................................................... 178

A. Nitrogen-Fixing Bacteria in Soil ..................................................................................................................... 178
B. Hydrogen-Gas–Utilizing Bacteria in the Rhizosphere ....................................................................................... 179

IV. SOIL AGRO-ECOSYSTEM MANAGEMENT ................................................................................................... 180

A. Tillage Effects ............................................................................................................................................... 180
B. Bacterial Endophytes and Crop Rotations ........................................................................................................ 180
C. Soil Ethylene and Crop Development .............................................................................................................. 180
D. Feeding Soil Microbes ................................................................................................................................... 181

V. PRECISION MANAGEMENT OF A SUSTAINABLE AGRO-ECOSYSTEM—PROGRESS AND FUTURE ...... 183

A. Plant–Microbial Ecosystems ........................................................................................................................... 184
B. Soil Priming .................................................................................................................................................. 184
C. Biopriming Plant Propagules .......................................................................................................................... 185
D. “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: jenowak@vt.edu

175
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 have
gone one step further by recognizing the need to target inputs where
they are required in the field. The major objective of these programs
has been to minimize adverse environmental impacts of intensive
agriculture practices and reduce per unit production costs. This
review surveys the literature, examining the manipulation of mi-
crobial (primarily bacterial) populations as linked to agricultural
production, and discusses new approaches that involve the pre-
cision management of microorganisms in the agro-ecosystem. It
is proposed that our understanding of plant–soil interactions can
be greatly refined through the development of “smart” field tech-
nology, where real-time, computer-controlled electronic diagnostic
devices can be used to monitor rhizosphere and plant health. We
submit that “smart field” generated information could be used to
develop a prescription for timely and low-level production interven-
tions that will avoid the traditional inundative approaches to crop
maintenance and soil husbandry. Consequently, a lesser impact on
the agricultural soil environment is envisioned. The maximization
of production efficiencies will also involve the development of crop
cultivars 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; the
quality of the soil has changed; and if we will live as well, and become
as rich and respectable as our fathers, we must cultivate their virtues;
but abandon their farming system.
- The Farmers Manual (1819)
A. Overview
Mismanaging soil health and fertility is not a prerogative of
twenty first century agriculture. In the early part of the nineteenth
century commentators had already noticed the occurrence of soil
exhaustion and fertility loss, the consequences of overworking
farmland 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 management
mistakes, 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, leaving
in their wake a ruined rural landscape, stripped of its forests and
depleted of its fertile topsoil (Strickland, 1801). Accordingly,
one of the most intractable problems in American agriculture in
the 1800s became managing the relationship between yields and
soil nutrient balance. For although farmers understood that fer-
tility could be taken away, few understood the best methods for
returning it.
In his treatise on the history of soil regeneration practices in
early America, Stoll (2002) outlines a number of the systems
that more enlightened farmers used to conserve and improve
their soils, maintain tilth, and increase productivity. This was
not new knowledge; pioneers in land experimentation had their
roots in Great Britain, where Jethro Tull’s The Horse-Hoeing
Husbandry (1733) promoted what today might be described as
a system of sustainable soil management.
Such calls to farming practices, which espoused the main-
tenance or improvement of the land base, were taken up by
successive sets of producers who praised the benefits of soil
conditioning based on “closed” nutrient cycles and soil micro-
bial rejuvenation. These practices were principally the result of
reincorporating 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 of
food 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. Chemical
fertilizers came to supplant organic farming systems and the
“natural” accumulation of soil nutrients and soil microflora that
produced them. Newly developed classes of plant cultivars be-
came increasingly reliant upon the support of agrichemistry. At
the same time, the yield potential of agricultural soils began to
decline as the biological processes that maintained their health
and quality became overtaxed (Greenland and Szabolcs, 1994;
Pankhurst et al., 1997). Accordingly, an environmental price was
paid for a food security system based upon technological and
agrichemical innovation and the exploitation of nonrenewable
energy reserves. Most notably, in the 1970s, 1980s, and 1990s the
scientific literature became filled with reports of “soil-fatigue,”
“soil degradation,” and “soil loss.”
B. Some Definitions
Despite 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 that
sustain them. And while the physical and biological benefits
of 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 “soil
quality,” “soil resilience,” and “soil health,” or that conserve “soil
stability” above and beyond the application of chemical fertil-
izers and certain well-established systems of crop rotation and
residue management.
In the general context of this review, we define soil quality in
terms of its “suitability for chosen uses” (Warkentin and Fletcher,
1977), usually for the purpose of sustaining plant and animal
productivity 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
arrangement of solid and void space when exposed to different
stresses” (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 key
role in soil quality and health (Pankhurst et al., 1997; Karlen
et al., 1997; Vessey, 2003), a general dearth of information ex-
ists when it comes to categorizing the assembly of species that
assure soil fertility, the critical forces that govern their com-
munity structure and function. What has become clear is that
the interaction between root zone microflora and plants involves
a continuum of colonization events that are initiated at seed
germination and traverse the rhizosphere to the rhizoplane, to
the endoroot via the root epidermis and apoplast, directly to the
shoots (Petersen et al., 1981; Kloepper et al.,1992; Van Bruggen
et al., 2002). Consequently, phyto-microbial relationships can
become extremely intimate, extending over the life-cycle and
growth habit of the plant, and involving both exo- and endo-
plant environments (Wardle, 2002). In this review we focus on
methods to create sustainable agro-ecosystems of crop produc-
tion through the selective management of phyto-microflora.
