Soil Born Plant Pathogens

ANNUAL
REVIEWS Further
Quick links to online content
1988. 26:93-121
Ann. Rev. Phytopathol.
Copyright © 1988 by Annual Reviews Inc. All rights reserved
EVOLUTION OF CONCEPTS
ASSOCIATED WITH SOILBORNE
Access provided by Punjab Agricultural University on 04/05/16. For personal use only.
Annu. Rev. Phytopathol. 1988.26:93-121. Downloaded from www.annualreviews.org
PLANT PATHOGENS
John L. Lockwood
Department of Botany and Plant Pathology, Michigan State University, East Lansing,
Michigan 48824
INTRODUCTION
This article reviews the development of major concepts in the field of

soilborne plant pathogens. In a previous essay (1 13), I emphasized rela
tionships among components within, and interconnections between, concepts
and theorems, whereas in this article I place greater emphasis on their
development. The four major concepts that provide the framework for this
review are: (a) that there exist in soil different ecological groups of root
infecting fungi, designated as soil invaders and soil inhabitants; (b) inoculum
potential, which includes as a component the stimulation of plant pathogens
by root exudates; (c) that hosts may be predisposed to infection and disease by
environmental stresses; and (d) that soil microorganisms can influence
pathogen survival and development.
SOIL INVADERS AND SOIL INHABITANTS
This concept is important historically because it provided the initial impetus

for several different lines of research and thought (113). It is derived from a
question that arose early in this century regarding the existence of a fungal
flora in soils. It was generally held that organic materials were decomposed
by bacteria, whereas fungi were thought to occur in soil only as dormant
spores deposited by chance from the air. However, Waksman's (175) discov
ery of fungal mycelium in soil strongly suggested that fungi must have a role
III decomposition. He further postulated the existence of two ecological
93
0066-428 6/88/0901-0093$02.00
94 LOCKWOOD
groups of fungi in soil (175); those characteristically occurring in soil were

"soil inhabitants"; transient sojourners of limited activity were "soil invad
ers. "
The distinction between an indigenous and a transient fungal flora is related
to the even older idea (33) of a zymogenous component of the fungal flora that
bursts into activity when presented with a suitable resource, otherwise
remaining quiescent, and an autochthonous component that maintains a slow
but sustained development, presumably on refractory substrates. There also
are exochthonous species, which enter the soil by chance but cannot maintain
themselves in an active condition (33). The soil-inhabiting fungi would

roughly correspond to zymogenous and autochthonous groups and the soil
invaders to the exochthonous group. The validity of these distinctions has
been questioned, however (33).
The categories of soil inhabitants and soil invaders were applied to plant
pathogens by Reinking & Manns (143), who studied the genus Fusarium in
Central American soils. Certain fusaria were found in all soils examined and
were therefore classified as soil inhabitants, whereas others were found only
in specific localities and so were classified as soil invaders. Among the latter
was Fusarium oxysporuni f. sp. cubense, the cause of banana wilt.
This latter finding led Garrett (59,60) to recognize two contrasting types of
behavior among root-infecting fungi: the soil-inhabiting parasites were re
garded as primitive, unspecialized parasites infecting seedlings and juvenile
root tissues (e.g. Rhizoctonia and Pythium species), for whom parasitism was
incidental to a saprophytic existence in soil; the root-inhabiting parasites were
considered more highly specialized, in that they were often host specific, their
destructive effect on the host was delayed, and their existence in soil was
transitory. Thus, pathogenic specialization was viewed as incompatible with a
well-developed saprophytic existence. Loss of saphrophytic ability in evolv
ing parasites was regarded as inevitable, with obligate parasites as the tinal
product in an evolutionary series (59, 61). Mycorrhizal symbionts were
regarded as the most highly evolved of root parasites, followed by the
vascular wilt fungi, then by the ectotrophic root parasites such as Gaeuman
nomyces graminis var. tritici (65).
Garrett's general scheme seems intuitively logical. The specialized wheat
root-infecting pathogen, G. graminis var. tritid, has low competitive
saprophytic ability compared to the less specialized pathogen, Fusarium
culmorum (63). Of two other wheat-root pathogens, the one, Cochliobolus
sativus, possesses low, and the other, Curvularia ramosa, high competitive
saprophytic ability; however, the relative parasitic specialization of these two
species is not clear.
The above evolutionary sequence has been called into question by recent
thinking in mycology (34, 142, 146). On this view, biotrophy (the ability to
CONCEPTS OF SOILBORNE PATHOGENS 95
exploit living host cells) and a broad host range are regarded as attributes of
primitive groups of fungal parasites of aquatic plants, from which necrotrophy
(the ability to derive nutrients from host cells killed by pathogenic activity)
and saprotrophy (the ability to live on dead organic matter) arose many times
as plants became terrestrial. It is noteworthy that present-day aquatic forms
such as the Chytridiales, Hyphochytridiales, and Oomycetes are represented
by a high proportion of parasites, including many biotrophs. Host specificity
occurs among both biotrophs and necrotrophs, while substrate specificity is
common among saprotrophs.
A broad host range has been cited as a primitive character and a narrow one
as advanced (61, 63). This may be true of strict biotrophs, but may not
necessarily be so for either facultative biotrophs or obligate necrotrophs. For
example, the vascular wilt pathogens Verticillium and Fusarium oxysporum
are regarded as specialized parasites (59, 61), yet Verticillium has a wide host
range, with little evidence of host specificity, whereas F. oxysporum has a
narrow host range with biotypes specific to species and even cultivars of
plants. By contrast, R. solani is generally regarded as a more primitive,
non-specialized parasite. Most pathogenic rhizoctonias can indeed infect
seedlings of many hosts, yet on older plants, they are rather restricted in their
host range. For example, sugar beet seedlings are readily infected by several
anastomosis groups of R. solani, but root rot of older plants is caused mainly
by isolates of AG2-2 (173).
Life History Strategies

Another perspective has been derived from general ecology. This is the theory
of r- and K-selection (33, 117). Briefly stated, individual r-selected organ
isms tend to be short-lived and allocate a large proportion of resources to
reproduction, whereas K-selected organisms tend to be long-lived and allocate
a small proportion of resources to reproduction. Andrews & Rouse (2) have
examined the applicability of this distinction to plant pathogens; although
plant pathogens as a broad category tend to lie near the r-extreme, there is
some diversity. Thus R. solani, a pathogen lacking asexual spores, but whose
hyphae have rela�ively large cells that can persist in soil, was considered to be
relatively K-selected. Pythium and Phytophthora were considered to be less
K-selected than R. solani, because sexual and asexual reproduction occur
frequently. Foliar pathogens were regarded to be more r-selected than root
pathogens, with rust fungi at the r-extreme.
Major and Minor Parasitizing Pathogens and Nonparasitizing

Exopathogens
The parasitizing pathogens are sometimes divided into "major" and "minor"
pathogens, depending on symptom severity. Minor pathogens are primarily
96 LOCKWOOD
those parasitizing root tips, root hairs, or superficial cortical cells of roots,
whereas major pathogens penetrate the cortex and endodermis and may enter
the vascular system (144). A third group might also be recognized: the
nonparasitizing exopathogens, also called deleterious rhizosphere microor
ganisms (149, 169, 188), which colonize rhizospheres, apparently without
infecting roots. They include bacteria as well as fungi, and while some cause
distinct and even severe symptoms, others suppress growth and yield without
producing other obvious symptoms.
Knowledge of this latter group arose from substantial yield depressions
occurring in potatoes grown with short rotations, in The Netherlands (149,

150). The causal agents appear to be bacteria, and there is some evidence that
the growth suppressions are caused by cyanide produced in the potato rhizo
sphere (15). Recognition of this new class of pathogens must be regarded as a
highly significant advance in the etiology of plant diseases. Further research
might reveal their connection with other examples of limited yields and
growth in short rotations or monoculture with other crops, with direct (no-till)
drilling, with "soil sickness," and with "replant" diseases such as those of
apple and citrus, which have long been unresolved problems (45 , 149, 150,
1 68).
The growth-suppressive effect of growing potatoes in short rotations has
been ameliorated by application of Pseudomonas bacteria that produce iron
chelating compounds (siderophores) that starve the exopathogens of the iron
needed for their growth (149-151) and for cyanide production (15) (See
"Microbial Antagonism").
The concept that soil fungi exist as two broad ecological groups has given
rise to several important lines of thought. The association of low populations
of F. oxysporum f. sp. cubense with specific soils (143) led to the idea of
pathogen-suppressive soils (see "Microbial Antagonism"). The concept also
has led to Garrett's notion of ecological groups of root-infecting pathogens; to
his opinion concerning the evolution of these fungi; and to his idea of
competitive saprophytic ability. Professor Garrett's penetrating insights, his
introduction and development of several of the key ideas in our field com
mand deep respect, even though in light of present-day knowledge, one might
find fault with certain aspects of these. However, as Garrett himself has said
(62), ". .. a wrong hypothesis often provides as much motive power as the
right one."
INOCULUM POTENTIAL
The term inoculum potential has had many meanings (9, 11), but I agree with
Baker (11) that its greatest utility lies in describing the "invasive force" of
inoculum, as proposed by Garrett (59, 63), who defined it as "the energy of
growth of a fungal parasite available for infection of a host at the surface of

the host organ to be infected." Some have included susceptibility of the host
plant as part of the concept (36), but to me this expands the concept to one of
disease severity (9) and consequently detracts from the focus on inoculum.
Inoculum potential consists of four components: inoculum density (or
number of propagules); the endogenous and exogenous energy of the prop
agules per unit; the genetic virulence of the propagules; and the abiotic or
biotic environment as it affects the inoculum. Although the inclusion of the
environmental effects was implicit in Garrett's concept of inoculum potential
(63), its importance was emphasized by Baker (9), who, with Benson ( 1 8),
provided experimental evidence for the effects of temperature on the in
oculum potential of R. solani causing damping-off of radish.
The concept of inoculum potential has been criticized as unnecessary; and
objections have been made to the inclusion of energy as one of its key
components, because the energy in question is unmeasurable (174). The
thesis that inoculum potential is based on the energy available to the inoculum
is probably an oversimplification. An adequate complement of hydrolases,
toxins, or other metabolites must be required for the invasion and colonization
of host tissues. However, production of these substances depends in
part on energy-supplying nutrients. In spite of these reservations, I have
found the concept useful in that it provides a focal point for information
about the invasive power of inoculum, and it has stimulated research on
this question.
Since in practice it may not be possible to measure inoculum potential or its
components directly, Winner ( 187) has proposed the idea of Infektionsdruck.
This describes the infective "power" or "pressure" of inoculum in a field,
based on the percentage yield increase of a resistant over a susceptible crop
cultivar. Thus, Infektionsdruck takes into account the number and severity of
infections over a season. It has been used for the classification of different
experimental fields with respect to specific pathogens. Diagrammatically,
Infektionsdruck is placed between inoculum potential and disease severity or
index (58). This seems a useful element of the concept of inoculum potential
in that it provides an objective measure of infective power.
I would divide the concept of inoculum potential into two parts: one dealing
with the energy or infective quality of the inoculum, and the other with
inoculum density (113). It could be argued that they should be combined since
increasing inoculum density increases the total energy or invasive force of the
inoculum. However, the increasing numbers of infections with increasing
inoculum density usually result from an increasing probability of infection by
individual propagules rather than from increased energy, at least up to the
concentration at which propagules may become close enough together to act
synergistically.
98 LOCKWOOD
Inoculum Density
The number of infections or of infected plants frequently is related to the
number of propagules. Baker et al (14) proposed models of the relationship of
inoculum density to number of infections based on a distribution of propa
gules on the vertices of regular tetrahedra. Baker then provided data
corroborating the predicted slopes, when plotted as logs of inoculum density
and numbers of infections (10). These models have been strongly criticized
(174), and there continues to be much discussion about the most appropriate
models to apply to the problem (68, 69).
The biomass of different pathogens in soil appears to be rather consistent

