Table Of ContentOTHER TITLES IN THIS SERIES
1. Plant Modification for More Efficient Water Use
by J.F. Stone (Editor)
1975 xii + 320 pp.
2. Tree Ecology and Preservation
by A. Bernatzky
1978 viii + 358 pp.
3. Cycling of Mineral Nutrients in Agricultural Ecosystems
by M.J. Frissel (Editor)
1978 viii + 356 pp.
4. Interactions between Non-Pathogenic
Soil Microorganisms and Plants
by Y.R. Dommergues and S.V. Krupa (Editors)
1978 xii + 476 pp.
6. Soil Disinfestation
by D. Mulder (Editor)
1979 xiv + 368 pp.
7. Management of Semi-Arid Ecosystems
by B.H. Walker (Editor)
1979 (in preparation)
Developments in Agricultural and Managed-Forest Ecology, 5
ECOLOGY OF ROOT PATHOGENS
edited by
S.V. KRUPA
Department of Plant Pathology, University of Minnesota, St. Paul, U.S.A.
and
Y.R. DOMMERGUES
CNRS and ORSTOM, Dakar, Senegal
ELSEVIER SCIENTIFIC PUBLISHING COMPANY
Amsterdam — Oxford — New York 1979
ELSEVIER SCIENTIFIC PUBLISHING COMPANY
335 Jan van Galenstraat
P.O. Box 211, 1000 AE Amsterdam, The Netherlands
Distributors for the United States and Canada:
ELSEVIER NORTH-HOLLAND INC.
52, Vanderbilt Avenue
New York, N.Y. 10017
Library of Congress Cataloging in Publication Data
Main entry under title:
Ecology of root pathogens.
(Developments in agricultural and managed-forest
ecology ; 5)
Includes bibliographies and index.
1. Soil micro-organisms—Ecology. 2. Soil
nematodes—Ecology. 3. Roots (Botany)—Diseases and
pests. I. [Krupa, Sagar V.| II. Dommergues, Yvon.
III. Series.
QR111.E2U 582f.02f 3 79-208
ISBN 0-^-1+1639-0
ISBN 0-444-41639-0 (Vol. 5)
ISBN 0-444-41637-4 (Set)
ISBN 0-444-41515-7 (Series)
© Elsevier Scientific Publishing Company, 1979
All rights reserved. No part of this publication may be reproduced, stored in a re
trieval system or transmitted in any form or by any means, electronic, mechanical,
photocopying, recording or otherwise, without the prior written permission of the
publisher, Elsevier Scientific Publishing Company, P.O. Box 330, 1000 AH Amster
dam, The Netherlands
Printed in The Netherlands
IX
LIST OF CONTRIBUTORS
H. G. Diem ORSTOM, B.P. 1386, Dakar, Senegal.
T. Kommedahl Department of Plant Pathology, University of Minnesota, St. Paul,
Minn. 55108, U.S.A.
D. MacDonald Department of Plant Pathology, University of Minnesota, St. Paul,
Minn. 55108, U.S.A.
F. Mangenot Laboratoire de Botanique et de Microbiologie , Case Officielle no. 140,
54037 Nancy Cedex, France.
M. N. Schroth Department of Plant Pathology, University of California, Berkeley,
Calif. 94720, U.S.A.
S. V. Thomson Department of Plant Pathology, University of California, Berkeley,
Calif. 94720, U.S.A.
A. R. Weinhold Department of Plant Pathology, University of California, Berkeley,
Calif. 94720, U.S.A.
C. E. Windeis Department of Plant Pathology, University of Minnesota, St. Paul,
Minn. 55108, U.S.A.
R. J. Zeyen Department of Plant Pathology, University of Minnesota, St. Paul,
Minn. 55108, U.S.A.
X
FOREWORD
"For six years you shall sow your land and gather in its yield; but the seventh year
you shall let it rest and lie in fallow, that the poor of your people may eat."
Exodus 23:10—11.
Soil is a reservoir for innumerable plant pathogens. Roots interact with
soil-borne plant pathogens exhibiting temporal and spatial variations. If
the pathogen becomes dominant, disease is the result. While fungi con
stitute the largest number of plant pathogens, soil-borne bacteria, nematodes
and viruses are also important in relation to plant health and productivity.
The authors contributing to this book have summarized the state of our
knowledge regarding the major categories of soil-borne plant pathogens. They
have also attempted to discuss concepts relevant to root disease as well as
their own ideas.
