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Intellectual nucleation,
like its physical counterpart, derives from small, spontaneous, and
unusual juxtapositions that produce positive feedback. Such potential
for intellectual nucleation was seen June 1 through 3, 2001, in a
meeting organized by the Rhizosphere Biology Initiative at the
University of California (Davis). The unusual juxtaposition of
molecular biologists, ecologists, modelers, and evolutionists
precipitated opportunities for productive discussions and friendly
hectoring, which had been previously unavailable. The result for all
was a greater appreciation of complexity in the root zone and an
increased willingness to consider viewpoints expressed by previously
faceless colleagues who study different levels of concentric processes
in that nexus of genes, molecules, organisms, and food webs that
comprises the rhizosphere.
Until recently, the difficulty of working underground has kept the
rhizosphere in a scientific state of "out of sight, out of mind,"
except to the most intrepid, mainly agricultural, researchers concerned
with plant nutrition and disease prevention. Many workers have
commented on the dearth of knowledge about this scientific frontier
beneath our feet. Although those assessments are largely valid in the
sense that the organismic interactions in rhizospheres are poorly
defined outside of a few species of microorganisms important as
pathogens or symbionts, what is missed is the wealth of molecular data
and tools developed for work in laboratory rhizospheres with
microbiologically controlled conditions. These new molecular tools,
together with fiber-optic monitoring systems and advances in
measurement of physical discontinuities, offer opportunities for
addressing many significant ecological issues.
The University of California (Davis) symposium "Rhizosphere Control
Points: Molecules to Food Webs" was an attempt to develop an
integrated picture of rhizosphere biology by discussing the newest
discoveries, hypotheses, and directions for future investigations among
the previously noncommunicating fields loosely comprising contemporary
rhizosphere biology. Represented at the meeting were workers interested
in fundamental plant biology, molecular pathogenesis and symbiosis,
receptor biochemistry, new signaling paradigms, evolutionary theories
of root-microbe mutualism, and synergies of multiple species in
rhizosphere food webs. Floating over the meeting and guiding aspects of
the discussion were the mathematical modelers hawking their wizardry of
direct, indirect, synergistic, and chaotic interactions among
rhizosphere organisms and processes.
General discussions among the 75 participants
(http://agronomy.ucdavis.eduucd-rbp/Symposium/Participants.html)
ranged widely, but a dominant theme was the need to maintain healthy,
productive rhizospheres. The immense practical importance of
rhizospheres to agricultural and other terrestrial biomes impels their
study beyond mere curiosity-driven research. It is clear that humans have an interest in maintaining their green earthly shield, which is
linked through rhizosphere ecology to the mineral substratum. Guenther
Stotzky (New York University) made the cogent point that root
zones are the detrital repository for genetically modified plants.
Today, although the main products of such plants are human or animal
food and cotton fiber, the near future may see genetically modified
plants yielding pharmaceuticals. If this occurs, then current fears
about the release of Bacillus thuringiensis toxins may be
replaced with more serious concerns for the root zone as additional
complex molecules become available for binding to surface-active particles in soil. Fergal O'Gara (National University of
Ireland, Cork) noted that many genetically modified bacteria with
improved traits for biocontrol or symbiosis currently have been proven safe for use, but he emphasized that continued testing will be important as new or multiple traits are added to these bacteria in the
future. Linda Thomashow (Washington State University, Pullman) gave examples of the genetic information now available for using Pseudomonas bacteria to control important fungal
pathogens in the rhizosphere.
A second element of general discussion distinguished the rhizosphere as
an environment that is more viscous and finely heterogeneous for the
plant than either the aboveground aerial or purely aquatic milieus
where plants find themselves. Owing to the traits of soil as modified
by the living root and decomposition, the rhizosphere is an environment
through which dispersal is more limited and in which ecological
neighborhoods are smaller, grain is finer, and abiotic factors
(gravity, moisture, temperature, and nutrients) vary over shorter
distances than the other two main biomes in which plants grow. Despite
this fact, diffusion, leaching, and species interactions can project
rhizospheric influences into soil away from the root. Steven
Lindow (University of California, Berkeley), through analogy to
his work on leaf surfaces, described how molecular sensors that monitor
specific compounds can measure the chemical ecology of rhizospheres at
a scale useful for management and modeling. It is clear that many more
in situ measurements are needed, and microorganisms and fiber-optic
probes are better suited for that task than traditional tools, such as shovels.
Powerful, poorly understood synergies evident in rhizospheres were a
major topic of discussion. These traits develop through both continuous
and discontinuous interactions. Common mycorrhizal networks discussed
by Caroline Bledsoe (University of California, Davis) are
physically continuous connections that move nutrients among multiple
individuals and species of plants connected by various species of
fungi. Equally common, discontinuous networks known as food webs move
nutrients through multiple predators, prey, and various interactive
species. Heikki Setälä (University of
Jyväskylä, Jyväskylä, Finland)
demonstrated that constructing food webs by adding soil fauna (mites,
enchytraeid worms, collembola, etc.) to coniferous seedlings already
colonized by microorganisms can increase plant growth markedly. This
response, which is tremendously important in forests, currently is
explained by the additional mineral nutrients that are released through
faunal grazing on the rhizosphere bacteria and fungi.