II. SOIL AGRO-ECOSYSTEM AND MICROBIAL
COMMUNITIES
A. Soil Microbial Diversity and Functionality
It 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 and
Shine, 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 functional
stability—in response to perturbation—remains an unresolved
question (Pankhurst, 1994).
While several studies have shown that a reduction in species-
abundance relationships—measured, for example, by species
richness (total species) and species evenness (defined by the rel-
ative frequency within a community)—can precede declining
ecosystem processes (Naeem et al., 1995; Knops et al., 1999;
Wilsey and Potvin, 2000), there is little conclusive evidence to
support the hypothesis that ecosystem function depends upon
the “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, where
studies of biodiversity can often become confounded by diffi-
culties associated with the recovery and identification of suitable
taxonomic units necessary to describe species (O’Donnell et al.,
1994; Pankhurst et al., 1996).
177
Part of the difficulty in resolving soil microbial community
structure is our limited ability to examine soil ecosystems in real
time. The current trend of community-based analysis using PCR
extraction does provide a new insight into the enormous diversity
of 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 remain
constant, 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 that
of changes in compositional variability (relative abundance of
component 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 of
turnover of species within an ecosystem, and the accumulation
of biological diversity over time, if any, is subject to a number of
rate-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 that
environmental perturbations will increase the variability of eco-
logical systems (Odum et al., 1979; Underwood, 1991). Whether
this variability leads to increasing species diversity—thus pro-
moting increased productivity and stability within ecosystems—
becomes the basis for an interesting discussion (Cottingham
et al., 2000; Johnson et al., 1996; Kennedy and Smith, 1995;
Naeem and Li, 1997).
B. Plant-Engineered Root Zone Communities
While 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 agricultural
soil. The vast surface area provided by roots is an extraordinarily
diverse habitat for a huge assortment of microorganisms ranging
from transient epiphytic saprophytes to epiphytic commensals,
mutualistic symbionts, endophytes, and pathogens.
The biogeography of the habitats comprising the root system
are defined by physical and chemical characteristics such as
increased exposure to light, water, aeration, plant photosynthate
leakage, root architecture, and root longetivity (Andrews and
Harris, 2000; McCully, 1999). However, it is primarily through
the general release of carbon-rich material in the form of root
border 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 with
substrates that encourage the development of cultivar-specific,
178 G. E. WELBAUM ET AL.
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 initiate
changes in the root biochemistry (Darrah, 1993; Hinsinger,
1998; Parmar and Dardarwal, 1999; Lugtenberg, 2001; Patten
and 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 substrate
loading in the root zone, which in turn promotes rhizobacte-
rial proliferation, leading to further root growth, a concomitant
increase in root exudation that leads to substrate loading, and
so on.
All such root–microbial exchanges can be considered a form
of allelopathy (Barazani and Friedman, 1999) and include those
biochemical interactions, both inter- and intraspecifically, that
involve microbial- or plant-produced secondary metabolites (al-
lelochemicals) that influence growth and development of bi-
ological systems in the soil. Consequently, phyto-microbially
governed 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 it
is also the final recipient. An analogous process can be found
in autotoxicity, where phytochemical autoinhibitors collect in
the root zone and inhibit same or nonsame species’ growth and
development (Singh et al., 1999).
Since this can involve ecological phenomena at the trophic
level (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 substrate
determines reversible transition between active and dormant mi-
crobial states and differentially affects microbial community
structure (Stenström 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 soil
agro-ecosystem (Taylor et al., 2002).
C. Beneficial and Detrimental Microbial Allelopathies
The 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 include
both inhibitory and stimulatory effects, and the definition has
been extended to include “any process involving secondary
metabolites produced by plants, microorganisms, viruses and
fungi that influence the growth and development of agricultural
and biological systems (excluding animals), including positive
and negative effects” (Torres et al., 1996, p. 278).
As a class of relationship between organisms, allelopathy
is considered to be one where no direct contact occurs, the
effect 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 provide
the host plant with a distinct ecological advantage through
the cultivation of beneficial allelopathies (Sturz and Christie,
2003). Microbially generated secondary metabolites have been
shown to aid plant growth (Glick et al., 1999; Patten and Glick,
2002; Mathesius, 2003), increase availability of minerals and
nutrients (Murty and Ladha, 1988; Darrah, 1993; Marschener
and Römheld, 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 direct
biocontrol of phytopathogens (Weller et al., 2002; Van Bruggen
et al., 2002), induce systemic forms of plant disease resistance
(Van Loon et al., 1998; van Wees et al., 1999), and secure
plant establishment (Lazarovits and Nowak, 1997; Burd et al.,
1998).
By contrast, detrimental allelopathies occur where bacte-
rially produced secondary metabolites adversely affect plant
growth and development. These detrimental effects occur in
the absence of any pathogenic symptomology (Schippers et al.,
1987; Barazani and Friedman, 2001), although affected plants,
in their weakened state, can subsequently become susceptible
to phytopathogen attack (Frederickson and Elliot, 1985). Ac-
cordingly, such organisms have been termed deleterious rhi-
zosphere microorganisms (DRMO) and include the deleterious
rhizobacteria (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 (Åström and Gerhardson, 1988; Grayston et al.,
1998), and accompanying mycorrhizal status (see review by
Azcón-Aguilar and Barea, 1992). Sturz et al. (1997) showed
that bacterial strains, which individually inhibit plant growth,
can stimulate plant growth when applied as coinoculants. Sim-
ilarly, the order in which bacterial populations form consortia
and become established in the root zone can affect subsequent
plant growth responses (Sturz and Christie, 1995).