Kommedahl and Windeis have described a new approach to the ecology
of soil-borne fungal pathogens. Schroth, Weinhold and Thompson have
approached the bacterial plant pathogens via a classification of bacterial
genera. MacDonald has synthesized our knowledge on nematode pathogens
through their ecology and their interactions with the host root. The new
and interesting subject of soil-borne plant viruses is discussed by Zeyen with
a fundamental approach of transmission, infection and interaction of the
infected roots with other microorganisms in its microclimate.
Health is a rule and disease is an exception. In spite of this generality,
plants suffer from numerous root diseases. Man has attempted to control
plant disease since 1000 B.C. As demands are imposed on energy conserva
tion and increased food production scientists have made intensive efforts
to manipulate crop production through biological management. To both of
us (SVK and YRD) biological control of plant disease offers an exciting ap
proach to increased crop productivity. It may become an important aspect
in integrated pest management. Hence, Mangenot and Diem have provided
their views on biological control of root disease.
After reviewing all the manuscripts, it became apparent to us that this
book will stimulate other soil microbiologists and plant pathologists and
attract their increased attention to soil-borne plant pathogens. It is our
sincere hope that it will serve that purpose.
Department of Plant Pathology, S. V. KRUPA
University of Minnesota, U.S.A.
and
Centre OSTROM de Dakar, Y. R. DOMMERGUES
Senegal
October, 1977
1
Chapter 1
FUNGI: PATHOGEN OR HOST DOMINANCE IN DISEASE*
THOR KOMMEDAHL AND CAROL E. WINDELS
1. INTRODUCTION
Of the maladies that affect roots there is seemingly no end. Plant roots are
beset with problems described as damping-off, seedling blight, root rots,
crown rots, foot rots, club roots, root browning, pink roots, root parasites
and wilts. Sometimes roots are killed before plants emerge from the soil;
sometimes the plants emerge, only to succumb as seedlings. Sometimes the
struggle continues until plants either grow to be reasonably healthy or they
grow but lead unthrifty or aborted lives. Sometimes plants succumb to
disease as they become weakened or reach maturity. Root-infecting fungi are
found the world over, but perhaps do more damage in hot, dry regions. Most
root diseases are caused by fungi; their greatest enemies in soil are bacteria
which flourish less in dry than moist earth, but many other factors may also
affect the occurrence and development of root-infecting fungi.
It is our purpose to indicate the importance of root-infecting fungi,
emphasize the important root diseases and their symptoms, name the
important genera and species of fungi that cause root disease, and classify
and characterize the interaction between root and pathogen in soil.
Root disease fungi have been classified in various ways according to
disease symptoms, taxonomic groups, hosts, nutrition and mode of life, and
ecological relations.
1.1. Root disease symptoms
Root-infecting fungi can effect a diverse array of symptoms that are
described as necrosis, discoloration (pink, red, yellow, brown and black),
tissue destruction, gum formation, root distortion or malformation, wilting,
and sloughed cortical cells. Symptoms may be induced by production of
either toxins or enzymes that predispose or kill cells in advance of
penetration. Tissues invaded include epidermis, periderm, cortex, cambium,
♦Paper No. 1622, Miscellaneous Journal Series, Minnesota Agricultural Experiment
Station, St. Paul.
2
xylem and phloem. Fungi invade root tips; root hairs; primary, secondary
and adventitious roots; and young actively growing to senescent roots. Some
root-infecting fungi are primary, and some are secondary, or wound
parasites, and some act as part of a root-disease complex. Root-infecting
fungi may be parasites without being pathogens.
Plant pathologists in the United States Department of Agriculture (1960)
have compiled in the Agricultural Handbook No. 165, a list of more than
50,000 diseases of parasitic and nonparasitic origin. Of the more than 1,200
genera of plants listed, 655 are host to 3,330 root diseases. Of this number,
64% are root rots, 9% damping-off diseases, 7% wilts, 6% seedling blight, 6%
crown and foot rots, 3% root-browning diseases, 3% root-infecting fungi, and
1% club roots. In our summary, root rots include dry rots, rootlet rot, pink
rot, black leg, black root, charcoal rot and secondary root rot. Not included
are rots of storage organs of stem or leaf origin, or butt rot, collar rot, fairy
rings and slime molds.