regardless of propagule size, i.e. smaller units occur in large numbers and
larger units in smaller numbers. Chuang & Ko (28) found a surprisingly close
(r = 0.95) linear inverse relationship between the logarithms of propagule
-
size and population density. Though population densities of a species can vary
quite widely, the results indicate an apparently fundamental relationship
between their size and their numbers in soil.
Population density in soil has been related mathematically to the average
distance between propagules, and by analogy to the average distance between
propagules and a root (13). The shape of the curve expressing this relationship
suggests that it might have evolutionary significance inasmuch as the mean
proximity of propagules to the root would not increase much at densities >ca.
3000/g, which is near the upper limit for populations of fungal pathogens in
soil (13,28). However, a corrected formula (119) gives a curve that flattens at
an inoculum density far in excess of most known inoculum densities of plant
pathogens in soil. Other factors seem more likely to determine maximum
inoculum densities in soil.
The number of infections is always much smaller than the number of
inoculum units at or near the host surface. This raises the question whether
infection occurs by single but relatively few propagules (independent action)
or by the joint action of several propagules (synergism) (63). There seems
little doubt that viruses, bacteria, and fungi can indeed infect by single units
(63). However, synergism might be expected when inoculum densities are
high enough for propagules to be close to each other. Dosage-response data
suggest that synergism occurs with R. solani (18). That zoospores of Oomy
cetes characteristically accumulate near host root tips suggests the possibility
of synergistic action; indeed, the joint action of multiple zoospores was
required to establish a sustained infection of bentgrass roots by Pythium
aphanidermatum (100). The extent to which obligate synergism occurs with
other zoosporic pathogens is unknown. Garrett (63) has suggested that the
requirement of hyphal aggregates such as hyphal cushions (R. solani), rhizo
morphs (Armillaria meUea), or mycelial strands (Phymatotrichum om
nivorum) for infection implies a synergistic interaction among the hyphae.
Inoculum density is not always related to the incidence or severity of

disease. The occurrence of little or no disease, even though the pathogen is
present at densities expected to produce severe disease, can be attributed
either to (a) decreased infectivity of the inoculum, or (b) interference with the
infection or disease development, usually via microbial antagonism.
Exogenous Energy
The exogenous energy component of inoculum potential is usually provided
by root-derived matcrials (63). Since both soluble and insoluble materials are
present in the rhizosphere, the term "rhizodeposition" has been proposed as

more encompassing than "exudates" (129). The rhizosphere is usually thought
to extend about 1 mm outward from the root, with respect to stimulation of
germination of fungal propagules. However, stimulatory effects of
rhizodeposition may occur at greater distances (133). The extent of the
rhizosphere is dependent on the metabolic state of the plant, the nature of the
soil (22, 136), and the sensitivity of the microbial propagule. Reported effects
at distances greater than 5-10 mm could possibly be due to volatile stimu
lants.
To avoid the implication of a maximum distance to which root-derived
exudates diffuse, Gilligan (69) proposed the term "pathozone" as "the region
of soil surrounding a host unit within which the center of a propaguie must lie
for infection of the host unit to be possible." Thus the pathozone would vary
in extent, depending on the propaguJe, and can be used with reference to
roots, seeds, and hypocotyls, as well as fungal propagules that exude nutrients
stimulatory to hyperparasites. This notion has the advantage of being more
widely applicable, but it seems likely that nonpathogenic members of the soil
microbiota would also be affected differentially according to their distance
from a root.
The products of rhizodeposition may (a) stimulate germination of quiescent
propagules in soil; (b) attract zoospores of Oomycetes to the root; (e) direct
growth of germ tubes towards the root; (d) stimulate the formation of infection
cushions in certain rhizoctonias; and (e) provide a food base to aid in infection
(157). Although it is generally assumed that plant pathogens are stimulated by
water-soluble components of rhizodeposition, there is some evidence that
infection of wheat roots by G. graminis var. tritici is benefitted by coloniza
tion of senesced cortical cells (90). For many pathogens that survive
saphrophytically in remnant host tissues, such as wood and straw colonized
through parasitism, the residues provide a food base from which nutrients are
transferred to the growing tips.
Recent findings using plants grown in atmospheres containing 14COZ have
revealed that 40% of total photosynthate, or 33-82% of the carbon translo
cated to the roots, is lost from plant roots via rhizodeposition n29 , 179).
100 LOCKWOOD
This loss must have enormous consequences for the inoculum potential of root
pathogens and also provides for interactions of these pathogens with other
microorganisms competing for the released materials.
Root exudates that stimulate germination of fungal pathogens are generally
nonspecific with respect to the fungi affected ( 1 57). However, an exception is
Sclerotium cepivorum. whose sclerotia are specifically stimulated in the
presence of roots and bulbs of Allium spp. (89). The active stimulants are
volatile thiols and sulfates produced in soil as microbial degradation products
of alkyl and alkenyl-L-cysteine sulfoxides in exudates.
One would expect that roots of crop cultivars that exude less should
stimulate germination of fewer pathogen propagules and have fewer in
fections and less disease. Germination of chlamydospores of Thiclaviopsis
basicola was much greater in rhizosphere soil of three host plants [bean,
cotton, and tobacco (47-56%)], than in rhizosphere soil from three nonhosts
[com, wheat, and kale (0- 1 4%) ( 1 34)]. Whether the lower rates of germina
tion in the rhizosphere of the nonhosts is related to their "resistance" is not
known. The entire area of rhizosphere populations and rhizodeposition, as
they affect root infection, seems to me to be a potentially fruitful field for
investigation.
There has long been interest in the possibility of altering root exudates
genetically to reduce root infections. Quantitative or qualitative differences
between the rhizospheres of resistant and susceptible plants have been demon
strated for flax and tobacco and the pathogens F. o xysporum f. sp. lini and T.
basicola, respectively (107, 171), for wheat and C. sativus (7),and for potato
and Verticillium dahliae (8). However, in no case has it been established that
the "resistance" was due to the alteration of the rhizosphere microbial commu
nity.
Root and even foliar pathogens can occupy rhizospheres and spermo
spheres of hosts and nonhosts as sites of survival (101, 156), and F. oxyspor
urn invades cortical cells of nonsusceptible weeds and crop plants (87). It
seems likely that the rhizosphere could serve as a site for survival of many
pathogens in addition to the few so far described as inhabiting this niche.
The fact that roots and other plant parts exude nutrients suggests that
microbial cells, including fungal propagules, might do the same. Motile
bacteria, including plant pathogenic bacteria, are attracted chemotactically to
fungal propagules (4), and bacteria extensively colonize the surfaces of fungal
propagules in soil (55). Fungal surfaces thus could provide an important niche
for bacteria in soil, and this bacterial occupation of fungi could in tum be
detrimental to the fungi (See "Microbial Antagonism").
Endogenous Energy
The concept of inoculum potential also encompasses the endogenous energy
component of the inoculum. Larger propagules of the same type (20, 74,
184), or larger propagule types of the same fungus (93), are more infectious
than smaller ones. Below a certain size limit, fragments of mycelial inoculum
of R. solani (74), or of crowns of wheat containing G. graminis var. tritid
( 184), were noninfectious; aggregations of several smaller particles, equal in
total volume to those of larger fragments, remained noninfectious or were less
so than an equivalent mass of larger fragments. The inoculum potential of the
fragments of R. solani was related to their ability to produce the hydrolytic
enzymes cellulase and polygalacturanase ( 106). There was some tendency for
the sclerotia of Cylindrocladium crotalariae recovered from field plots with
resistant soybeans to be smaller than those from plots cropped to susceptible

cultivars (20). This phenomenon could be of epidemiological significance,
since the smaller sclerotia were less infective.
Complex structures, such as rhizomorphs, mycelial strands, and infection
cushions, have a higher inoculum potential than single hyphae. In fact, these
complex structures are required for infection of woody tissues by many
pathogens (59, 63). The same propagule type may have different inoculum
potentials, depending on its mode of germination. For example, the sclerotia
of Sclerotium rolfsii require a supplementary food base in order to infect by
"hyphal" germination, characterized by emergence of a few individual
hyphae, but require no food base to infect by "eruptive" germination, which is
characterized by emergence of a hyphal mass ( 1 4 1).
The concentration of energy substrate on which fungal inoculum has been
produced can significantly affect its inoculum potential. This was first shown
by Phillips ( 1 40) , who investigated conidia of Fusarium roseum f. sp. cere
aUs as the cause of stem rot of carnations. Weinhold and co-workers ( 1 77)
strengthened this concept in experiments with mycelium of R. solani grown in
media with varying concentrations of glucose or asparagine; equal quantities
of the inoculum grown in the richer media were more damaging to cotton
seedlings than those grown in the weaker media. The low virulence of
inoculum from the weaker media was overcome by applications of exogenous
nutrients, a circumstance consistent with the overall concept of inoculum
potential (59, 63). More recently, sclerotia of R. solani grown on media rich
in energy sources were more virulent on pea seedlings than those from weaker
media ( 120). These types of findings may also have relevance to inoculum
grown on natural substrates. For example, inoculum of F. solani f. sp.
phaseoli grown on bean stems was much more virulent to beans than in
oculum grown on barley straw (85). The greater infectivity of larger or more
enriched inoculum is frequently associated with more vigorous and more
distant growth of mycelium from its source (74, 1 77, 1 83a).
Once acquired, inoculum potential can also be lost. For example, incuba
tion of conidia of C. sativus and Cochliobolus victoriae in soil reduced the
capacity of the conidia to infect hosts (6, 149). Aging of inoculum can also
reduce its inoculum potential ( 103).
1 02 LOCKWOOD
While measurements of the energy contents of inoculum could place the

concept of inoculum potential on a firmer basis scientifically, its practical
determination will probably depend on other approaches, such as that of
Infektionsdruck, explained above.
It is worth repeating that, other factors being equal, numbers of infections
and disease severity should be proportional to inoculum density. However,
the prior nutritional history of the inoculum, its age, the size of the propa
gules, the associated microflora, and the abiotic environment all can affect
inoculum potential.
PREDISPOSITION
The concept of predisposition is part of a vast area of knowledge concerning

environmental effects on disease. It is difficult to condense such a large body
of information into one or few concepts, but the topic of predisposition is
sufficiently restricted that it can be so treated.
Even so, the concept has been viewed somewhat differently by different
people. Quite surprisingly, the concept of predisposition does not appear in
the encyclopedic treatise by Giiumann (66). Although he dealt at great length
with effects of the environment and genotypic constitutional changes in the
plant on its proneness to disease, he did not segregate effects occurring before
either infection or symptom expression.
Yarwood ( 192) and Colhoun (30) included in their treatments of the subject
the effects of environment and autogenetic changes (e.g. host age) as pre
disposing factors, and restricted the concept to events occurring before infec
tion. It was implied that susceptibility to infection could be either increased or
decreased. These would seem to be reasonable parameters for the concept.
However, it seems to me appropriate to include in the concept postinfection
environmental effects that result in latent infections becoming symptomatic.
In some instances ( 1 9, 73, 1 02, 1 04), stress conditions increase exudation
from roots, and the increased disease has been associated with the augmented
food base, which increases the inoculum potential of the pathogen. For
inoculum consisting of zoospores, increased exudation might also increase the
chemotactic accumulation of zoospores at the infection court, increasing
inoculum potential by this means also. Colhoun (30) regarded such phenome
na as outside the concept of predisposition, but to omit this subject seems to
unduly restrict the scope of the concept. It is probably appropriate to exclude,
as Yarwood ( 1 92) did, instances in which differences in exudates of resistant
and susceptible plants affect disease, since such differences are based on
genetic characters of the host.
Many abiotic and biotic factors can lead to infection and disease that
otherwise would not occur or would occur to a lesser extent. A partial list
CONCEPTS OF SOILBORNE PATHOGENS 1 03
includes: decreased photosynthesis (leaf diseases, shading, defoliation); salin