For a more comprehensive overview of the involvement of
plant and microbial secondary metabolites in ecosystem func-
tioning (including allelopathy), please see Hadacek (2002) and
Barazani and Friedman (2001).
III. NITROGEN-FIXING AND
HYDROGEN-GAS–OXIDIZING BACTERIA
A. Nitrogen-Fixing Bacteria in Soil
The amount of N present on this planet as dinitrogen is ap-
proximately 4 × 1015 tons in the atmosphere and about 20 times
that 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. Although
significant amounts of nitrogen are derived from industrial
fertilizers, most of the fixed nitrogen present in the world’s
 MANAGING SOIL MICROBES
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 and
often enter the root and/or shoot interior, occupying intercellular
spaces (the so-called diazotrophic endophytes). Free-living N2
fixers contribute only small amounts of N to plants. Symbiotic
N2 -fixing bacteria can contribute directly to the productivity of
plants at a high rate, while less direct contributions may be made
to the growth of plants by associative bacteria. Although their
nitrogen contribution is minuscule, the associative diazotrophs
enhance 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 wave
of investigations into associative endophytic diazotrophs in non-
legume plants (Riggs et al., 2002).
The rhizobia–legume symbiotic relationship is the most
widely studied and utilized of plant–microbe interactions
(Sprent, 2001). Rhizobia residing inside nodules of legume
plants 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 bacteria
provide 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 for
organic carbon. In this system, microbial populations respond
to plant exudates, and plant exudation follows from microbial
activity in the rhizosphere.
The organic carbon exuded from plant roots into the rhizo-
sphere promotes microbial population development around the
roots. Studies have shown that root exudation is positively re-
lated to soil inorganic N pool, its subsequent uptake by plants
and its final accumulation in leaves (Hamilton and Frank, 2001).
Although no N fixation was shown in that study, it was clearly
demonstrated that plants were capable of promoting soil micro-
bial populations through nutrient delivery, especially nitrogen
nutrient supply. Direct soil deposition of plant-derived nitro-
gen, including rhizodeposits (decaying roots), functions as a
source of nutrients for the surrounding bacteria (Høgh-Jensen
and Schjoerring, 2001). Retaining crop residues increase the
number of N-fixing bacteria in soil by a factor of 100 and their
activity by more than 10 (Roper, 1983). For a detailed overview
of the nitrogen fixation by the associative diazotrophs, and root
exudation, see the review by Jones et al. (2003).
B. Hydrogen-Gas–Utilizing Bacteria in the Rhizosphere
It is well known that intercropping legumes with nonlegumes,
or crop rotation involving legumes and nonlegumes, can lead
to significant increases in the growth and yield in the non-
legume crop. However, only about 25% of the increase in
the growth of the nonlegume crop can be attributed to im-
proved N nutrition. The remaining 75% of the effect have
179
eluded explanation (Bolton et al., 1976; Hesterman et al., 1986;
Fyson and Oaks, 1990; Zanetti et al., 1996; Høgh-Jensen and
Schjoerring, 2001). Recent studies showed that the H2 produced
as a by-product of N2 fixation by legume nodules is responsi-
ble for a substantial portion of the growth- or yield-enhancing
effects of legume soils. Antibiotic and/or fungicide treatments
have 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). In
most free-living diazotrophs and some symbioses, the bacteria
also produce an enzyme called an uptake hydrogenase (HUP),
which is able to oxidize the H2 and thereby extract chemical
energy from it. However, many legume symbioses, including
most of the rhizobia used in agricultural production, lack this
uptake hydrogenase (Uratsu et al., 1982). Thus the H2 produced
by the nitrogenase diffuses out of the nodule into the soil. The
H2 production represents an energy source equivalent to 5 to
7% of the crop’s net photosynthesis (Dong and Layzell, 2001).
This H2 loss from nodule to soil is traditionally believed to be
a disadvantage of HUP− over HUP+ . But the evolutionary pro-
cess, plant breeding of agricultural crops, or selection of optimal
N2 -fixing bacteria have not reduced this energy loss in legumes.
This leads to the hypothesis that H2 released by legume nodules
may 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 Favre
and Focht, 1983), resulting in an increase in rhizobial biomass
(Popelier et al., 1985), and greater rates of O2 consumption and
chemoautolithotrophic CO2 fixation (Dong and Layzell, 2001).