1.2. Taxonomic groups
Of the 3,330 root diseases listed in the U.S. Department of Agriculture
Handbook No. 165 (1960), 60% of the causal fungi are in the Class Fungi
Imperfecti, 23% are in the Phycomycetes, 12% in the Basidiomycetes, and
6% in the Ascomycetes. Of the 81 genera of fungi that cause root disease, 38
are in the Fungi Imperfecti, 18 in the Ascomycetes, 14 in the Basidio
mycetes and 11 in the Phycomycetes. The 10 genera of root-infecting fungi
in order of incidence on host species are as follows: Phymatotrichum,
Pythium, Rhizoctonia, Fusarium, Armillaria, Verticillium, Phytophthora,
Helminthosporium, Clitocybe, and Polyporus. The 10 most frequently
reported species are: Phymatotrichum omnivorum (20%), Rhizoctonia solani
(12%), Armillaria mellea (5%), Fusarium oxysporum (4%), Fusarium roseum
(4%), Pythium debaryanum (4%), Verticillium albo-atrum (4%), Pythium
ultimum (3%), P. arrhenomanes (3%), and Clitocybe tabescens (3%), and
together make up 62% of all root-infecting fungi. There are 235 species of
fungi listed as causing root diseases in North America.
Most wilts are caused either by Verticillium albo-atrum or by Fusarium
oxysporum. Wilts are sometimes reported when there is no vascular invasion;
instead plants wilt from a massive destruction of the root system. Such
disease syndromes are not considered as wilt in this chapter and wilt is
restricted to diseases where the vascular system is invaded.
1.3. Host and type of parasitism
Root diseases may be classified on the basis of host, in which the
root-infecting fungi cause damping-off, seedling blight, root rot, foot rot,
crown rot or wilt. Wheeler (1969) grouped plants into annuals and perennials
3
then subdivided pathogens on annuals into three groups: (i) pathogens that
perennate as sclerotia or resting spores and have a wide host range,
(ii) pathogens that perennate as resting spores and have a restricted host
range, and (iii) pathogens that perennate as mycelium in crop debris and
have a somewhat restricted host range. He treated wilt separately.
Luttrell (1974) combined organisms according to their mode of nutrition
and way of life (autotrophs and heterotrophs). In his system, parasitic fungi
(heterotrophs) comprise three broad categories: biotrophs, hemibiotrophs,
and perthotrophs. Biotrophs must complete their life cycles on host plants,
whereas hemibiotrophs can become parasitic after a saprophytic phase. Few
root-infecting fungi are 'biotrophs but many would be hemibiotrophs.
Perthotrophs are fungi that grow from a food base of fungus origin, such as
sclerotia or rhizomorphs, prior to parasitism. Other workers, such as Griffin
(1972) have emphasized the importance of substrate composition and the
physical ecology of soil fungi.
1.4. Ecological relations
Garrett (1970) has characterized many of the root pathogens ecologically
as root inhabitants or soil inhabitants. Root inhabitants are considered to be
ecologically obligate parasites, whereas soil inhabitants grow well sapro-
phytically and can survive longer in soil in the absence of a susceptible host
plant. Garrett points to the ectotrophic habit of growth as a means for
root-infecting fungi to exist, at least for a time, as symbionts with the host
until the inoculum potential is high enough for pathogenesis to be
established, and the host resistance overcome.
Many other works treat the ecology of soil fungi and these include
volumes edited or written by Parkinson and Waid (1960), Baker and Snyder
(1965), Toussoun et al. (1970), Baker and Cook (1974), and Bruehl (1975).
1.5. Pathogen—host dominance system
We have arranged root-infecting fungi in a sequence from the unspecial-
ized pathogens that attack plants having little or no disease resistance to
pathogens having an increasing degree of specialization in which the
pathogen is dominated more and more by the host and a near-symbiotic
relationship is attained. Our approach differs from others in that we are
classifying the interaction of fungus and plant root. From this standpoint
there appears to be a continuum of fungus—root interactions that reflects an
increasing trend toward symbiosis; however we have separated diseases into
two groups: pathogen-dominant diseases and host-dominant diseases.