ity; soil compaction; mechanical shaking; high, low or freezing temperatures;
excess or insufficient soil moisture; nematode or virus infection; herbicides.
Though the effects on disease are well-documented, the underlying mech
anisms are not well understood, except in a few cases. Most such influences
increase disease severity in plants that were genetically somewhat resistant.
There appear to be few instances of the converse, i.e. resistance of susceptible
plants being increased by the aforementioned factors . However, the practical
value of investigations of predisposition is in identifying and quantifying
predisposing conditions and using this information to so manage the crop as to

avoid damage to it.
In much research on predisposition, the experimental design does not
permit a distinction between an effect on infection and one on disease
development, i.e. usually only the latter is addressed. However, infection of
roots and crowns of wheat by Fusarium roseum 'Culmorum' can occur
without predisposition of the host, in the semi-arid summerfallow region of
the northwestern United States, but root and foot rot are not manifested unless
drought stress occurs ( 1 34a). A combination of early (late August) planting,
high rates of nitrogen fertilizer, and narrow row spacing resulted in mid-day
leaf water potentials of - 35 to -40 bars by June, which greatly increased the
susceptibility of the plants. The disease can be lessened by reduced N
applications, later sowing, and wider row spacing, to conserve moisture. In
the case of com stalk rot, infection by a range of fungi can occur, apparently
also without host predisposition (99), but disease is not expressed until a
stress factor such as drought is imposed (38). Symptom expression in charcoal
rot diseases, caused by Macro phomina phaseolina, may be similar to that of
stalk rot, inasmuch as infection of soybean roots by the pathogen occurs
widely every year, whereas severe disease does not ( 1 9 1 ).
There are numerous instances of environmental stresses predisposing hosts
to increased severity of disease. Examples include exposure to cold of seed
lings of bean, pea, cucumber, and com, for diseases caused by R. solani
( 158); low soil moisture, low light intensity, or short day lengths, for fusar
ium wilt of tomato (54); salinity, in the case of phytophthora root �ot of
chrysanthemum ( 1 1 8); high temperature and low soil moisture (40, 1 3 1 ), or
the onset of host maturity ( 1 9 1 ), or an interaction between the two ( 1 9 1 ), for
charcoal rot of soybean or sorghum; drought stress, in the case of phytoph
thora root rot, of safflower (39), and rhododendron (21 ), particularly in
normally resistant varieties; and pre-inoculation flooding, for phytophthora
root rot of alfalfa ( 1 02). However, pre-inoculation flooding does not always
predispose plants to infection by Phytophthora spp. ( 1 6, 1 83). In all of these
instances, it is not clear whether infection could occur without the predispos
ing treatment.
Distinguishing between pre- and postinfection predisposition is important,
104 LOCKWOOD
not only from the standpoint of the basic understanding of mechanisms, but
also for the elaboration of strategies for disease management. In plants very
susceptible to infection, such as seedlings, the avoidance of pre-infection
stress during the period of greatest susceptibility should suffice to prevent
disease. Diseases induced by postinfection stresses might be kept low by
avoidance of stresses during the growing season. Furthermore, there may be
critical periods in the phenology of the plant when avoidance of environmen
tal stresses is more crucial than others. For example, early season drought
stress is more important than later season drought in predisposing com to stalk
rot (155). In addition, hosts whose root exudates are increased little by
environmental stresses should suffer less disease from pre-inoculation pre
disposition. This advantage may provide opportunities for germ plasm selec
tion.
MICROBIAL INTERACTIONS WITH PATHOGENS
According to its generally accepted definition, microbial antagonism in

cludes, as separate categories, competition, antibiosis, and parasitism and
predation (176). Antibiosis and parasitism and predation may also be consid
ered as mechanisms of competition (29). This latter classification is similar to
that used by plant and animal ecologists, who generally divide competition
into two types: exploitation and interference (121). The former is restricted to
the depletion of resources by one organism or population that does not reduce
the access of another organism or population to the same resource pool (Le.
nutrient competition); the latter refers to the behavioral or chemical mech
anisms through which access to a resource is influenced by the presence of a
competitor (antibiosis, and parasitism and predation). Lockwood (111) and
Wicklow (180) have applied these concepts to interactions between fungi, an
approach which Cooke & Rayner (33) have criticized as inadvisable, but
which Wicklow (181) has strongly defended.
I would distinguish coactions, in which a microbial population directly
interferes with a pathogen population, from interactions involving some larger
portion of the microbial community (or in some instances of a population) that
affect a pathogen population by altering the substratum in which the pathogen
exists, e.g. soil or plant residues. The latter category of interactions has been
termed "substrate antagonism" (113), but perhaps "substratum antagonism" is
more appropriate, as it implies an effect on the physical habitat rather than on
the food material. This is similar to the background or reaction antagonism
described by Park (135).
The idea that microbes in soil can interfere with root disease fungi arose in
the 1920s and 1930s as a result of three kinds of observations: (a) that it is
difficult to produce disease in wheat in natural soil artificially infested with c.
sativus, G. graminis var. tritici or F. culmorum, as compared with sterilized

soil ( 145); (b) that a small amount of natural soil and specific individual
microorganisms, added to sterilized soil and incubated for some days, sup
pressed development of root rot of wheat caused by C. sativus (75); and (c)
that the common scab of potato can be controlled by treating soil with green
manure or spent hops ( 128). Excellent accounts of this early history are given
by Sanford ( 145), and especially by Garrett (59, 60).
Coactions
Coactions between different microorganisms in culture media have been

recognized for many years and form a basis for hypotheses about the occur
rence of microbial interactions in soil and for conceiving measures to biologi
cally control plant diseases.
ANTIBIOSIS During the 1920s and 1930s, it was generally assumed that
microorganisms that interfered with root disease development in soil did so by
means of antibiosis. This possibility was studied extensively during the 1950s
and 1 960s (70), following the discovery of numerous antibiotic substances,
(many finding use in medicine) that were produced by microorganisms iso
lated from soil. These studies led to the conclusion that production of antibio
tic substances probably does not occur in the bulk soil due to an insufficiency
of substrate. Even if produced, these substances would be subject to chemical
or biological degradation or would be adsorbed onto soil colloids. This view
has recently been confirmed ( 186).
Although several investigators provided evidence during this period that
specific antibiotics could be produced in nutrient-rich microsites in soil (71,
1 89, 1 90), there is scant evidence for their production on roots or seeds in
soil. The best evidence for the latter thus far has been gained from genetic
manipulation of an antibiotic-producing strain of Pseudomonas fluorescens
that affords some protection of wheat against take-all ( 170). In greenhouse
experiments, transposon TnS mutants defective in antibiotic production were
less suppressive of that disease than the parent strain; however, antibiotic
production and inhibition of G. graminis var. tritici in vitro and on roots were
restored by complementation of the inactivated gene with wild-type DNA
introduced with a comid vector.
By far the most successful instance of biological control through antibiosis
is the control of crown gall by Agrobacterium radiobacter strain 84 (88).
Biological control capability among strains was associated with their ability to
produce the bacteriocin agrocin.
R. solani (79) and Pythium ultimum (80) on cotton seedlings are controlled
by seed treatment with a strain of Ps. fluorescens that produces two different
antibiotics, one active against each pathogen. Each antibiotic also afforded
106 LOCKWOOD
substantial protection against its corresponding disease. However, genetic

experiments have not been done, nor have the antibiotics been detected in
soil.
An antibiotic produced by the wheat pathogen Cephalosporium gramineum
may contribute to its saprophytic survival in wheat debris colonized during
pathogenesis (24). Antibiotic-producing isolates of C. gramineum survived
longer than nonproducing isolates in artificially infested, buried wheat straws,
and were more effective in excluding other fungi than isolates not producing
antibiotics. However, the role of the antibiotic has been called into question
by results showing that antibiotic and nonantibiotic strains of C. gramineum

survived equally well in naturally-infested straws in several soils ( 1 24). The
subject of antibiosis is treated in more detail in the articles by Fravel and
Weller in the present volume.
COMPETITION Competition, as a coaction, has been studied relatively little,

possibly because it is not readily recognized, or differentiated from antibiosis,
in agar tests. In fact, inhibition zones indistinguishable from those caused by
antibiosis can be produced by exhaustion of nutrients, at least by actinomy
cetes (81 ). The biological control of P. ultimum-induced damping-off of
cucumber and of other crop plants by bacteria applied to seeds has been
attributed to competition for carbon and nitrogen (44).
Siderophores are produced by fluorescent Pseudomonas spp. in iron
limited conditions, such as soil, and this form of competition has been
intensely investigated in recent years. On an iron-deficient medium, the
production of inhibition zones has led some researchers to regard siderophores
as antibiotics (92, 1 69). However, it seems more correct to consider them as
agencies abetting competition for iron. Some fluorescent pseudomonads pro
duce antibiotics in addition to siderophores (67).
Diseases caused by several major pathogens ( 148, 1 78) have been con
trolled experimentally by applications of fluorescent pseudomonads. More
over, growth promotion, apparently due to the prevention of root colonization
by parasitizing minor pathogens and nonparasitizing exopathogens also has
been achieved through these bacteria (67, 92, 149, 1 69). The evidence for the
involvement of siderophores in biological control and increased growth of
plants is strong (92 1 49, 169).
,
Baker and coworkers ( 12, 43, 147, 148, 16 1 ) have obtained evidence that
the suppressiveness to fusarium wilts of a Metz sandy loam from the Salinas
Valley of California is due to iron competition by fluorescent pseudomonads,
inhibiting germination and growth of F. oxysporum in rhizospheres. E1ad &
Baker (43) have claimed that competition for iron is the only mechanism so
far clearly identified that induces substantial suppressiveness in soil. Howev
er, there seems to be strong evidence that carbon competition plays a role in a
number of pathogen-suppressive soils ( 1, 1 12); indeed, gennination of
chlamydospores of F. oxysporum f. sp. cucumerinum was stimulated by

glucose and asparagine even in the suppressive soil from the Salinas Valley
( 1 6 1).
PARASITISM AND PREDATION Parasitism has been widely studied from the
standpoint of physiology ( 17) and ultrastructure (42, 77) of the host-parasite
interaction. Two broad types of mycoparasitic interactions are recognized
( 1 7 , 1 16): biotrophic, in which the parasite obtains nutrients from the living
cells with little or no apparent harm to the fungal host, at least early in the
relationship; and necrotrophic, in which the parasite destroys the host cells
before or soon after invasion. Most mycoparasitic interactions that affect the
persistent structures of soilborne plant pathogens are necrotrophic ( 1 1 6).
Little is known of the occurrence of mycoparasitism in soil, but the fact that
persistent structures of several pathogens were invaded by a variety of
mycoparasitic fungi in natural soils suggests that it may be of some im
portance in the regulation of the populations of these pathogens in soil ( 1 1 6).
Numerous attempts have been made to exploit mycoparasitism in biological
control ( 1 16).
The importance of predation upon pathogenic fungi by members of the soil
microfauna is even less well understood. Perhaps the most significant of such
predations, at least in terms of biological control studies, are those by the
mycophagous Collembola that graze the hyphae of R. solani in the rhizo
sphere of cotton (35) , and the mycophagous amoebae that perforate spores
and devour their contents ( 132).
Substratum Interactions
CARBON COMPETITION One of the basic facts of microbial life in the soil is
that these organisms exist in a milieu characterized by an insufficiency of
energy substrate ( 114, 185). A number of assessments of the energy inputs
into both natural and agricultural soils, and of the microbial biomasses that
this energy must support, all suggest that the soil is a grossly oligotrophic
environment, permitting only a few new microbial generations per year ( 114).
Fungistasis The concept of a generalized restriction on fungal germination