A recent study showed that this H2 uptake in H2 -treated soils
and soil around HUP− nodules is promoted by bacterial activity
(McLearn and Dong, 2002). Since the H2 released by nodules is
oxidized by bacteria in the adjacent soils, it has been proposed
that the soil microfloral community structure is changed by the
H2 released into the soil, and this microbial alteration influences
plant growth. Plant growth studies showed that H2 -treated soil
promoted soybean, barley, and canola growth by 10 to 20, and
spring wheat by 20 to 30% (Dong and Layzell, 2002). These
experiments indicate that a considerable amount of energy is
transferred to the rhizosphere microbial population in a HUP−
legume field in the form of H2 , and in return the energy-enriched
soils promote plant growth. These discoveries could help to ac-
count for the beneficial effects of legumes used in rotations with
cereals and other crops. We can speculate that H2 produced as
a by-product of N2 fixation in legumes enhances certain micro-
bial populations in soil and improves the growth and yield of
the subsequent crop. This hypothesis would also account for
the evolutionary questions surrounding why HUP− symbioses
have thrived when there are genes (in many cases within the
same genus and species) for the more energetically efficient
HUP+ symbioses (Uratsu et al., 1982). Perhaps the plant growth
180 G. E. WELBAUM ET AL.

advantages of the HUP− symbioses offset the greater energy ef- For a recent overview of the soil-borne disease management
ficiency of the HUP+ symbioses. approaches under a direct seeding system (no till), see Paulitz
et al. (2002).
IV. SOIL AGRO-ECOSYSTEM MANAGEMENT
B. Bacterial Endophytes and Crop Rotations
A. Tillage Effects
A continuous apoplastic pathway exits from the root epi-
The use of tillage techniques in seed bed preparation and land
dermis to the shoot, which appears sufficient for movement of
use management not only impose a physical stress on the soil
microorganisms from the root cortex into the xylem and from
structure but also on the soil microbial communities that inhabit
there throughout the plant (Petersen et al., 1981). Consequently,
that soil (Doran and Linn, 1994; Elliot and Stott, 1997). In an
many bacterial endophyte communities are the product of a col-
effort to minimize such stresses, modern arable farming systems
onizing process initiated by rhizobacteria in the root zone. In
are attempting to reduce excessive cultivation in favor of limited
this regard, the plant host offers the microbial endophyte a rela-
or strategic tillage practices (Massé et al., 1994).
tively homeostatic, spatially diverse environment that is suitable
Here we define a conventional tillage system as a prelimi-
for biotrophic mutualists, benign commensals, and necrotrophic
nary deep primary operation followed by some secondary tillage
pathogens alike (Chanway, 1996: Stone et al., 2000).
system for seedbed preparation (Soil Conservation Society of
Where plant–endophyte populations are complementary, two
America, 1976). In contrast, conservation, or reduced tillage,
broad categories of beneficial effect are found in the literature,
can encompass any tillage practice that reduces loss of soil and
namely (1) plant growth promotion (e.g., Frommel et al., 1991,
water as compared to unridged or clean tillage. This can include
1993; Pillay and Nowak, 1997; Glick et al., 1998, 1999) and
(1) minimum tillage, considered to be the minimum amount of
(2) disease control based on postinfection pathogen suppression
tillage required for seed bed preparation and plant establish-
(Benhamou et al., 1996; Sturz et al., 1999). Recently, increased
ment; (2) notillage/zero tillage/direct drilling, which involves
interest has been expressed in further defining and exploiting
no seedbed preparation other than chemical preparation and soil
this relationship (Turner et al., 1993; Hallman et al., 1997;
opening for seed placement (Baeumer and Bakerman, 1973);
Sturz et al., 2000; Kobayashi and Palumbo, 2000; Lodewyckx
and (3) high-residue mulched beds (Morse, 1999, 2000)
et al., 2002; Mathesius, 2003), especially in those situations
Compared to conventional tillage systems, reduced-tillage
where endophytes are able to mitigate plant responses to en-
practices offer not only long-term benefits from soil stability,
vironmental stress, such as those found as a result of drought
reduced soil erosion, and sustainable agriculture (Anderson and
(Nowak et al., 1999), transplantation (Nowak et al., 1995) and
Gregorich, 1983; Lal, 1991; Larson and Pierce, 1991), but they
heat (Bensalim et al., 1998). However, where plant–endophyte
can also enhance soil microbial diversity (Davis et al., 2002;
populations are noncomplementary, inhibitory allelopathic ef-
Hassink et al., 1991; Lupwayi et al., 1998; Magdoff and van
fects can result (Sturz and Christie, 1996).
Es, 2000; Phatak, 1998; Phatak et al., 2002; Wander et al.,
It soon becomes clear that a fundamental source of potential
1995). Thus, minimizing the mechanical upheaval associated
endophytes is to be found in the soils and organic debris of previ-
with tillage operations tends to maximize soil microbial diver-
ous crop plantings. Thus, by extension, complementarity among
sity because the disruption of food substrate at the trophic level,
rotation crops will involve a microbial compatibility between the
desiccation and soil compaction are reduced, and optimum pore
newly planted crop and the resident autochthonous soil popula-
volume is maintained (Giller, 1996).
tion. Consequently, it has been proposed that the yield benefits
Paradoxically, fallow periods in a crop rotation can reduce
from complementary cropping systems involving, for example,
soil microbial diversity (Zelles et al., 1992), an effect proba-
legume rotations—and often attributed solely to residual nitro-
bly associated with food substrate depletion over time. Thus,
gen and improved soil structure—may also include an additional
heterogeneity in soil microbial populations tends to coincide
benefit from the carryover of the residual populations of endo-
with heterogeneity of food resources, which is often greatest in
phytically competent bacteria able to promote plant growth and
crops under conservation or zero tillage management, where the
inhibit disease development (Sturz et al., 1998). These relation-
residue of the preceding year’s crops adds sequentially to the
ships between crops in complementary rotations can be cultivar
variety of food substrates available for utilization.