Setälä's experiments demonstrate that plant growth is
regulated by species several trophic steps away from the plant. Don
Phillips (University of California, Davis) suggested that,
although mineral N released by nematodes preying on microorganisms is a
major component of the plant growth stimulation by rhizosphere food
webs, bacteria can be viewed as more than simple bags of N fertilizer.
His data showed how bacterial metabolites, such as lumichrome and
homoserine lactone, can affect root respiration and transpiration,
respectively, when supplied to roots at nanomolar concentrations.
One crucial aspect of rhizosphere food webs involving predator-prey
relationships is the concept of "indirect interactions." This idea,
in which the influence of one species upon a second indirectly affects
a third, is best exemplified by a phenomenon called "trophic
cascades." Don Strong (University of California, Davis) and
his associates recently showed for the first time that trophic cascades
with large aboveground effects occur in the rhizosphere of a sea coast
lupine. Plant deaths caused by root-feeding insect larvae are virtually
eliminated when nematodes that kill the root-feeding larvae are
present. Thus, the nematodes have an indirect, beneficial effect on
plant survival that cascades through the trophic level occupied by the
insect grubs. At this conference, Strong discussed how nematode
suppression of the insects is the end of neither the story nor the
cascade. Fungi that kill these nematodes are abundant in lupine
rhizospheres and constitute a fourth level in the nematode-insect-plant
cascade. It is possible that huge lupine "die-backs" caused by the
root-feeding insects are the result of these fungi suppressing the
predacious nematodes. Exactly how such underground trophic cascades
evolved is unclear, but if they parallel aboveground interactions, then
signals involving plants, nematodes, and/or insects may have been
coopted by the nematode-eating fungi. Such deceit is detrimental to the
plant, but the potential complexity of the molecular interactions
served as a strong stimulant to meeting participants.
The dynamic nature of synergies was the topic of a presentation by
Kevin McCann (McGill University, Montreal), which hinged on his
view that weak interactions stabilize, and perhaps control, rhizosphere
food webs. Orthodox ecological theory suggests that complexity
destabilizes food webs. With more predators and competitors, probability increases that common prey and common predators are driven
to extinction. This destabilizing effect increases at a rate faster
than the numbers of species in the model food webs that gave rise to
the orthodox result. Thus, the large number of interacting species that
we see in rhizospheres is an enigma. McCann's recent results show that
some types of weak links are control points in networks of consumers
and resource species; weak links can increase stability by acting to
dampen oscillations of predator and prey species. McCann stressed that
not all weak interactions increase stability. In the rhizosphere, links
that buffer resource species away from zero are most likely to increase the stability of networks. One implication is that species that appear
to be insignificant in terms of pair-wise interactions can serve as
crucial weak integrators in indirect interactions of trophic cascades
and other interaction networks of the rhizosphere. John Moore
(University of Northern Colorado, Greeley) supported the view
that weak interactions are important and proposed how predator-prey
relationships under differing levels of mineral nutrition might
establish either stable or unstable equilibria.
Mutualism in the rhizosphere was the major evolutionary theme discussed
throughout the weekend. Plant roots form a range of mutualistic and
facilitative interactions with microorganisms that equal the importance
of pollination and dispersal mutualisms that plant shoots form with
animals aboveground. Plant-microbe mutualisms are ancient and extremely
common. This presents an enigma of major proportions because ecological
and evolutionary views of interspecific interactions imply that
mutualisms should be delicate, unstable, and rare. The popular,
"everybody wins" view of mutualism is simplistic, because in the
short term, natural selection will eliminate lines that cannot protect
themselves against exploitation by their mutualistic partner. What
counters this drive? Bringing a fresh approach to models of mutualism, Mark Schwartz and Jason Hoeksema (University of California,
Davis) described rationalizations of "biological markets" and
"resource exchange mutualisms" that give a general context for the
balance of competing self interests of mutualistic partners. These
models suggest that specialization and exchange of two resources can lead to persistence of species that differ in resource competitive ability. Michael Kahn (Washington State University) used data from
various host-symbiont interactions to quantify the contributions made
by each partner to the symbiosis and suggested how specific biochemical
and/or genetic traits in the partners contributed to maintaining
symbiotic behavior.
Using a different approach, R. Ford Denison (University of
California, Davis) stepped down one level from the interspecific marketplace between two partners to focus on the tough intraspecific competition between different strains of
N2-fixing rhizobial bacteria infecting the same
host in mutualistic legume root nodules. If the host provides
photosynthate to fixers and non-fixers alike, then a strain may benefit
by parasitizing roots rather than fixing N2, but
the plant has a quite different perspective. Denison formulated a
testable hypothesis that plants may sanction nonperforming rhizobia by
cutting off the oxygen supply to the nodule and presented preliminary data supporting this intriguing concept, which leads to the important insight that plant sanctions against cheating bacteria could be a
fundamental mechanism for preserving mutualism. Ellen Simms (University of California, Berkeley) agreed that plant sanctions may
occur, but she placed greater emphasis on how plants might choose
bacterial partners that fix more N2, perhaps by
supplying more photosynthate. Thus, whereas Denison emphasizes the
stick, Simms highlights the potential for carrots in the interactions between plant roots and rhizobia.