and growth in soils was first put forward by Dobbs & Hinson in 1953 (37).
They referred to it as a "widespread fungistasis in soils," and focused atten
tion on the nature of the inhibition and on its probable survival value to the
fungi, by preventing spontaneous germination in the absence of a potentially
colonizable substrate. Bacteria and actinomycetes are similarly restricted,
apparently by the same mechanisms as those affecting the fungi (94, 95).
Thus, it is appropriate to expand the concept of fungistasis to that of micro
biostasis (94).
The ability of microorganisms to impose fungistasis appears to be relatively
108 LOCKWOOD
nonspecific. Different isolates of actinomy cetes, bacteria, and fungi all im
posed some degree of fungistasis when used to infest sterilized soil ( l08), and
similar inoculations of an artificial soil imposed a general microbiostasis ( 76).
Even bacterial isolates, obtained with methods devised to increase the likli
hood of obtaining fungistatic isolates, were no more fungistatic or numerous
than isolates not so selected (47).
Most investigators (l08 , 1 10 ) have believed that soil fungistasis was caused
by inhibitory substances of microbial origin, but without substantial evidence.
Because of failure in my laboratory to find inhibitory substances in soil, we
began to evaluate the possibility that soils lacked sufficient available nutrients
to support germination (105, 108 ), a proposition that theretofore had general
ly been rejected.
Most of the fungistasis-sensitive propagules that we (96) te sted, notably the
smaller conidia, also failed to germinate in a small volume of distilled water,
suggesting that a similar deficiency of nutrients in soil could be the cause of
its fungistatic effect. On the other hand, some kinds of spores, such as rust
urediospores, powdery mildew conidia, and heat-activated ascospores of
carbonicolous Ascomycetes, all of which germinated freely on soil, also
germinated in distilled water (96, 182 ).
There was no obvious explanation, in terms of energy deprivation, why
some kinds of spores germinated in water, but not in soil. However, the
realization that a large microbial community exists with a chronic in
sufficiency of food, suggested that its total metabolic activity might deprive
the soil mass of any readily available energy sources. The soil microbial
community was viewed as a nutrient (energy ) sink, possibly causing excess
leakage of nutrients from neighboring fungal propagules via a steepened
diffusion gradient.
This idea was tested in model systems in which the diffusion gradient from
fungal propagules was artificially steepened by percolation of water or a salts
solution through a bed of sand on which the propagules, borne on membrane
filters, were incubated. Several kinds of fungal propagules incubated in these
systems failed to germinate or germinated poorly (23, 83, 96). Since the
systems are aseptic, any possibility of an exogenous inhibitor was ruled out.
By using 14C-Iabeled propagules, and measuring radioactivity in the
leachings, it was determined that exudation was in fact increased (23 ), and
was proportional to the flow rate of the leaching solution (162). Further,
germination was suppressed as flow rate and exudation increased (5 1 , 162).
Evidence for the existence of a microbial sink for energy substrates in soil
was first shown by the more rapid loss of glucose from paper disks incubated
on nonsterile than on sterile soil (109 ). Later it was possible to show that
losses of 14C from fungal propagules on soil also were elevated by measuring
14C02 evolved from, and 14C residual in soil (51 ). Losses of 14C from
propagules incubated in soil were equal to or greater than those in the model
system, which indicates that energy stress alone might account in large part
for the suppressed germination occurring in soil.
Direct evidence for the role of microorganisms in the energy sinks of soil
was obtained by coincubating several bacteria or fungal spores separated from
14C-Iabeled test propagules by a membrane filter (5). Loss of 14C was greater
in the presence than in the absence of the "sink" microorganisms. Moreover, .
the greater the loss of 14C, the less the germination. The inhibition of spore
germination apparently was due to nutrient stress, as inhibitory materials were
not found in sterile filtrates of any of the sink microorganisms incubated in the
presence of conidia of C. sativus (5, 105).
We had previously thought that the greater part of the 14C lost from fungal
propagules in soil was by way of exudation (51, 162) (we assumed that the
14C02 was derived mostly from respiration of fungal exudates by soil mi
crobes). Recent findings indicate, though, that more 14C02 is lost by pro
pagule respiration than by microbial respiration of exudates (M. Hyakumachi,
J. L. Lockwood, unpublished results).
Further support for the nutrient-deprivation hypothesis for soil fungistasis
was obtained by experiments demonstrating similar fungal behavior in a
natural soil and in a synthetic soil that was inhibitor-free ( 76 ).
A corollary of the nutrient-sink hypothesis for soil fungistasis is that fungal
propagules with long germination times should be more sensitive to fungista
sis than those with slower germination times, as measured by their germina
tion response in soil to which nutrients were added. This was the case ( 1 6 5). It
also was shown for different fungi that small conidia had longer germination
times than large conida. The same rationale would suggest that hyphae, which
are able to initiate growth immediately after contacting an energy source,
should be less sensitive to fungistasis than spores. This also was verified (82,
1 65). Among hyphae of different fungi, those with narrow hyphae and slow,
early growth rates (on agar) were most fungistasis-sensitive.
Interruption of progress towards germination, by transfer of the spores from
sterile to natural soil, resulted in a gradual regression towards the original
(ground) state (193 ). Loss, via respiration and exudation, of 14C taken up
during germination progress paralled closely the percentage regression.
Thus the extremes of spore size appear to represent different ecological
strategies. Species with large spores tend to germinate rapidly and to exhibit
low sensitivity to fungistasis. They give rise to large hyphae whose early
growth is rapid and relatively uninhibited in soil. These species may be better
adapted to exploit transient resources and thus tend to be more r- than
K-selected. The opposite is true of species with small spores; these also may
regress to the ground state if resources are of insufficient duration for
germination to occur, and they seem to be more K- than r-selected.
1 10 LOCKWOOD
The mechanism by which increased loss of 14C loss in soil leads to the
suppression of germination is not understood. That it represents a loss of
reserve materials essential for germination seems less likely than that it is in
some way a more subtle regulatory mechanism (46 , 1 1 2).
Energy source deprivation also appears to account for pathogen suppression
in environments other than soil, such as the suppressiveness of planting media
containing composted hardwood bark to damping-off caused by P. ultimum
(25, 26). The reduced germination of some fungi on leaf surfaces in the
presence of leaf-inhabiting saprophytes was explained by competition for
amino acids (4 1 ).
In some soils, volatile or nonvolatile inhibitors of biotic or abiotic origin
may play a role in fungistasis ( 1 10 , 1 1 2 , 1 14). The most likely candidate is
ammonia, which is detectable in some soils of pH > 7.0 ( 1 39, 1 52). Even
ammonia does not occur in all soils, and not all fungi are sensitive to it at the
concentrations at which it occurs. Other possible fungistatic agents are iron
chelating siderophores of microbial origin. Lockwood & Schippers ( 1 1 5 )
could find n o evidence for their role i n fungistasis in two soils, but such
metabolites appear to be involved in the inhibition of growth and germination
of chlamydospores of F. oxysporum in rhizospheres of plants (43 , 1 6 1 ).
However, the rhizosphere is not the arena of the fungistasis phenomenon.
Inhibitory substances might be subsidiary factors superimposed in some
situations on the widespread and pervasive fungistasis imposed by energy
deprivation ( 1 10 , 1 14).
Propagule debilitation The fungistatic mechanism protects the propagules

from spontaneous germination in the absence of a potentially colonizable
substrate-but apparently at a price. Propagules tend to become debilitated
with respect to germinability and inoculum potential after prolonged incuba
tion in soil, probably from loss of energy reserves (23, 52, 1 14). Losses of
14C from propagules can be considerable, e.g. ca. 20 % for conidia of C.
sativus or C. vicTOriae incubated on water-saturated soil for 5 days, but one
fourth that amount for sclerotia of M. phaseolina (50 ). Nutrient independence
in sclerotia of S. rolfsii incubated in soil at -0 . 1 bar matric potential was lost
when about 20 % of the sclerotia's 1 4C was lost, and death occurred when
about 40 % was lost; between these values infectivity declined (M. Hyaku
machi, J . L. Lockwood, unpublished results). Loss of inoculum potential,
like loss of germinability and of 14C, was imposed more or less nonspecifical
ly by individual microorganisms used to reinfest soil (3).
The imposition of fungi stasis and subsequent debilitation of fungal propa
gules might be augmented by bacterial colonization of the propagules. Motile
bacteria are attracted to propagules by their exudates (4), and fungal spores
may become extensively colonized by bacteria in soil (55). Spores so
colonized became less germinable, and lysed and died more rapidly than
spores not so colonized (56, 5 7).
Propagules that become debilitated due to energy stress may be invigorated
by exposure to energy-yielding compounds. For example, conidia of C.
sativus recovered a portion of their lost germinability through uptake of a
quantity of an energy substrate too small to support germination (52) , and
exposure of conidia to potato-dextrose agar or to certain sugars restored a
portion of their lost infectivity (3). These results suggest that the energy status
of dormant fungal propagules in soil is dynamic-an ebb and flow
depending on the extent of energy stress and the availability of energy

substrates.
Autolysis Energy stress also can cause the autolysis of fungal hyphae,
particularly of younger hyphae (9 7) . Autolytic enzymes capable of lysing the
hyphal walls were activated in soil or in the leached-sand model. Hyphal lysis
occurred under conditions that ruled out the participation of enzymes pro
duced by other microorganisms, but the possible involvement of heterolysis in
other circumstances, e.g. breakdown of older hyphae or the digestion of
hyphal remnants following autolysis, remains a possibility. The phenomenon
of lysis needs much more study, for its own sake as well as for its potential
usefulness in biological control of fungal infection ( 112).
Several mechanisms apparently have evolved that help young somatic
hyphae to compensate for their vulnerability to lysis. Lysis of germ tubes
causes death to many but not all propagules. Persistant propagules of some
fungi are able to regerminate several times after lysis of germ tubes in soil
(48 , 82, 1 64) , although at decreasing frequencies. It is important to know if
propagules of other fungi can survive the lysis of germ tubes and germinate
again.
Persistent structure formation Autolysis is linked with the formation of at

least some asexually produced persistent structures, in that it provides for the
mobilization of mycelial resources from which such structures are formed
(27). A similar autolytic mechanism is associated with chlamydospore forma
tion within macroconidia of Fusarium ( 1 53), with the formation of spor
ophores in some Basidiomycetes ( 130), and with the production of aerial
mycelium and spores of the Actinomycete Streptomyces antibioticus (126) .
Thus the formation of persistent or reproductive structures from mycelial
resources following the exhaustion of substrate may be a fairly general
phenomenon in mycelial microorganisms. What at first appears to be a
mechanism of self-destruction is then actually a means of survival, when
biomass is sufficient to support the formation of such structures, and perhaps
other conditions are fulfulled.
1 12 LOCKWOOD
Hyphal growth The hyphae of saprophytic fungi appear to be adapted for

conserving resources while maximizing their extension in soil, when energy
substrate is at a low level in soil ( 1 37, 1 38). Cytoplasm is transported from
substrate-depleted regions of the mycelium to new growing tips, without a net
increase in cytoplasm. This strategy, which preferentially allocates resources
to wall synthesis, is far less costly energetically than is cytoplasm synthesis ,
and i t Serves t o maximize the extent o f substrate exploration. This concept has
been formalized into a growth model ( 1 37) and verified experimentally ( 1 38).
The extent to which the modd can be applied to parasitic fungi in either their
parasitic or saprophytic existence in soil is not known: but A. B. Lloyd and I