specific (Sturz et al., 1999, 2003). Accordingly, crop rotation
Clearly, while the act of mixing soil during tillage increases
selection criteria should include an evaluation of the effects of
seedbed homogeneity, it will simultaneously destroy the diver-
rhizobacteria and their associated endoplant-competent bacte-
sity of trophic microsites that occur down the soil profile together
rial communities when considering the long-term consequences
with the assemblages of soil microorganisms that occupy them.
of those crop choices, since the benefits to soil health and quality
The result is a reduction in both the structural and functional di-
of such choices are likely to be cumulative.
versity of the soil microbial community (Beare et al., 1995) and
the efficiency of those microbially mediated processes that sus-
tain the agricultural productivity of soils, e.g., nutrient recycling, C. Soil Ethylene and Crop Development
degradation of toxic residues, maintenance of soil structure, and While the details and significance of soil ethylene (C2 H4 )
aggregation (Sparling, 1997). have only recently become appreciated, some repercussions
 MANAGING SOIL MICROBES
have already been recognized. Soil ethylene can affect plant
growth and is certainly a significant factor in field production
of agricultural crops. Soil is itself a source of ethylene, and the
amount 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 accumulation
in soil (Arshad and Frankenberger, 2002), most soil ethylene is
produced 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 to
Smith 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” of
soils 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 and
Smith (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 and
Moreau, 1979; Smith and Dowdell, 1974), sufficiently high to
cause 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 gaseous
plant hormone ethylene can, in very small concentrations, af-
fect plant release from dormancy, shoot and root growth and
differentiation, adventitious root formation, leaf and fruit ab-
scission, floral induction, female flower formation, flower and
leaf 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 compound
in 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 (Nayani
et al., 1998; Grichko and Glick, 2001a, 2001b; Penrose and
Glick, 2001; Penrose et al., 2001; Ma et al., 2002, 2003; Stearns
and Glick, 2003; Grossman and Hansen, 2001; Ton et al., 2002).
It may also affect the rate of root infection by phytopathogens
that 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-
181
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 to
stress, 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-deaminase
cleaves ACC to α-ketobutyrate and ammonia (reviewed in Ma
et al., 2002). ACC-deaminase commonly occurs in soil bac-
teria (Li and Glick, 2001; Gosh et al., 2003), including the
pseudomonads (Campbell and Thomson, 1996), and in rhizo-
bia (Shah et al., 1998), where it stimulates the formation of root
nodules in leguminous plants upon infection (Ma et al., 2002).
Thus it is not beyond the bounds of possibility to modify crop
growth by manipulation of soil ethylene level via management
of ACC-deaminase–containing bacterial communities.
D. Feeding Soil Microbes
The 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 the
mainstream of agriculture in the U.S. because the scientific basis
of such amendments was poorly understood. However, it is in-
creasingly apparent that many of these materials and treatments
directly benefit or stimulate microbial populations by perform-
ing functions that directly benefit plants. Tailoring amendments
and cultural practices to promote beneficial soil microbes has
been an underappreciated area of crop production science that
offers potential for increasing agricultural productivity in a nat-
ural and sustainable manner.
It is already well established that sugars and amino acids are
released by decomposing plant material and can serve as carbon
sources for soil microbes. However, in modern crop production
monocultures that rely on mineral fertilizers, carbon sources can
become limited, especially where crop residues are removed
from 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-K
primarily intended to provide essential nutrients to crop plants
do not also benefit soil microbes. The point is that traditional
fertilizer inputs are intended primarily for crop plants and not
the microbes that sustain them. Even when soil organic matter
is low, relatively few agriculturalists would fertilize their fields
specifically to benefit soil microbes.
Even so, simple sugars, in the form of molasses, have often
been added to compost to hasten decomposition, and on occasion
they are used in small quantities by agriculturalists as a soil
amendment (Story, 1939; Schenck, 2001). The benefits of sugar
supplements have been reported for many years and include
no detrimental environment effects because they decompose in
soil to CO2 and harmless organic products (Anonymous, 1939
182 G. E. WELBAUM ET AL.

in Schenck, 2001; Story, 1939). As such, molasses have been

used as a carbon source for microbes in bioremediation of soil
contaminants (Park et al., 2002).
Using sugar as a fertilizer was found to increase sugarcane
yields, particularly on soils low in potassium (Schenck, 2001).
It has been suggested that molasses soil treatments effectively
reduced crop damage by root parasites (Anonymous, 1939 in
Schenck, 2001; Story, 1939). Vawdrey and Stirling (1997) ob-
served a reduction in the severity of root galling in tomato when
molasses was added without urea. Molasses applied to field
plots at relatively high rates lowered nematode soil populations
and improved papaya tree growth and harvestable fruit, and in
Chinese cabbage fields it decreased the numbers of Heterodera
nematode cysts following harvest (Schenck, 2001). Here it was
reasoned that the suppressive effects of sugar on nematodes were
due variously to antagonism by microorganisms in the soil that
were stimulated by molasses, changes in oxygen concentration
caused by microbial metabolism of molasses, or the release of
toxic compounds from decomposing molasses (Schenck, 2001).
