A.V. Sturz, J. Nowak Applied Soil Ecology 15 2000 183–190 185
organizing forces that govern such communities need to be determined.
3. A strategy for creating stable microbial communities
When considering the anthropogenic introduction of new-colonists ‘beneficial microorganisms’ into
the root zone — through seed amendments or dur- ing seed-bed preparation — the potential for severe
negative interactions with autochthonous microbial populations should be borne in mind Atlas, 1986.
It is now appreciated that the microbiological pop- ulations of an ecosystem are able to interact with
one another through the production and reception of signalling molecules. Such signalling molecules
can subsequently influence gene expression, and thereby bacterial phenotype Salmond et al., 1995;
Albus et al., 1997; Surette and Bassler, 1998. ‘Quo- rum sensing’ describes one such signalling system,
whereby responses to bacterial population density are modulated through the accumulation of extracellular
signalling molecules, that can regulate an assorted range of metabolic processes Swift et al., 1996.
Similarly, the relationship between host and bacte- rial endophyte is not static. Communities of bacterial
endophytes may not only be host specific, but also plant tissue sensitive, reacting and adapting at certain
tissue sites and among certain tissue types within the host plant as it develops Sturz et al., 1999. The dy-
namic nature of bacterial phenotype expression, in this case antibiotic secretion, may be being governed by a
phenomenon analogous to ‘quorum sensing’ — which can also be influenced by environmental factors such
as oxygen concentration Sitnikov et al., 1995.
While positive interactions commensalism, mutu- alism, and synergism may enable some populations
to function as a community within a habitat Rayner, 1997, negative interactions may result in the exclu-
sion of microbial colonists from an established com- munity, or in a range of negative allelopathic events
Sturz and Christie, 1995, 1996.
In mature communities, positive interactions among autochthonous populations are usually better devel-
oped than in newly established communities. The successful establishment of beneficial organisms will
be influenced, to varying degrees, by the network of connections among species in a mature estab-
lished ecosystem. In essence, the establishment of the ‘new-colonist’ population can be prejudiced by
the dynamics of the ecosystem it is trying to invade, through a form of defensive mutualism Clay, 1988.
Thus, one component of an approach designed to favour the successful assimilation of selected organ-
isms into a rhizosphere, would be to introduce the ben- eficial microorganisms at the earliest possible stage
in the metapopulation continuum Levins, 1976; Hast- ings and Harrison, 1994. As endophytic bacteria have
been recovered from the ovules, seeds and tubers of a variety of plants Mundt and Hinkle, 1976; Holland
and Polacco, 1994, the creation of selected commu- nities of beneficial bacterial endophytes within these
germinal structures would form one of the earliest pio- neer colonization events possible. Initially, such com-
munities may be relatively stable and could compete with native soil bacteria once plant propagules had
been planted.
4. Engineering microbial communities
The ability to successfully manipulate endophytic bacteria in agricultural production systems will depend
upon the ability to select, incorporate and maintain beneficial microbial populations in the field. How-
ever, the reciprocity among populations of exo- and endorhizal origin has not been fully explored. If the
composition and function of endophytic populations is determined by co-existing rhizosphere populations,
then altering the exoroot community may be unde- sirable; especially where associations of co-operating
species occupy a single niche that could not be col- onized by either partner population alone Henry,
1966. A number of strategies may enable the early establishment of selected beneficial microbial popula-
tions within the host and in the surrounding field soil.
Biotization. One of the more elegant ways to in- troduce selections of endophytes into the host plant,
at an early stage, would be through tissue culture Varga et al., 1994; Nowak, 1998. Biotization, in the
current context, may be defined as the metabolic re- sponse of in vitro grown plant material to microbial
inoculants which promote developmental and physi- ological changes that enhance biotic and abiotic stress
resistance in subsequent plant progeny. Such systems
186 A.V. Sturz, J. Nowak Applied Soil Ecology 15 2000 183–190
allow for mutual adaptation between the host plant and the introduced bacteria Nowak et al., 1999; Sturz
and Nowak, unpublished data. The benefits of an established, thriving and stable microbial endoplant
community can include disease resistance, through the de novo synthesis of structural compounds and
fungitoxic metabolites at sites of attempted fungal penetration Benhamou et al., 1996, the induction
and expression of general molecular-based plant im- munity Richards, 1997; Sticher et al., 1997; Nowak et
al., 1998, or the simple exclusion of other organisms phytopathogens or colonists by niche competition.
Bacterized plantlets not only grow faster than un- bacterized plantlets Chanway, 1997; Bensalim et al.,
1998, but they are sturdier, have a better developed root system Nowak, 1998 and a significantly greater
capacity to withstand adverse biotic stresses i.e., drought and low level disease pressures Stewart,
1997; Sharma and Nowak, 1998. In potato culture, endophyte bacteria can be translocated to successive
generations of potato plants during multiplication, either through stem explants Frommel et al., 1991,
microtubers Nowak and Sturz, unpublished or in seeds Varga, personal communication. Of recent in-
terest to sustainable agriculture systems has been the realization that stable, beneficial associations between
plant species and diazotrophic bacteria Varga et al., 1994; Preininger et al., 1997 under conditions of low
soil nitrogen Gyurján et al., 1995 may be used to improve plant growth and crop productivity.