(unpublished results) have observed this kind of behavior in the hyphae of R .
solani incubated o n soil surfaces.
In this section, I have discussed several responses of fungi to life in
energy-limited soil. Nonadaptive responses include the lysis of hyphae, loss
of germinability, loss of inoculum potential and reduced longevity. The last
three responses appear to be reversible by inputs of energy-yielding sub
stances . Adaptations to energy deprivation that enhance survival are the
production of persistent structures from products of mycelial autolysis, their
ability to withhold germination until presented with an energy source, the
capacity of some propagules to regerminate following germ tube lysis, and
cytoplasmic translocation within newly formed hyphal wall extensions. I have
commented elsewhere ( 1 12) on opportunities for the explOitation of some of
these aspects of fungal behavior for biological control.
NITROGEN COMPETITION The supply of nitrogen does not appear to limit

microbial activity in most soils ( 159), except when the carbon supply is
artificially increased ( 53 , 123 , 1 67). The use of plant residues of high C/N
ratio has made it possible to experimentally control bean root rot ( 125, 163);
apparently the residues limit the availability of nitrogen required for chlamy
dospore germination (32) and penetration growth ( 1 72) by the pathogen, F .
solani f . sp. phaseoli, i n soil. Barley straw has been employed i n the control
of bean-root rot in the western United States (8a). Straw plowed into the
pathogen-infested soil immobilizes nitrogen, but the bean roots are able to
penetrate more deeply and escape nitrogen starvation.
Nitrogen is important for the saprophytic survival of wheat root- and
foot-rot pathogens in the highly cellulosic wheat stem bases (63, 64). The
longevity of G. graminis var. tritiei and F. eulmorum, which was relatively
short in unsupplemented straw pieces, was enhanced by supplemental nit
rogen, whereas that of Phialophora radicieola and C. sativus, which was
relatively long in unsupplemented pieces, was reduced by supplemental
nitrogen. The contrasting behavior of these pathogens was explained by
differences in their mycelial growth rates and in their ability to decompose
cellulose. G. graminis var. tritici and F. culmorum had relatively inefficient

cellulolytic ability in relation to growth needs, and this was increased by
supplemental nitrogen. By contrast, P. radicicola and C. sativus had efficient
cellulolytic ability, even when nitrogen was in short supply. The reduced
longevity of these pathogens, when supplemental nitrogen was provided, was
attributed to competitive displacement by other microorganisms .
SUPPRESSIVE SOILS The historical origins and current status of this subject
have been described in numerous reviews (e.g. 3 1 , 1 54) , and certain aspects
have also been discussed elsewhere in this review. Because the many mech
anisms of suppressiveness remain obscure, it is difficult to classify them as
co-actions or substratum interactions. However, it must be emphasized that
the recognition and analyses of the mechanisms involved is an extremely
important aspect of the biology of soilborne plant pathologens. Soils histor
ically suppressive of F. oxysporum ( 1 , 1 60 ) , P . ultimum (72), Phytophthora
cinnamomi ( 1 22), and R . solani (86), among others, have been identified .
Analyses of suppressive soils indicate participation of biotic and abiotic
factors in their suppressive effects , including siderophore-producing bacteria
( 1 2, 9 1 ) , competition for energy sources, ( 1 , 1 1 2) , pH (98), or geologic
origin of a given soil ( 1 66) . Such analyses might suggest ways of making
disease-conducive soils suppressive.
In addition to pre-existing suppressiveness, soils also can become suppres
sive during monoculture of a crop , a phenomenon exemplified by the classic
take-all decline of take-all of wheat (3 1 ) . Declines in root rot of sugarbeet (84)
and common scab of potato ( 12 7) during monoculture of these crops are also
known.
A recent study indicates that the induction of suppressiveness can be
cultivar-specific (78) . In a monoculture of watermelons, most cultivars,
including some resistant ones, wilted severely after 4-5 years owing to F.
oxysporum f. sp. niveum, but the moderately resistant 'Crimson Sweet'
exhibited much less wilt than expected thoughout 7 years of monoculture.
Other cultivars grown in soil previously cropped to Crimson Sweet also had
less wilt than expected, given their known susceptibilities. The population of
the pathogen did not differ in soil cropped to the various cultivars. Why a
single variety only induced suppressiveness is not known.
EPILOGUE
Many topics meriting discussion have not been dealt with here, for example,
environmental effects on pathogens and disease in addition to predisposition
of plants ; the role played in disease by nematode-fungal interactions, mathe
matical modeling of inoculum density-disease relationships and of disease
1 14 LOCKWOOD
development over time, and disease resistance. These omissions are due to
limitations of time and space and the range of the author' s knowledge. I
especially regret not treating concepts having to do with the persistence, i. e .
survi val o f pathogens i n soil. Certain aspects of this subject have been
mentioned in other contexts in this review , but it merits inclusion as a separate
topic.
I hope that this review , even with its limitations, will provide a useful
perspective on the origin and current status of concepts pertaining to soilborne
pathogen s , and that it will serve as a guide to future research and thinking in
this area.
ACKNOWLEDGMENT
I would like to thank Ralph B aker, Christian Winner, Yaacov Katan, and
Wen-hsiung Ko for critical comments on a previous article ( 1 13 ) that helped
greatly in the preparation of this one.
Literature Cited
1 . Alabouvette, C. 1986. Fusarium-wilt logical Control ofPlant Pathogens. San
suppressive soils from the Chiiteaure Francisco: Freeman
nard region: review of a 10-year study. 9. Baker, R . 1 965. The dynamics of in
Agronomie 6:273-84 oculum. In Ecology of Soil-Borne Plant
2. Andrews, J. H . , Rouse, D. I. 1 982. Pathogens, cd. K. F. Baker, W. C.
Plant pathogens and the theory of r- and Snyder, pp. 395-403. Berkeley: Univ.
K-selection. Am. Naturalist 1 20:283-96 Calif. Press
3 . Arora, D. K. 1988. Effect of microor 10. Baker, R. 1 97 1 . Analyses involving in
ganisms on aggressiveness of Bipolaris oculum density of soil-borne plant
sorokiniana. Can. 1. Bot. In press pathogens in epidemiology. Phytopa
4. Arora, D. K . , Filonow, A. B . , Lock thology 6 1 : 1 280-92
wood, 1. L. 1983. Bacterial chemotaxis 1 1 . Baker, R. 1978. Inoculum potential. In
to fungal propagules in vitro and in soil. Plant Disease: An Advanced Treatise,
Can. 1. Microbiol. 29: 1 1 04-1 1 09 ed. J. O. Horsfall, E. C. Cowling,
5 . Arora, D. K . , Filonow, A. B . , Lock 2 : 1 37-57. New York: Academic
wood, 1. L. 1983 . Exudation from 14C_ 1 2 . Baker, R . , Elad, Y . , Sneh, B. 1986.
labeled fungal propagules in the pres Physical, biological and host factors in
ence of specific microorganisms. Can. iron competition in soils. In Iron, Sider
1. Microbiol. 29: 1 487-92 ophores, and Plant Diseases, ed. T. R.
6. Arora, D. K . , Filonow, A. B . , Lock Swinburne, pp. 77-84. New York:
wood, J. L. 1 985. Decreased Plenum
aggressiveness of Bipolaris sorokiniana 1 3 . Baker, R . , McClintock, D . L. 1965.
conidia in response to nutrient stress. Populations of pathogens in soil.
Physiol. Plant Pathol. 26:1 35-42 Phytopathology 55 :495
7. Atkinson, T. G . , Neal, J. L. Jr. , Larson, 14. Baker, R . , Maurer, C. L . , Maurer, R .
R. I . 1 974. Root rot reaction in wheat: A . 1967. Ecology o f plant pathogens i n
resistance not mediated by rhizosphere soil. VII. Mathematical models and in
or laimosphere antagonists. Phytopa oculum density . Phytopathology 57:
thology 64:97- 1 0 1 662-66
8 . Azad, H. R . , Davis, J. R . , Schnathorst, 1 5 . Bakker, A. W . , Schippers , B . 1 987.
W. C . , Kado, C. I. 1987. Influence of Microbial cyanide production in the rhi
verticillium wilt resistant and susceptible zosphere in relation to potato yield
potato genotypes in populations of an reduction and Pseudomonas spp - medi
tagonistic rhizosphere and rhizoplane ated plant growth-stimulation. Soil Bioi.
bacteria and free nitrogen fixers. Appl. Biochem. 19:451-57
Microbiol. Biotechnol. 26:99-104 16. Barta, A. L . , Schmitthenner, A. F.
8a. Baker, K. F. , Cook, R. J. 1 974. 8io- 1986. Interaction between flooding
stress and Phytophthora root rot among 30. Colhoun, J. 1 979. Predisposition by the
alfalfa cultivars. Plant Dis. 70: 3 1 0-- 1 3 environment. In Plant Pathology - A n
1 7 . Barnett, H . L . , B inder, F. L . 1983. the Advanced Treatise, ed . J. G . Horsfall ,
fungal host-parasite relationship. Ann. E . B . Cowling. 4:75-96. New York:
Rev. Phytopathol. 1 1 : 273-92 Academic
1 8 . Benson, D. M . , Baker, R. 1 974. 3 1 . Cook, R. J . , Baker, K. F. 1 98 3 . The
Epidemiology of Rhizoctonia solani pre Nature and Practice of Biological Con
emergence damping-off of radish: in trol of Plant Pathogens. SI. Paul, Minn:
oculum potential and disease potential Am. Phytopathol. Soc.
interaction. Phytopathology 64:957-62 32. Cook, R. J . , Snyder, W. C . 1 965. Car
1 9 . Beute, M. K . , Lockwood, J. L. 1 968. bon and nitrogen compounds and the
Mechanism of increased root-rot in germination of chlamydospores of
virus-infected peas. Phytopathology 58: Fusarium solani f. sp. phaseoli.
1 643-5 1 Phytopathology 55:254-56