Control of organisms and ecological synergies at the molecular
level was a point of great interest and considerable debate among
participants. Some scientists concluded that flow of mineral nutrients
is the most important determinant of rhizosphere activity, whereas
others recognized that plant genes regulate development of both
mycorrhizae and rhizobial root nodules in legumes. Thus, products of
these genes actually control the flow of mineral nutrients. Julie
Cullimore (Institut National de la Recherche Agronomique, Toulouse, France) illustrated the importance of signaling
processes in establishing the legume-rhizobia symbiosis and
pointed out that recent work has shown that certain plant genes
involved in transducing a rhizobial lipochitooligosaccharide (Nod
factor) signal are also involved in establishing a symbiosis with
endomycorrhizal fungi. The nature of plant receptors for microbial
symbiotic signals is an area of intense research activity. Marilynn
Etzler (University of California, Davis) reported progress
toward identifying one putative plant receptor for a Nod factor signal
and summarized the rigorous biochemical and genetic requirements that
must be met to draw such a conclusion.
Concepts of how rhizosphere organisms may take advantage of other
species and the role of deceitful signals in that process were
uppermost in the minds of several speakers. W. Dietz Bauer (Ohio
State University, Columbus) discussed his findings on
N-acetylated-homoserine-lactone signal-mimic molecules that
are released into the rhizosphere by plants. Many plant-associated
bacteria use N-acetylated-homoserine-lactones as
quorum-sensing signals to control processes that are linked to host
interactions and survival. Structures of the mimic compounds from
terrestrial plants have not been identified, but their biological activities suggest they can have major effects on rhizosphere bacteria.
The importance of other plant compounds for controlling oomycetes, such
as the plant pathogen Phytophthora sojae, was described by
Brett Tyler (University of California, Davis). Chemotactic responses of both the motile spores and the infective germ tube to
nanomolar concentrations of plant flavonoids show how this pathogen
finds its host. John Yoder (University of California, Davis)
used examples of how parasitic plants respond to host plant compounds
to show that chemical allelopathy at the scale of molecular signals
among fine roots occurs and is probably important in both natural and
agricultural systems.
Many participants felt that genomic tools offer
opportunities for new insight into rhizosphere biology. M. Kahn
(Washington State University) and Sharon Long (Stanford, Palo
Alto, CA) reported on recent progress in annotating the complete DNA
sequence from Sinorhizobium meliloti, the
N2-fixing symbiont of Medicago,
Melilotus, and Trigonella spp. Douglas
Cook (University of California, Davis) reported how rapidly
expressed sequence tag data in Medicago truncatula have been
accumulating and gave examples of how such information can be used to
understand infection by both symbiotic and pathogenic rhizosphere
organisms. David Bird (North Carolina State University, Raleigh)
described an expressed sequence tag project that has been initiated in
the plant-parasitic nematode Meloidogyne sp. and referenced
this information to the completely sequenced genome from the nematode
Caenorhabditis elegans. One interesting finding from this
work is the presence in Meloidogyne sp. of surprisingly close homologs of genes that have already been studied in S. meliloti for their role in forming legume symbioses. An intriguing
possibility is that the gene in Meloidogyne sp. was acquired
by horizontal gene transfer from S. meliloti. The
natural forces favoring horizontal transfer of such genes may be
substantial, and Clarence Kado (University of California, Davis)
reported new data on the mechanism used by Agrobacterium
tumefaciens to transfer Ti DNA into plant cells. One common thread
in all of these presentations was that following the genes will lead
one to a deeper understanding of the organisms, the interactions, and
the rhizosphere.
In the final analysis, although mineral nutrients are important, weak
interactions can have strong effects, synergies are everywhere, and the
ecologically exhilarating rhizosphere community of organisms depends
almost completely on the root for both its identity and its carbon
substrates. The heterotrophic root, in turn, depends completely on the
autotrophic plant shoot for photosynthate. Thus, most issues discussed
at this colloquium returned to the central importance of plant biology.
Martha Hawes (University of Arizona, Tucson), John Farrar, and
David Jones (University of Bangor, Bangor, Wales) summarized
how plant carbon resources in the form of border cells, mucilaginous
sheaths, and simple, biochemically defined exudates move into the
rhizosphere. The border cells, because of their semi-autonomous nature,
have much to tell us about evolution and the continuing dominance of
the plant in the rhizosphere. The other chemical carbon substrates released from roots are truly the building blocks of the rhizosphere, and yet, the mechanisms by which the root obtains photosynthate and
converts it into these exudates remain nearly as dark a black box as
the rhizosphere itself once was thought to be. It is clear that plant
biologists have an important role to play in defining rhizosphere
ecology for the ecologists.
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