Crop production systems. Crop rotations and tillage management have been shown to influence specific
soil microbial populations see reviews by Alabou- vette et al., 1996; Sturz et al., 1997. Selecting crop
production systems which sustain and encourage the development of consortia of beneficial rhizobacterial
populations will be crucial, if the cumulative bene- fits of microbial synergies are to be harnessed. It is
likely that such benefits will be small in any given season, and their incremental value only recognized
over time. In this respect, the iatrogenic effects be- tween agrichemicals and non-target exo- and endo-
root microflora bears closer examination Ingham, 1985; Bollen, 1993, as long-term applications of
crop protection chemicals may adversely affect soil fertility by reducing the quantity and quality of bene-
ficial rhizobacteria populations Sturz and Kimpinski, 1999.
Cultivar selection. It is generally acknowledged that rhizobacterial populations can be manipulated, in the
short term, through plant species selection Neal et al., 1970; Grayston et al., 1998. Root exudates can
determine, to a great extent, which organisms will re- side in the rhizoplane Cook and Baker, 1983; Kunc
and Macura, 1988. Rhizobacteria can, themselves, spur a root exudation response in plants Bowen and
Rovira, 1976; Bolton et al., 1993 that is species spe- cific Chanway et al., 1988; Merharg and Killham,
1995. Such close interactions have prompted specu- lation that rhizobacteria and plants have co-evolved;
plants encouraging the establishment of specific and beneficial rhizospheres through the selective exuda-
tion of specific root exudates Bolton et al., 1993.
This close relationship between plants and rhizobac- teria is also found to extend to endophytic bacteria.
In some cases complementary crops grown in rotation can share 70 of the same species of endophytic bac-
teria Sturz et al., 1998. Such associations between different crop species can be cultivar specific. Thus,
certain cultivars of clover can foster the development of rhizo- and endophytic bacteria which favour the
growth and development of specific cultivars of pota- toes Sturz and Christie, 1998.
Genetic modification. Altering the genetic make-up of plants to manipulate both internal and external
bacterial populations offers the possibility of creat- ing preferred rhizosphere communities O’Connell et
al., 1996. Other than research into rhizobia–legume interactions, most selection criteria in plant breeding
programs have not considered which components of superior progeny performance are attributable to
the inherited ability of plants to respond to, modify or create communities of beneficial bacteria in their
rhizospheres. Even so, it is likely that there has been some collateral selection for host-endophyte interac-
tive ability.
To capitalize further on such associations, breeding programs could proceed in a number of directions. Im-
proved plant performance, based on superior interac- tions between host plants and their endophytes, could
result in yield benefits; either directly, or indirectly through a healthier, vigorous and more stress resistant
crop. Alternatively, selections could be based upon host responsiveness to specific beneficial bacteria,
which would then become a part of any bacterization step during multiplication, e.g. interactions between
A.V. Sturz, J. Nowak Applied Soil Ecology 15 2000 183–190 187
temperature, bacterization and potato genotype indi- cate the importance of clonal variations for utilization
of beneficial microorganisms in potato production under heat stress conditions Bensalim et al., 1998.
Several strategies have already been proposed to optimize endophyte nitrogen fixation in non-legume
crops, including: i altering the receptivity of the host plant to colonization by nitrogen-fixing bacte-
ria through nodule induction de Bruijn et al., 1995; Christiansen-Weniger, 1998; ii exploiting stable
plant–diazotrophic endophyte bacteria associations able to fix nitrogen endophytically Reddy and Ladha,
1995; Kennedy et al., 1997; Stoltzfus et al., 1997; Swensen and Mullin, 1997 and iii through the ge-
netic alteration of selected endophytic bacteria, or direct incorporation of nitrogen-fixing genes Dixon
et al., 1997; Gough et al., 1997. The reader is referred to reviews in Ladha et al. 1997.
Seed treatments. Judging by past experience, ap- plying bacterial seed treatments prior to planting does
not guarantee the establishment of a beneficial endo- or exorhizal flora Frommel et al., 1993 nor does it
always enhance yield Volkmar and Bremer, 1998. Introductions of non-local microfloras must compete
with established microbial communities in the soil, the rhizosphere and within the plant. Both true seeds
and plants which are propagated vegetatively are likely to carry enduring consortia of adapted endo-
phytes, a portion of which will be transferred to the subsequent progeny. Niche specialization will ensure
that local communities are better positioned to col- onize and retain niche dominance at the expense of
later introduced species. Our feeling, at the present time, is that seed treatments are best suited to aug-
menting established consortia of microbial organisms fungal, bacterial and mycorrhizal created as part of
a long-term strategy of harmonized crop cultivar selection and management practices.
5. Conclusions