20. Black, M. c . , Beute, M. K. 1 984. Rela 3 3 . Cooke, R. c. , Rayner, A. D. M. 1984.
tionships of inoculum density, micro Ecology of Saprotrophic Fungi. London:
sclerotium size, and inoculum efficiency Longman
of Cylindrocladium crotalariae causing 34. Cooke, R. c . , Whipps, J. M. 1 980. The
root rot of peanuts. Phytopathology evolution of modes of nutrition in fungi
74: 1 1 28-32 parasitic on terrestrial plants. Bioi. Rev.
2 1 . Blaker. N. S . , MacDonald, J. D. 1 98 1 . 5 5 : 34 1 -62
Predisposing effects of soil moisture ex 3 5 . Curl, E. A. 1 979. Effects of
tremes on the susceptibility of rho mycophagous Collembola on Rhizocto
dodendron to Phytophthora root and nia solani and cotton seedling disease.
crown rot. Phytopathology 7 1 :83 1-34 See Ref. 22, pp. 253-69
22 . Bowen, G. D. 1 979 . Integrated and ex 36. Dimond, A. E . , Horsfall, 1 . G . 1 960.
perimental approaches to the study of Prologue-Inoculum and the diseased
growth of organisms around roots. In population. In Plant Pathology: An Ad
Soil-Borne Plant Pathogens. ed. B . vanced Treatise, ed. J. G. Horsfall , A .
Schippers, W . Gams. London: Academ E. Dimond, 3 : 1-22. New York: Aca
ic demic
23. Bristow, P. R . , Lockwood, J . L . 1 97 5 . 3 7 . Dobbs, C. G . , Hinson, W. H . 1 95 3 . A
So i l fungistasis: role of spore exudates in widespread fungi stasis in soils . Nature
the inhibition of nutrient-independent 1 72: 1 97-99
propagules. J. Gen. Microbiol. 90: 1 47- 3 8 . Dodd, 1. L. 1 980. The role of plant
56 stresses in development of com stalk rot.
24. Bruehl, G . W . , Millar, R . L . , Cunfer, Plant Dis. 64:533-37
B. 1 969. Significance of antibiotic pro 39 . Duniway, 1. M. 1 977. Predisposing
duction by Cephalosporium firamineum effect of water stress on the severity of
to its saprophytic survival. Can. J. Plant Phytophthora root rot of safflower.
Sci. 49:235-46 Phytopathology 67: 884-89
2 5 . Chen, W . , Hoitink, H . A. J . , Schmitten 40. Edmunds, L. K. 1 964. Combined rela
ner, A. F. 1 98 7 . Factors affecting tion of plant maturity , temperature and
suppression of Pythium damping-off in soil moisture to charcoal rot develop
container media amended with com ment in grain sorghum. Phytopathology
posts. Phytopathology 77:755-60 54:5 1 4- 1 7
26. Chen, W . , Hoitink, H. A. J . , Tuovinen, 4 1 . Edwards, M . c . , Blakeman, J . P. 1 986.
O. H. 1 987. Thc role of microbial activ Thc use of autoradiography and other
ity in suppression of damping-off caused isotope techniques in phyllosphere stud
by Pythium ultimum. Phytopathology ies. In Microbiology of the Phyllos
78:3 1 4-22 phere. ed. N. J. Fokkema, J. Van den
27 . Christias, c . , Lockwood, J. L. 1 973. Heuvel, pp. 35-49. Cambridge: Cam
Conservation of mycelial constituents in bridge Univ. Press
four sclerotium-forming fungi in nutri 42. Elad, Y . , B arak, R . , Chet, I . , Henis, Y .
ent-deprived conditions. Phytopathology 1 98 3 . U ltrastructural studies o f the in
63 :602-5 teraction between Trichoderma spp . and
2 8 . Chuang, T. Y . , Ko, W. H. 1 98 1 . Propa plant pathogenic fungi. Phytopathol. Z.
gule size: its relation to population den 1 07 : 1 6�-75
sity of microorganisms in soil. Soil Biol. 43 . Elad, Y . , Baker, R. 1 985 . The role of
Biochem. 1 3 : 1 85-90 competition for iron and carbon in sup
29. Clark, F. E. 1 965. The concept of com pression of chlamydospore germination
petition in microbiology. See Ref. 9, pp. of Fusarium spp. by Pseudomonas
339-45 spp. Phytopathology 75 : 1 053-1 059
116 LOCKWOOD
44. Elad, Y . , Chet, I. 1987. Possible role of survival in soil. Can. J. Plant Pathol.
competition for nutrients in biocontrol of 7 : 1 9-27
Pythium damping-off by bacteria. 58. Fiirsch, H . , Winner, C. 1987. Un
Phytopathology 77: 1 90-95 tersuchung von Ackerboden auf das In
45. Elliott, L. F . , Lynch, 1. M . 1984. okulumpotential von pilzlichen Wurzel
Pseudomonads as a factor in the growth parasiten der Zuckerriibe. Zuckerindus
of winter wheat (Triticum aesrivum L.). trie 1 1 2:2 1 7-22, 292-97
Soil Bioi. Biochem . 1 6:69-71 59. Garrett, S. D. 1956. Biology of Root
46. Epstein, L . , Lockwood, 1. L. 1 983. The Infecting Fungi. Cambridge: Cambridge
role of exudation in the germination of Univ. Press
Cochliobolus victoriae conidia. J. Gen. 60. Garrett, S. D. 1959. Biology and ecolo
Microbiol. 1 29:3629-35 gy of root-disease fungi. In Plant Pa
47 . Epstein, L . , Lockwood, J. L. 1984. thology: Problems and Progress. 1 908-
Effect of soil microbiota on germination 1958, ed. C. S . Holton, G . W. Fischer,

of Bipolaris victoriae conidia. Trans. R. W. Fulton, H. Hart, S. E. A. McCal
Br. Mycol. Soc. 82:63-69 lan, pp. 309- 1 6 . Madison: The Univ.
48. Farley, 1. D . , Wilhelm, S . , Snyder, Wis. Press
W. C. 197 1 . Repeated germination 6 1 . Garrett, S . D. 1 963. Soil Fungi and Soil
and sporulation of Verticillium albo Fertility. Oxford: Pergamon
atrum in soil. Phytopathology 61 :260- 62. Garrett, S . D. 1965. Toward biological
64 control of soil-borne plant pathogens.
49. Filonow, A. B . , Akueshi, C. 0 . , Lock See Ref. 9, pp. 4-16
wood, J. L. 1983. Decreased virulence 63. Garrett, S . D . 1970. Pathogenic Root
of Cochliobolus victoriae conidia after Infecting Fungi. Cambridge: Cambridge
incubation on soils or on leached sand. Univ . Press
Phytopathology 73: 1 632-36 64. Garrett, S. D. 1976. Influence of nitro
50. Filonow, A. B . , Arora, D. K. 1987. gen on cellulolysis rate and saprophytic
Influence of soil matric potential on 14C_ survival in soil of some cereal foot-rot
exudation from fungal propagules. Can . fungi. Soil Bioi. Biochem. 8:229-34
J. Microbiol. 66:2084-2087 65. Garrett, S. D. 1979. The soil-root in
5 1 . Filonow, A. B . , Lockwood, 1. L. 1983. terface in relation to disease. In The Soi/
Mycostasis in relation to the microbial Root Interface, ed. 1. L. Harley, R. S .
nutrient sinks of five soils. Soil Bioi. Russell, London: Academic
Biochem . 15:557-65 66. Gaumann, E. 1950. Principles of Plant
5 2. Filonow, A. B . , Lockwood, 1. L. 1983. Infection . New York: Hafner
Loss of nutrient-independence for 67. Geels, F. P . , Schippers, B . 1 983.
germination by fungal propagules in Reduction of yield depressions in high
cubated on soils or on a model system frequency potato cropping soil after seed
imposing diffusive stress. Soil Bioi. tuber treatments with antagonistic
Biochem. 1 5 :567-73 fluorescent Pseudomonas spp. Phyto
5 3. Finstein, M. S . , Alexander, M . 1962. pathol. Z. 1 0 8:207-1 4
Competition for carbon and nitrogen be 68. Gilligan, C . A . 1 983. Modeling of soil
tween Fusarium and bacteria. Soil Sci. borne pathogens. Ann. Rev. Phyto
94:334-39 patho!. 2 1 :45-64
54. Foster, R. E . , Walker, 1. C. 1 947. Pre 69. Gilligan, C . A . 1985. Probability mod
disposition of tomato to Fusarium wilt. els for host infection by soilborne fungi.
1. Agr. Res. 74: 1 65-85 Phytopathology 75:61-67
5 5. Fradkin, A . , Patrick, Z. A. 1982. 70. Gottlieb, D. 1976. The production and
Fluorescence microscopy to study col role of antibiotics in soil. J. Antibiot.
onization of conidia and hyphae of 29:987-1 000
Cochliobolus sativus by soil microor 7 1 . Grossbard, E. 1952. Antibiotic produc
gani sms. Soil BioI. Biochem. 1 4:543- tion by fungi on organic manures and in
48 soil. J. Gen. Microbiol. 6:295-3 1 0
56. Fradkin, A . , Patrick, Z. A . 1 985. In 7 2 . Hancock, 1. G . 1 979. Occurrence of
teractions between conidia of Coch soils suppressive to Pythium ultimum.
liobolus sativus and soil bacteria as See Ref. 22, pp. 183-89
affected by physical contact and ex- 7 3 . Hayman, D. S. 1969. The influence of
0genous nutrients. Can. J. Plant Pathol. temperature on the exudation of nutri
7:7- 1 8 ents from cotton seeds and on pre
5 7 . Fradkin, A . , Patrick, Z. A . 1985. Effect emergence damping-off by Rhizoctonia
of matrie potential, pH, temperature, solani. Can. J. Bot. 47: 1663-69
and clay minerals on bacterial coloniza; 74. Henis, Y . , Ben-Yephet, Y. 1970. Effect
tion of Cochliobolus sativus and on their of propagule size on saprophytic growth,
infectivity and virulence on bean seed cepivorum Berk. Ann. Appl. Bioi. 64:
lings. Phytopathology 60: 1 35 1-56 303- 1 4
75. Henry , A. W. 1 93 1 . The natural micro 90. Kirk, J . J . 1 984. Ability o f Gaeuman
flora of the soil in relation to the foot-rot nomyces graminis to benefit from
problem of wheat. Can. J. Res. 4:69-77 senescence of the cereal root cortex dur
76. Ho, W . C . , Ko, W . H. 1986. Micro ing infection. Trans. Br. Mycol. Soc.
biostasis by nutrient deficiency shown in 82: 107- 1 1
natural and synthetic soils. 1. Gen. Mi 91. Kloepper, J . W . , Leong, J . , Teintze,
crobiol. 1 32:2807- 1 5 M . , Schroth, M. N . 1 980. Pseudomonas
7 7 . Hoch, H . c . , Fuller, M . S . 1 977. siderophores: a mechanism explaining
Mycoparasitic relationships. I . Morpho disease-suppressive soils. Curro Micro
logical features of interactions between bioi. 4 : 3 1 7-20
Pythium acanthicum and several fungal 92. Kloepper, J. W . , Schroth, M. N. 1 98 1 .
hosts. Arch. Microbiol. 1 1 1 :207-24 Relationship of i n vitro antibiosis of

78. Hopkins, D. L . , Larkin, R. P . , Elm plant growth-promoting rhizobacteria to

strom, G. W. 1987. Cultivarspecific in plant growth and the displacement of
duction of soil suppressiveness to Fusar root microflora. Phytopathology
ium wilt of watermelun. Phytopathology 7 1 : 1 020-- 1 024
77:607- 1 1 93 . Ko, W. H . , Chan, M. J. 1974. Infection
79. Howell, C. R . , Stipanovic, R. D. 1 979. and colonization potential of sporangia,
Control of Rhizoctonia solani in cotton zoospores, and chlamydospores of Phy
seedlings with Pseudomonas fluorescens tophthora palmivora in soil.
and with an antibiotic produced by the Phytopathology 64:1 307-1 309
bacterium. Phytopathology 69:480--82 94. Ko, W. H . , Chow, F. K. 1 977. Charac
80. Howell, C. R . , Stipanovic , R. D. 1 980. teristics of bacteriostasis in natural soil.
Suppression of Pythium ultimum J . Gen. Microbial. 102:295-98
induced damping-off of cotton seedlings 95 . Ko, W. H . , Ho, W. C. 1 984. Soil mi
by Pseudomonas fluorescens and its crobiostasis. In Soilborne Crop Diseases
antibiotic, pyoluteori n. Phytopathology in Asia, ed. J. B ay-Petersen, pp. 175-
70:7 1 2- 1 5 84. Taipei: Food & Fert. Technol. Ctr.
8 1 . Hsu, S . C. , Lockwood, J . L. 1969. Asian & Pacific Reg.
Mechanisms of inhibition of fungi in 96. Ko, W . H . , Lockwood, J. L. 1 967. Soil
agar by streptomycetes. J. Gen. Micro fungistasis: relation to fungal spore
bioi. 57: 1 49-58 nutrition. Phytopathology 57:894-901
82. Hsu, S. c . , Lockwood, J. L. 1 97 1 . Re 97. Ko, W. H . , Lockwood, J. L. 1 970.
sponses of fungal hyphae to soil fungis Mechanism of lysis of fungal mycelia in
tasis. Phytopathology 6 1 : 1 355-62 soil. Phytopathology 60: 1 48-54
83. Hsu, S. c . , Lockwood, J. L. 1973 . Soil 98 . Kobayashi , N . , Ko, W. H. 1 985. Nature
fungistasis: hehavior of nutrient of suppression of Rhizoctonia solani in
independent spores and sclerotia in a Hawaiian soils. Trans. Br. Mycol. Soc.
model system. Phytopathology 63:334- 84:69 1-94
37 99. Kommedahl, T . , Windels, C. E . , Stuck
84. Hyakumachi, M. 1 983. Disease decline er, R. E . 1979. Occurrence of Fusarium
phenomenon of sugarbeet root rot. Sho species in roots and stalks of symptom
kubutso Boeki (Plant Prot.) 37:22-27 less com plants during the growing sea
8 5 . Ito, I. 1975. Ecology and control of son. Phytopathology 69:96 1 -66
Fusarium solani f. sp. phaseoli. Shoku 100. Kraft, J. M . , Endo, R. M . , Erwin, D. C.
butso Boeki (Plant Prot.) 29:366-70 1967. Infection of primary roots of bent
86. Jager, G . , Velvis, H . 1 983. Suppressiun grass by zoospores of Pythium apha
of Rhizoctonia solani in potato fields. I. nidermatum. Phytopathology 57: 86-90
Occurrence. Neth. J. Plant Pathol. 101 . Kritzman, F . , Zutra, E. 1 983. Survival
89: 2 1 -29 of Pseudomonas syringae pv. lachry
87 . Katan, J . 1 97 1 . Symptomless carriers of mans in soil, plant debris, and the rhi
the tomato Fusarium wilt pathogen. zospheres of nonhost plants. Phytopar
Phytopathology 6 1 : 1 2 1 3- 1 7 asirica 1 J :99- 1 08
8 8 . Kerr, A . 1 980. B iological control of 102. Kuan, T. L . , Erwin , D. C. 1 980. Pre
crown gall through production of agro disposition effect of water saturation of
cin 84. Plant Dis. 64:24-30 soil on Phytophthora root rot of alfalfa.
89. King, J. E. , Coley-Smith, J. R. 1969. Phytopathology 70:981-86
Production of volatile alkyl sulphides by 10 3. Last, F. T. 1 960. Longevity of conidia
microbial degradation uf synthetic alliin of Botryris Jabae Sardina. Trans. Br.
and alliin-like compounds, in relation to Mycol. Soc. 43:673-80
germination of sclerotia of Sclerotium 104. Lee, M . , Lockwood, J. L. 1977. En-
1 18 LOCKWOOD
hanced severity of Thielaviopsis basico sources in evaluating peas (Pisum sat