Soils in wheat, ryegrass, bentgrass, and clover crops have all
been amended with sucrose to mimic rhizosphere carbon inputs
(Grayston et al., 1998). After treatment, microbial communities
were 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 utilized FIG. 1. Changes in the water content of Sunshine Mix growing media av-
by microbial communities from the different plant rhizospheres eraged from 3 12-celled trays without plants in a growth chamber following a
single treatment with 8 mL of water or 50, 60, 80, or 100 mM sucrose. Water
was shown (Grayston et al., 1998). Accordingly, different carbon contents were determined from fresh and oven dry weights. Sterilization of me-
sources may stimulate specific soil microbes so that microbial dia in an autoclave for 20 min prior to sugar treatment resulted in no increase
fertilization can be customized to benefit particular microbes and in water-holding capacity. Staining with alician blue, a carbohydrate-specific
thus the crops associated with them. Carbohydrates, carboxylic stain, revealed positive staining beginning 48 h after treatment. Bacteria from
acids, and amino acids were the substrates mainly responsible treated soils were cultured on high sucrose media and genetically identified as
Baccillus megaterium, a known producer of extracellular polysaccharide. Error
for this differentiation, suggesting that plants may differ in the bars represent ± SE.
selective 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 supplemented Rolland et al., 2002; León and Sheen, 2003). The concept of
with NH4 Cl (Omar et al., 2001). B. megaterium has the abil- sugars as central signalling molecules is relatively novel. Hex-
ity to solubilize inorganic phosphate (Cakmakci et al., 1992), okinase (HXK) has been found to be a glucose sensor that mod-
suppress Rhizoctonia root rot of soybean (Zheng and Sinclair, ulates gene expression and multiple plant hormone-signalling
2000), and produce polysaccharides (Bishop and White, 1993). pathways (Sheen et al., 1999; Smeekens, 2000; León and Sheen,
In greenhouse studies, B. megaterium isolated from sugar- 2003). Diverse roles of SNF1-related protein kinases (SnRKs)
treated potting soils displayed improved soil particle aggrega- in carbon metabolism and sugar signalling are also emerging
tion and increased water-holding capacity, which was considered (Halford and Hardie, 1998; Hardie et al., 1998). Recent molec-
due to his same exopolymer (G. Welbaum, personal communica- ular analyses have revealed direct, extensive glucose control of
tion) (see Figure 1). Similarly, soils amended with molasses had abscisic acid biosynthesis and signalling genes that partially an-
greater moisture retention in a pawpaw field study in Australia, tagonizes ethylene signalling during seedling development un-
although the authors did not speculate on a possible mecha- der light (León and Sheen, 2003). Glucose and abscisic acid pro-
nism (Vawdry et al., 2002). Sugars may also directly impact soil mote plant growth at low concentrations but act synergistically to
properties in ways not related to microbial activity. Molasses inhibit growth at higher concentrations (León and Sheen, 2003).
and gypsum, applied either alone or combined, improved the Sugar molecules modulate many vital processes that are
structural stability of two sodic soils by decreasing dispersion also controlled by hormones during plant growth and develop-
and/or slaking (Suriadi et al., 2002). ment (Smeekens, 2000; León and Sheen, 2003). For example,
Apart from their trophic role, sugars also have a hormone- trehalose (∝-D glucopy-ranosyl-[1,1]-∝-D-glucopyranoside),
like function as primary messengers in signal transduction in a nonreducing disaccharide common in fungi and bacteria
plants and certain microbes (Koch, 1996; Smeekens, 2000; that does not accumulate in plants but is involved in the
 MANAGING SOIL MICROBES
regulation of plant growth and stress responses (Godjin and van
Dun, 1999; Ho et al., 2001). Transgenic plants expressing the
Escherichia 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; Romero
et al., 1997).
The mechanisms by which trehalose metabolism alters plant
development are not entirely known. Seedling growth has been
inhibited after treatment with 25 µM trehalose (Aeschbacher
et al., 2000). Similarly, Shen and Welbaum (2004) found
that 15 mM trehalose reduced both root and hypocotyl growth
of alyssum and muskmelon by approximately 15%. Thus, mi-
crobially derived trehalose may similarly affect plant growth
and development. The fact that sucrose, trehalose, and other
sugars are not just simple molecules providing carbon and en-
ergy source but are also involved in sensing and signalling
pathways 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 of
sugars and amino acids along live roots in an intact soil–root
matrix with native microbial soil flora and fauna present. Jaeger
et al. (1999) genetically engineered Erwinia herbicola 299R to
contain a promoterless ice nucleation reporter gene, driven by
either of two nutrient-responsive promoters, for use as a biosen-
sor. Both biosensors exhibited up to 100-fold differences in ice
nucleation activity in response to varying substrate abundance
in culture (Jaeger et al., 1999).
