184 A.V. Sturz, J. Nowak Applied Soil Ecology 15 2000 183–190
In recent times the term ‘endophyte’ has been ap- plied almost exclusively to fungi Carroll, 1988; Clay,
1988; including the mycorrhizal fungi O’Dell and Trappe, 1992. However, a more comprehensive defi-
nition is one which includes ‘fungi or bacteria, which for all or part of their life cycle, invade the tissues of
living plants and cause unapparent and asymptomatic infections entirely within plant tissues, but cause no
symptoms of disease’ Wilson, 1995.
The recovery of bacterial populations from the en- dodermis and root cortex of plants has been used
to promote the idea that many bacteria in the rhi- zosphere are able to penetrate and colonize root tis-
sues Quadt-Hallman et al., 1997a,b. The inclusion of endophytic bacteria into the bacterial rhizosphere
community was proposed by Darbyshire and Greaves 1973, and supported by Old and Nicolson 1978.
In this model the root cortex becomes part of the soil–root microbial environment, resulting in a con-
tinuous apoplastic pathway from the root epidermis to the shoot, sufficient for movement of microorganisms
into the xylem Petersen et al., 1981. Thus, a con- tinuum of root-associated microorganisms exist which
are able to inhabit the rhizosphere, the root cortex and other plant organs Kloepper et al., 1992.
2. Exo- versus endoroot bacteria
Conventional classifications, based on function, have grouped rhizobacteria — both those that exist
outside exoroot and within root tissues endoroot — into two broad categories based on the relative
benefit they confer to the plants with which they are associated. Thus, the deleterious rhizobacteria DRB
Fredrickson and Elliott, 1985; Schippers et al., 1987, are so-called because they are considered to adversely
influence root health and plant well-being, while the plant growth promoting bacteria PGPR see reviews
by Glick, 1995; Arshad and Frankenberger, 1998 are considered to form part of a protective flora which
provide benefit to the plant in the form of enhanced root function, disease suppression and accelerated
plant development. The equivocal nature of such classifications has been pointed out by Nehl et al.
1996, as exoroot bacterial influence has been shown to fluctuate according to environmental conditions
Bakker et al., 1987; Chanway and Holl, 1994, host genotype Cherrington and Elliot, 1987; Åström and
Gerhardson, 1988 and collateral mycorrhizal sta- tus see reviews by Azcón-Aguilar and Barea, 1992;
Linderman, 1994.
Interestingly, root health and cell longevity can be viewed as exclusive of rhizobacterial influence. Henry
and Deacon 1981 proposed that, for most plants, rhi- zodermal and cortical cell death is an autolytic process
which occurs in the absence of microorganism activity. Thus, the conventional view of root internal coloniza-
tion by exoroot bacteria is one which occurs following rhizodermal autolysis Darbyshire and Greaves, 1973;
Foster and Rovira, 1978; Old and Nicolson, 1978. This led Foster and Bowen 1982 to consider that the
population densities of organisms in the rhizoplane are the result of cell death and not its cause.
In all the above examples the emphasis has been on the influence of exoroot bacteria. However, plants
can be colonized by a beneficial microbial endoflora prior to root autolysis Frommel et al., 1991; Nowak,
1998. The specificity between endoroot bacteria and their hosts Conn et al., 1997; Bensalim et al., 1998
is similar to that found in exoroot associations Neal et al., 1970; Bowen and Rovira, 1976; Miller et al.,
1989; Bolton et al., 1993; Merharg and Killham, 1995. van Peer et al. 1990 reported that endophytic
and exoroot bacteria from the same genera formed discrete sub-populations each suited to colonizing
their respective niches, and such adaptations do not appear to be easily reversible. McInroy and Kloepper
1995 observed that seed endophytes tend to develop into seedling endophytes. Bell et al. 1995, however,
considered endophytic and rhizosphere populations of bacteria to be distinct, based on differences in their
hydrolytic enzyme complement.
The community effect of endoroot bacteria on ex- oroot populations is seldom examined. However, the
endoplant bacterial community can modify root mor- phology Nowak, 1998 and ultrastructure Benhamou
et al., 1996 and may influence the way in which exoroot bacterial communities function and affect
plant growth Sturz, 1995; Sturz and Christie, 1995; Quadt-Hallman et al., 1997a. To paraphrase Andrews
1990, if we are to manipulate the assembled species and construct or enhance complimentary communi-
ties of endo- and exorhizobacteria that confer positive benefits for crop production, a fuller appreciation
of community structure and function, and the major
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