la root rot induced in soybean by the ivum) for resistance to stem rot caused
herbicide chloramben. Phytopathology by Rhizoctonia solani. Plant Dis. 68:53-
67: 1 360--67 55
1 05 . Lingappa, B . T . , Lockwood, J. L. 1964. 121. McNaughton, S. J . , Wolf, L . L. 1973.
Activation of soil microflora by fungus General Ecology. New York: Holt,
spores in relation to soil fungistasis. J. Reinhart & Winston
Gen. Microbiol. 35:21 5-27 122. Malajczuk, N. 1 97 9 . Biological
106. Lisker, N . , Katan, J . , Henis, Y. 1 974. suppression of Phytophthora cinnamomi
Effect of propagule size on the in vitro in eucalypts and avocadoes in Australia.
induction of polygalacturonase and cel See Ref. 22, pp. 635-52
lulase by Rhizoctonia solani. Can. J. 1 23 . Marshall, K. C . , Alexander, M. 1 960.
Microbiol. 20: 1 7 1 3-21 Competition between soil bacteria and
107. Lochhead, A . G . , Timonin, M. 1 . , Fusarium. Plant Soil 1 2 : 1 43-53

West, P . M . 1 940. The microflora of the 1 24. Mathre, D. E . , Johnston, R. H. 1 979.
rhizosphere in relation to resistance of Decomposition of wheat straw infested
plants to soil-borne pathogens. Sci. Agr. by Cephalosporium gramineum . Soil.
20:414-18 Bioi. Biochem. 1 1 : 577-80
108. Lockwood, J. L. 1964. Soil fungistasis. 125. Maurer, C. L . , Baker, R. 1965. Ecology
Ann. Rev. Phytopathol. 2:34 1-62 of plant pathogens in soil: II. Influence
1 09 . Lockwood, J. L. 1975 . Quantitative of glucose, cellulose, and organic nitro
evaluation of a leaching model system gen amendments on development of
for soil fungistasis. Phytopathology bean root rot. Phytopathology 55:69-72
65:460-64 1 26. Mendez, C . , Brana, A. F . , Manzanal,
1 1 0. Lockwood , J. L. 1 977 . Fungistasis in M. B . , Hardisson, C. 1 985 . Role of sub
soils. Bioi. Rev. 52: 1-43 strate mycelium in colony development
111. Lockwood, J. L. 1 98 1 . Exploitation in Streptomyces. Can. J. Microbial.
competition . In The Fungal Community: 3 1 :446-50
Its Organization and Role in the Ecosys 127. Menzies, J. D. 1959. Occurrence and
tem, ed. D . T . Wicklow , G . C . Carroll, transfer of a biological factor in soil that
pp. 3 19-49. New York: Dekker suppresses potato scab. Phytopathology
1 1 2. Lockwood, J. L. 1984. Soil fungistasis: 49:648-52
mechanisms and relation to biological 128. Millard, W. A. 1923. Common scab of
control of soilborne plant pathogens. See potatoes . Part II. Ann. Appl. Bioi.
Ref. 95, pp. 159-74 10:70-88
1 13. Lockwood, J. L. 1 986. Soilborne plant 1 29. Newman, E. 1. 1985 . The rhizosphere:
pathogens: concepts and connections. carbon sources and microbial pop
Phytopathology 76:20--27 ulations. In Ecological Interactions in
1 14. Lockwood, J. L . , Filonow, A. B. 1 98 1 . Soil: Plants, Microbes and Animals, ed.
Responses of fungi to nutrient-limiting A . H . Fitter, D . Atkinson, D . J. Read,
conditions and to inhibitory substances M. B . Usher. Oxford: Blackwell
in natural habitats. Adv. Microb. Ecol. 1 30. Niederpruem, D. J . , Wessels, J. O. H .
5 : 1-6 1 1 969. Cytodifferentiation and mor
1 15 . Lockwood, J. L . , Schippers, B . 1984. phogenesis in Schizophyllum commune.
Evaluation of siderophores as a factor in Bacteriol. Rev. 33:505-35
soil mycostasis. Trans. Br. Mycol. Soc. 1 3 1 . Odvody, G. N . , Dunkle, L. D. 1979.
82:589-94 Charcoal stalk rot of sorghum: effect of
1 16 . Lumsden, R. D . 1 98 1 . Ecology of environment on host-parasite relations.
mycoparasitism. See Ref. 1 1 1 , pp. 295- Phytopathology 69:250--54
318 1 32. Old, K. M . , Patrick, Z. A . 1979. Giant
1 17. MacArthur, R . H . , Wilson, E . 0 . 1967. soil amoebae: potential biocontrol
The Theory of Island Biogeography. NJ: agents. See Ref. 22, pp. 6 1 7-28
Princeton Univ. Press 1 33 . Papavizas, G. C . , Davey, C. B . 1 96 1 .
1 18 . MacDonald, J . D. 1982. Effect of salin Extent and nature of the rhizosphere in
ity stress on the development of Phy Lupinus. Plant Soil 1 4 : 2 1 5-36
tophthora root rot of chrysanthemum. 1 34 . Papavizas, G. C . , Kovacs, M. F. Jr.
Phytopathology 72:214-19 1972. Stimulation of spore germination
1 19 . McCoy, M . L., Powelson, R. L. 1974. of Thielaviopsis basicola by fatty acids
A model for determining spatial distribu from rhizosphere soil. Phytopathology
tion of soil-borne propagules. 62:688-94
Phytopathology 64: 1 45-47 1 34a. Papendick, R. 1 . , Cook, R. J. 1974.
1 20. McCoy, R. J . , Krafts , J. M. 1984. Com Plant water stress and development of
parison of techniques and inoculum Fusarium root rot in wheat subjected to
different cultural practices. Phytopathol eterious and beneficial rhizosphere mi

ogy 64:358-63 croorganisms and the effect of cropping
1 3 5 . Park, D. 1960. Antagonism - The back practices. Ann. Rev. Phytopathol.
ground to soil fungi. In The Ecology of 25:339-58
Soil Fungi, ed. D . Parkinson, J . S. 150. Schippers, B . , Geels, F. P. , Hoekstra,
Waid. Liverpool: Liverpool Univ. Press 0 . , Lamers , J. G . , Maenhout, C. A. A .
1 36. Parkinson, D. 1967. Soil microorgan A . , Scholte, K . 1985 . Yield depressions
isms and plant roots. In Soil Biology, ed. in narrow rotations caused by unknown
A. Burges , F. Raw, pp. 449-78. Lon microbial factors and their suppression
don: Academic by selected pseudomonads. In Ecology
1 37 . Paustian, K . , Schniirer, J. 1 987.. Fungal and Management of Soilborne Plant
growth response to carbon and nitrogen Pathogens. ed. C. A. Parker, A. D .
limitation: a theoretical model. Soil BioI. Rovira. K . J . Moore, P. T . W . Wong, J .
Biochem. 1 9: 6 1 3-20 K . Kollmorgen, p p . 1 27-130. S t . Paul,

1 3 8 . Paustian, K . , Schniirer, J. 1 987. Fungal Minn: Am. Phytopathol. Soc.

growth response to carbon and nitrogen l S I . Schippers, B . , Lugtenberg, B . , Weis
limitations: application of a model to beek, P. J. 1987. Plant growth control
laboratory and field data. Soil BioI. by fluorescent pseudomonads. In Inno
Biochem . 1 9:62 1 -29 vative Approaches to Plant Disease
1 39. Pavlica, D. A . , Hora, T. S . , Bradshaw, Control, ed. I. Chet, pp. 1 9-39. New
J . J . , Skogerboe , R. K . , Baker, R . York: Wiley
1 978. Volatiles from soil influencing ac 1 52. Schippers, B . , Meijer, J. W . , Liem, J. I .
tivities of soil fungi. Phytopathology 1982. Effect o f ammonia and other soil
68:758-65 volatiles on germination and growth of
1 40 . Phillips, D. J. 1965. Ecology of plant soil fungi. Trans. Br. Mycol. Soc. 79:
pathogens in soil. IV. Pathogenicity of 25 3-59
macroconidia of Fusarium roseum f. sp. 1 5 3 . Schippers, B . , Van Eck, W. H . 1 98 1 .
cereaUs produced on media of high or Formation and survival of chlamydo
low nutricnt content. Phytopathology spores in Fusarium. In Fusarium: Dis
5 5 :328-29 eases. Biology, and Taxonomy, ed. P.
1 4 1 . Punja, Z. K . , Gorgan, R. C. 1 98 1 . E. Nelson, T. A. Toussoun, R. J. Cook,
Mycelial growth and infection without a pp. 250-60. University Park: Penn.
food base by eruptively germinating State Univ. Press
sclerotia of Sclerotium rolfsii. Phytopa 1 54. Schneider, R. W. 1 982. Suppressive
thology 7 1 : 1 099-1 1 03 Soils and Plant Disease. St. Paul, Minn:
142. Raper, J. R. 1 968 . On the evolution of Am. Phytopathol. Soc.
fungi . In The Fungi - An A dvanced Trea 1 55 . Schneider, R. W. , Pendery, W. E.
tise, Vol. III, ed. G. C. Ainsworth, A . 1983. Stalk rot of corn: mechanism of
S . Sussman. London: Academic predisposition by an early season water
1 4 3 . Reinking, O. A . , Manns, M. M. 1933. stress. Phytopathology 73:863-7 1
Parasitic and other fusaria counted in 1 56 . Schroth, M. N . , Hendrix, F. F. Jr.
tropical soils. Z. Parasitenkd. 6:23-75 1 962. Influence of non susceptible plants
1 44 . Salt, G. A. 1 979. The increasing interest on the survival of Fusarium solani f.
in 'minor' pathogens. See Ref. 22, pp. phaseoli in soil. Phytopathology 52:
289-3 1 2 906-9
1 45 . Sanford, G . B . 1939. Research o n cer 1 57 . Schroth, M. N . , Hildebrand, D. C .
tain soil-borne diseases as affected by 1 964. Influence o f plant exudates o n
other micro-organisms. Sci. Agr. 19: root-infecting fungi. Ann. Rev. Phyto
609- 1 5 pathol. 2 : 1 0 1-32
146. Saville, D . B . O . 1 968. Possible in 1 5 8 . Schulz, F. A . , Bateman, D. F. 1 969.
terrelationships between fungal groups. Temperature response of seeds during
See Ref. 142, pp. 649-75 the early stages of germination and its
147. Scher, F. M . , Baker, R. 1980. Mech relation to injury by Rhizoctonia solani.
anism of biological control in a Fusar Phytopathology 59:352-55
ium -suppressive soil. Phytopathology 1 59. Shields, J. A . , Paul, E. A . , Lowe, W.
70: 4 1 2- 1 7 E. 1 974. Factors influencing the stability
14 8. Scher, F. M . , Baker, R . 1 982. Effect of of labeled microbial materials in soils.
Pseudomonas putida and a synthetic iron Soil BioI. Biochem. 6:3 1-37
chelator on induction of soil suppres 160. Smith, S. N . , Snyder, W. C. 1972.
siveness to Fusarium wilt pathogens. Germination of Fusarium oxysporum
Phytopathology 72: 1 567-1 573 chlamydospores in soils favorable and
149. Schippers, B . , Bakker, A. W . , Bakker, unfavorable to wilt establishment.
P. A. H. M. 1 987. Interactions of del- Phytopathology 62:273-77
1 20 LOCKWOOD
1 6 1 . Sneh, B . , Dupler, M . , Elad, Y . , B aker, 4 1-52. Taipei: Taiwan Agr. Res. Inst.!
R . 1984. Chlamydospore germination of Plant Prot. Soc . , Republic of China
Fusarium oxysporum f. sp. cucumeri 1 74 . Van der Plank, J. E. 1975. Principles oj
num as affected by fluorescent and lytic Plant Injection . New York: Academic
bacteria from Fusarium-s uppressive 1 75 . Waksman , S. A. 1944. Three decades
soil. Phytopathology 74: 1 1 1 5- 1 1 24 with soil fungi. Soil Sci. 58:89-1 1 5
1 62 . Sneh, B . , Lockwood, J. L. 1 975. Quan 1 76. Waksman, S . A . 1 952. Soil Microbiolo
titative evaluation of the microbial nutri gy. New York: Wiley
ent sink in soil in relation to a model 1 77 . Weinhold, A. R . , Bowman, T . , Dod
system for soil fungistasis. Soil BioI. man, R. L. 1 969 . Virulence of Rhizocto
Biochem. 8:65-69 nia solani as affected by nutrition of the
163. S nyder, W. c . , Schroth, M . N . , Christ pathogen. Phytopathology 59: 1601-
ou, T. 1 959. Effect of plant residues on 1 605
1 7 8 . Weller , D. M . , Cook, R. J. 1 9 83.