Plants leak nutrients that nourish soil bacteria, which in
turn benefit plants by protecting then from disease (Zheng and
Sinclair, 2000; Vessey, 2003), stimulating plant growth, increas-
ing nutrient availability (Cakmakci et al., 1992), or, in the case
of B. megaterium, secreting polysaccharides (Bishop and White,
1993; Gandhi et al., 1997) that help both the bacteria and plants
avoid 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 a
wide range of soil microbes (Roberson et al., 1995). EPS con-
tribute to the stability of soil aggregates and are important factors
affecting soil structure in cultivated soils. In studies of tomato
production 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 taxonomic
order Glomales (Wright and Upadhyaya, 1996). Glomalin is
thought to seal and solidify the outside of the fungi’s hyphae that
transport 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
183
for soil carbon and increases soil water-holding capacity while
retaining soil structure and aeration, and soil stability to resist
erosion (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 arbuscular
fungi to produce more glomalin. Thus at CO2 levels of 670 µL
L−1 arbuscular mycorrhizal hyphae grew longer and produced
five times as much glomalin as fungi on plants grown under
ambient 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 most
of these products are advertised as enhancing plant growth, or
increasing stress tolerance, the stimulation of bacterial growth
may 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 organic
matter. Much of the humic acid research has dealt with its cre-
ation, function, and longevity in soils. Relatively few studies
have 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, since
humin is often broadly used to describe a mixture of materials
that 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 as
polysaccharides.
Tailoring inputs to feed soil microbes has not been
widely practiced. As our knowledge of soil microbial com-
munities progresses, more precise rhizosphere management
practices—enhancing soil and plant health and the overall crop
productivity—can be developed.
V. PRECISION MANAGEMENT OF A SUSTAINABLE
AGRO-ECOSYSTEM—PROGRESS AND FUTURE
In general, agricultural production tends to focus on practices
designed to manage nutrients, water, weeds, and crop diseases.
Precision agriculture and integrated pest management programs
have gone one step further by recognizing the need to target
inputs where they are required in the field. Here the objective
has 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 further
refined by the development and integration of new technolo-
gies, including new crop cultivars that capitalize on the holistic
management 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 and
their associated microflora, the introduction of the new ways
of microbial population management, and the development of
real-time monitoring and diagnostic devices, will favor timely
production interventions.
184 G. E. WELBAUM ET AL.
A. Plant–Microbial Ecosystems
Certainly from the above discussion there is support for the
view that the functional biodiversity of soil organisms can be
linked with the maintenance of soil functional processes. As a re-
sult, the study of soil food webs—the interrelationship between
biological 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 the
focus of intense interest in recent years. Even so, our knowl-
edge of the interaction between soil food web decomposers and
their 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 interactions
that 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 various
niches? What signal molecules are involved in nutrient sensing
and how are they exchanged between plants and their coloniz-
ing microflora? How do plants recognize beneficial microor-
ganisms and differentiate them from pathogens? Suppression of
plant defenses in early stages of the rhizobia–legume symbio-
sis development (Mithöfer, 2002) and in mycorrhizal infection
(Garcia-Garrido and Ocampo, 2002) indicates that such differ-
entiation is indeed possible.
Developments in genomics, proteomics, and metabolomics
provide new tools that will allow us to study genotype × en-
vironment molecular interactions (Bouchez and Hofte, 1998;
Briggs, 1998; Phillips and Freeling, 1998; Sommerville and
Sommerville, 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 essential
if we are to develop new approaches to the management of
agro-ecosystems.
Breeding plants for sustainable agricultural production sys-
tems will incorporate newfound disease resistance genes (see
reviews 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 signal
molecules in plant responses to environmental stresses, e.g., tre-
halose (Schiraldi et al., 2002), linear ß-1,3 glucans (Klarzynski
et 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 and
Salamini, 2003) genome sequencing, functional genomics (e.g.,
Askenazi et al., 2003), and in silico interaction of metabolic
networks modeling (Price et al., 2003) on the other, will in-
crease the number of breeding options and selection criteria
available to plant breeders. Certainly communities of microor-
ganisms and their host plants could benefit from closer genetic
links (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 affect
plants but also influence rhizomicrobial composition (Probanza
et 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-associated
bacteria can also switch between culturable and unculturable
forms (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 in
any population (Sessitsch et al., 2002). Moreover, a combina-
tion of molecular techniques and electron and epifluorescence
microscopy have opened up possibilities to study bacteriophages
in natural ecosystems (Asheford et al., 2003). These bacterial
viruses may play a significant role in the management of bacte-
rial populations, as their numbers seem to be much higher than
estimated before and may reach, on average, 1.5 × 108 g−1 of
soil (approximately 4% of the bacterial population) (Asheford
et al., 2003). Such powerful analytical tools will enable us to
better 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 plants
and beneficial organisms and understanding the molecular and
biochemical mechanisms of signal recognition and transduction
that occur in plant–microbial interactions under different envi-
ronments are most challenging study elements.
B. Soil Priming
Soil structure, its overall health, and crop yield potential can
be modified by cultural practices. However, the concept of “soil
priming,” which we interpret as setting the “readiness” of a
specific soil to receive a selected crop, is still new (Yunasa
and Newton, 2003). For example, the design composition of
a 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) for
the establishment of soil microbial communities (Yunasa and
Newton, 2003). Integration of legumes, which secrete com-
pounds recognized as signal molecules by rhizobacteria, into
life-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 of
nonhost plants by enhancing seed germination and early seedling
growth (Prithiviraj et al., 2003). Moreover, nodules of several
legumes produce high levels of hydrogen gas, which stimulates
proliferation of beneficial bacteria in the rhizosphere, improving
 MANAGING SOIL MICROBES
growth of cereals in rotation (Dong and Layzell, 2001; McLearn
and 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 Propagules
Despite decades of extensive investigation of seed inoculation
with beneficial microorganisms (seed biopriming) (McQuilken
et al., 1998; Dobbelaere et al., 2003; see reviews by Bennett
et al., 1992; Callan et al., 1997) and tuber (Burr et al., 1978;
Burr and Caesar, 1984; Lynch, 1990), the full potential for the
utilization of these natural allies has never been achieved.