root rot of bean. Phytopathology

49:755-56 Suppression of take-all o f wheat by seed
164. Stanghellini, M. E . , Hancock, 1. G . treatments with fluorescent pseudomo
1 97 1 . The sporangium o f Pythium ul nads. Phytopathology 73:463-69
timum as a survival structure in soil. 1 79. Whipps, J. M . , Lynch, J. M. 1 985. En
Phytopathology 6 1 : 1 57-64 ergy losses by the plant in rhisodeposi
1 65 . Steiner, G. W . , Lockwood, J. L. 1 969. tion. Ann. Proc. Phytochem . Soc. Eur.
Soil fungistasis: sensitivity of spores in 26:59-7 1
relation to germination time and size. 1 80. Wicklow, D. T. 1 98 1 . Interference com
Phytopathology 59: 1 084-1 092 petition and the organization of fungal
1 66. Stotzky, G . , Martin, R. T. 1963. Soil communities. See Ref. 1 1 1 , pp. 35 1 -
mineralogy in relation to the spread of 75
Fusarium wilt of bananas in Central 1 8 1 . Wicklow, D. T. The role of competition
America. Plant Soil 1 8 : 3 1 7-37 in the structuring of fungal communities.
1 67 . Stotzky, G . , Norman, A. G. 1 96 1 . Fac In Proc. 4th Intern . Symp . Microbial
tors limiting microbial activities in soil . Eco/. , Ljubljana, Yugoslavia. 1986. In
I . The level o f substrate, nitrogen and press
phosphorus . Arch. Mikrohiol. 40:341- 1 82. Wicklow, D. T . , Zak, J. C. 1 979.
69 Ascospore germination of carbonicolous
1 68 . S uslow , T . V . 1982. Role of root ascomycetes in fungistatic soils: an eco
colonizing bacteria in plant growth. In logical interpretation. Mycologia 7 1 :
Phytopathogenic Prokaryotes, ed. M. S . 238-42
Mount, G. H. Lacy, 1 : 1 87-223. New 1 83 . Wilcox, W. , Mircetich, S. M. 1985.
York: Academic Effecb of flooding duration on the de
1 69 . Suslow, T. V . , Schroth, M. N. 1 982. velopment of Phytophthora root and
Role of deleterious rhizobacteria as crown rots of cherry . Phytopathology
minor pathogens in reducing crop 7 5 : 1 4 5 1 -55
growth. Phytopathology 72: 1 1 1- 1 5 1 83a. Wilkinson , H . T., Alldredge , J . R . ,
1 70. Thomashow, L . S . , Weller, D. M . Cook, R . J . 1985. Estimated distances
1987 . Role of a phenazine antibiotic in for infection of wheat roots by
disease suppression by Pseudomonas Gaeumannomyces graminis var. tritici
fluorescens 2-79. Phytopathology 77: in soils suppressive and conducive to
1 724 (Abstr.) take-all . Phytopathology 75:557-9
1 7 1 . Timonin, M. I. 1 940 . The interactions 1 84 . Wilkinson, H . T . , Cook, R. J . ,
of higher plants and soil Alldredge, J. R . 1 985. Relation o f in
microorganisms. II. Study of the micro oculum size and concentration to infec
bial population of the rhizosphere in tion of wheat roots by Gaeumannomyces
relation to resistance of plants to soil graminis var. tritici. Phytopathology
borne diseases. Can. 1. Res. C 1 8:394- 75:98-103
413 1 8 5 . Williams, S . T. 1 985. OIigotrophy in
1 72 . Toussoun, T . A . , Nash, S . M . , Snyder, soil: fact or fiction. In Bacteria in Their
W. C. 1960. The effect of nitrogen Natural Environments. ed. M . Fletcher,
sources and glucose on the pathogenesis G. D. Floodgate, pp. 8 1 - 1 1 0 . London:
of Fusarium solani f. sp. phaseoli. Academic
Phytopathology 50: 1 37-40 1 86. Williams, S. T . , Vickers, J. C. 1986.
1 73 . Vi, T. 1985 . Problems and prospects of The ecology of antibiotic production.
Rhizoctonia diseases and their control in Microb. Ecol. 1 2:43-52
Japan . In Soilborne Plant Diseases, ed. 1 87 . Winner, C. 1 984. Virose Wiirzelbartig
R. J . Chiu, S. K. Sun, Y. S. Lin, pp. keit (Rizomania) der Beta-Rube a1s
Herausforderung flir Forschung and Re 1 9 1 . Wyllie, T. D . , Calvert, O. H. 1969.

sistenzziichtung. Zuckerindustrie 109: Effects of flower removal and pod set on
1 1 3-20 formation of sclerotia and infection
1 88. Woltz, S. S. 1978. Nonparasitic plant of Glycine max by Macrophomina
pathogens. Ann. Rev. Phytopathol. 16: phaseolina . Phytopathology 59: 1 243-
403-30 45
1 89. Wright, J. 1956. The production of anti 1 92 . Yarwood, C. E. 1959. Predisposition. In
biotics in soil. III. Production of gliotox Plant Pathology: An Advanced Treatise,
in in wheat straw buried in soil. Ann. ed. J. G. Horsfall , A. E. Dimond,
Appl. BioI. 44:461-66 1 :521-62. New York: Academic
1 90. Wright, J. 1 956. The production of anti 1 9 3 . Yoder, D. L . , Lockwood, J. L. 1973.
biotics in soil. IV. Production of antibi Fungal spore germination on natural and
otics in coats of seeds sown in soil. Ann. sterile soil. J. Gen. Microbiol. 74: 1 07-
Appl. BioI. 44:56 1-66 17

Soil Born Plant Pathogens

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Soil Born Plant Pathogens

Uploaded by

Copyright:

Available Formats

ANNUAL

This article reviews the development of major concepts in the field of

SOIL INVADERS AND SOIL INHABITANTS

This concept is important historically because it provided the initial impetus

groups of fungi in soil (175); those characteristically occurring in soil were

themselves in an active condition (33). The soil-inhabiting fungi would

Life History Strategies

Major and Minor Parasitizing Pathogens and Nonparasitizing

occurring in potatoes grown with short rotations, in The Netherlands (149,

growth of a fungal parasite available for infection of a host at the surface of

The biomass of different pathogens in soil appears to be rather consistent

Inoculum density is not always related to the incidence or severity of

present in the rhizosphere, the term "rhizodeposition" has been proposed as

resistant soybeans to be smaller than those from plots cropped to susceptible

While measurements of the energy contents of inoculum could place the

The concept of predisposition is part of a vast area of knowledge concerning

includes: decreased photosynthesis (leaf diseases, shading, defoliation); salin­

predisposing conditions and using this information to so manage the crop as to

MICROBIAL INTERACTIONS WITH PATHOGENS

According to its generally accepted definition, microbial antagonism in­

sativus, G. graminis var. tritici or F. culmorum, as compared with sterilized

Coactions between different microorganisms in culture media have been

substantial protection against its corresponding disease. However, genetic

by results showing that antibiotic and nonantibiotic strains of C. gramineum

COMPETITION Competition, as a coaction, has been studied relatively little,

chlamydospores of F. oxysporum f. sp. cucumerinum was stimulated by

Fungistasis The concept of a generalized restriction on fungal germination

Propagule debilitation The fungistatic mechanism protects the propagules

depending on the extent of energy stress and the availability of energy

Persistent structure formation Autolysis is linked with the formation of at

Hyphal growth The hyphae of saprophytic fungi appear to be adapted for

parasitic or saprophytic existence in soil is not known: but A. B. Lloyd and I

NITROGEN COMPETITION The supply of nitrogen does not appear to limit

cellulose. G. graminis var. tritici and F. culmorum had relatively inefficient

1 643-5 1 Phytopathology 55:254-56

Effect of soil microbiota on germination 1958, ed. C. S . Holton, G . W. Fischer,

hosts. Arch. Microbiol. 1 1 1 :207-24 Relationship of i n vitro antibiosis of

78. Hopkins, D. L . , Larkin, R. P . , Elm­ plant growth-promoting rhizobacteria to

hanced severity of Thielaviopsis basico­ sources in evaluating peas (Pisum sat­

107. Lochhead, A . G . , Timonin, M. 1 . , Fusarium. Plant Soil 1 2 : 1 43-53

different cultural practices. Phytopathol­ eterious and beneficial rhizosphere mi­

Biochem. 1 9: 6 1 3-20 K . Kollmorgen, p p . 1 27-130. S t . Paul,

1 3 8 . Paustian, K . , Schniirer, J. 1 987. Fungal Minn: Am. Phytopathol. Soc.

1 7 8 . Weller , D. M . , Cook, R. J. 1 9 83.

root rot of bean. Phytopathology

Herausforderung flir Forschung and Re­ 1 9 1 . Wyllie, T. D . , Calvert, O. H. 1969.

Appl. BioI. 44:56 1-66 17

You might also like

includes: decreased photosynthesis (leaf diseases, shading, defoliation); salin

According to its generally accepted definition, microbial antagonism in

78. Hopkins, D. L . , Larkin, R. P . , Elm plant growth-promoting rhizobacteria to

hanced severity of Thielaviopsis basico sources in evaluating peas (Pisum sat

different cultural practices. Phytopathol eterious and beneficial rhizosphere mi

Herausforderung flir Forschung and Re 1 9 1 . Wyllie, T. D . , Calvert, O. H. 1969.