A promising new area is that of induced-resistance responses
in 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 acquired
resistance (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 Meyer
and Höfte, 1997; De Meyer et al., 1999). Other rhizobacteria
activate 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 model
plant Arabidopsis thaliana, using Pseudomonas fluorescence
strain 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 in
plants 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, and
oomycete leaf pathogen Peronospora parasitica, and bacterial
leaf pathogens Pseudomonas syringae pv. tomato and Xan-
thomonas campestris pv. armaraciae (Pieterse et al., 1996; van
Wees et al., 1997; Pieterse et al., 2000).
Simple seed inoculation with beneficial organisms has not
been successful (Dobbelaere et al., 2003), as such inoculants
must 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 selected
microbial strains and/or strain combinations by sterile (or rela-
tively sterile) plant propagules. In vitro and ex vitro bacterization
and mycorrhization of vegetatively propagated material is cur-
rently being explored as an efficient way to improve production
practices of high value horticultural crops (reviewed in Nowak,
1998; Nowak and Shulaev, 2003; Rai, 2001). The use of en-
185
dophytic bacteria seems to be particularly promising (Nowak
and 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 tissue
culture plantlets to improve transplant establishment (Nowak
et al., 1999) and early vigor (Lazarovits and Nowak, 1997)
has also been found to increase resistance to biotic (Sharma
and Nowak, 1998; Barka et al., 2002) and abiotic (Bensalim
et al., 1998) stresses. Similar introduction of nitrogen-fixing en-
dophytes (other than Rhizobia) into clonally propagated plants
could 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 cane
plantlets with Acetobacter diazotrophicus, in vitro; and these
bacteria were reisolated from plants thirty days after transplant-
ing, demonstrating successful colonization.
The development of stable artificial associations between
plants and nitrogen fixing diazotrophic bacteria have also been
described 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 (Varga
et al., 1994), strawberries (Preininger et al., 1997), tomato,
potato, wheat, sugar cane, and poplar, using 11 strains of 8
Azotobacter species (Sz. S. Varga, personal communication). In
the tomato system, the bacterium could be transmitted through
seeds; approximately 20% of seedlings derived from the seeds
of 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 bacteria
on nutrition and growth of various crops have been demonstrated
by Paula et al. (1991, 1992). This promising finding, combined
with a substantial body of literature describing the presence of
“mycorrhiza helper bacteria” in natural ecosystems (see reviews
by Garbaye, 1994; Founoune et al., 2002) needs to be explored
further.
The development of a defined coculture microbial–plant mi-
croecosystem to study complex plant–microbial environment
interactions (Nowak and Shulaev, 2003) would contribute to the
overall understanding of the plant growth ecosystem (Probanza
et al., 2001) and the development of new technologies for stress
management and yield enhancement in plants. In this way, the
large-scale production of microbial propagules, seeds, tubers,
cuttings, or grafted transplants containing endophytic and/or
epiphytic microbial populations designed for specific planting
sites and/or crop rotations would contribute significantly to the
creation of sustainable agro-ecosystems.
D. “Microbial Precision” Production Systems: The
Development of the “Smart Field” Concept
Precision agriculture became a popular term in the 1980s to
describe the use of the Global Positioning System (GPS) to tailor
186 G. E. WELBAUM ET AL.
inputs and map productivity to specific geographical locations
within 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 the
rhizosphere while monitoring soil and plant health, in real time.
Although much progress has been made in understanding those
factors 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 to
design “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 in
plants, 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 in
the agro-ecosystem linked to soil and plant “health” (Passiora,
2002a; Paulitz et al., 2002; Ryszkowski et al., 1998; Stine and
Weil, 2002).
Today, genetically based microbial profiling (Sessitsch et al.,
2001, 2002) allows us to link microbial population dynamics to
soil type and farming inputs and outputs. Most microbial ecology
studies on this topic focus on the management of rhizosphere
diseases, 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 on
resident microbial populations (both exo- and endoplant) have
only begun to be considered (Kinkel, 1997; Andrews and Harris,
2000).
Adaptation of environmental probes based on nanosensors
for agro-ecosystem monitoring would allow the development
of “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, and
ethylene) could be monitored in real time and at multiple loca-
tions in the field. Such probes could be integrated into arrays and
linked to a computer-based “monitoring/command” system that
turns on specifically prescribed response inputs to correct for
imbalances that might arise. Changes to the rhizosphere could
be rapidly made through a subsurface irrigation system (e.g.,
http://www.irrigro.com/; http://www.gravityline.com/) buried to
a 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/or
signal 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 attention
could be paid to field site preparation prior to planting (soil prim-
ing) to reduce soil-borne disease pressures and thus postplanting
inputs.
Smart Field technology, combined with microbial popula-
tion analyses, offers the possibility of (1) further improving our
understanding of interactions within the soil microbial–plant
ecosystem; (2) better enabling the identification of indicators
of soil and plant health status, allowing for early interventions
and thus reducing the requirement for inundative system inputs;
(3) creating a scientific “workshop” for the development of new
sustainable 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 health
status parameters.
ACKNOWLEDGEMENTS
The 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 State
University), to literature searches, and Mrs. Maura Wood’s help
with manuscript preparation.
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