In the pathogen-dominant group, the pathogen is dominant over the host,
but the relationship is transitory because the resistance of the host is less
4
initially than it becomes eventually. Such pathogens are tissue-non
specific and attack young, immature root tissues or senescent tissues of
mature plant roots. They seldom damage a rapidly growing, maturing root,
so the period of disease development is short. Sometimes such pathogens are
macerative in that they digest their way through host tissues; sometimes they
are toxicogenic and kill tissues by toxins in advance of penetration, or
sometimes both can occur. In any of these situations, pathogenesis is due
primarily to the virulence of the pathogen, and the host has little influence
on the course of disease; the pathogen is opportunistic in that its virulence
depends upon the chance of its being located near a young root at the time
when factors are favorable for the pathogen. Physiological specialization is
relatively uncommon.
In the host-dominant diseases are included those in which the host is
dominant and the pathogen is successful only when factors favor the
pathogen over the host. The resistance of the host, or the factors favoring
host growth are strong enough to keep the pathogen from advancing too
rapidly against the host defenses during the vegetative growth phase and the
host thereby prolongs^the relationship. Damage is most severe in plants in
the reproductive and senescent phases. In this group are some pathogens
which are tissue-nonspecific but most are tissue-specific. This represents a
degree of specialization within the group of host-dominant diseases. Again,
the pathogen may be macerative, toxicogenic, or both.
In any study of root-infecting fungi there are frequently complexes of
fungi, or complexes of fungi and other taxa, that complicate the host-
pathogen relationship; in fact, all root diseases may be the result of
complexes of organisms. In some complexes there appear to be primary
pathogens and one or more secondary pathogens or saprophytes which
accentuate damage from primary ones. In other complexes there appear to
be two or more pathogens that seem to be equally destructive and
pathogenic but the exact role of each is not clear. In still other complexes
there appears to be no readily identifiable pathogen in the complex and the
relationships among organisms isolated are obscure or uncertain. Some
complexes behave like pathogen-dominant ones, others like host-dominant
ones while still others have characteristics of both types.
Many plant structures in soil are not roots, but are modified stems. These
include rhizomes, tubers, corms, and stolons. Diseases of these structures will
not be treated in this chapter nor will those of modified leaves, such as
bulbs. However, where these structures as well as seeds serve as the propagule
for the new seeding and as a source of inoculum for a root-infecting fungus,
they may be discussed.
2. PATHOGEN-DOMINANT DISEASES; TRANSITORY RELATIONSHIP
The pathogen-dominant relationship is one which depends predominantly
on the activity of the pathogen in the early stages of plant growth. At this
5
stage the host has little or no resistance to infection and has little if any
influence on the progress of disease. Pathogenic races are generally
uncommon. The pathogens are tissue-nonspecific and attack mainly
immature tissues either by means of enzymes, toxins, or both. The result is a
transitory relationship and plants generally are killed in a relatively short
time. In seedlings, loss of cortex is crucial because stelar and secondary
tissues are still in the developmental stage and vulnerable to infection. If
there is sudden change in environmental conditions that favors host growth,
seedlings survive this early period and become established as young plants.
Then host resistance is expressed with the maturation of tissues which in
turn arrests pathogen development.
As plants end their vegetative growth and enter the reproductive period,
the pathogen-dominant fungi resume their activity in infected roots, hasten
senescence by destroying roots, and bring about premature death of plants.
2.1. Macerative pathogens
Enzymes, toxins, growth regulators, polysaccharides, and antibiotics are
known to be secreted by pathogens in host tissues. Of these, enzymes and
toxins probably play a stronger role in pathogenesis than other compounds
do, and these are emphasized in our treatment. The mechanism of
penetration is probably enzymatic or toxicogenic, and in a few instances
perhaps both, and not mechanical.
As stated by Bateman (1968), it is difficult to define on a chemical basis
the phenomenon of tissue maceration. In his view, it might be attributed in
part to a lack of understanding of the chemical structure of the "intercellular
cement" between plant cells, as well as the routine use of enzyme mixtures
in studies of tissue maceration.
Enzymes produced by fungi affect host tissues in various ways and include
degradation of structural components of the cell wall, degradation of sub
stances inside the cell or interference with cellular functioning systems
(Agrios, 1969). In discussing the role of enzymes in pathogenesis, the term
maceration is used to mean dissolution of host tissues by enzymes. Such
tissues are characterized by a soft, watery decay and, when transferred to
water, they break into individual cells, or small clumps of cells. Maceration
appears to be initiated in the middle lamella where pectic enzymes, including
pectin methylesterase and chain-splitting enzymes act on a(l,4)glycosidic
linkages between galacturonic acid residues. Pectic enzymes have been found
to be produced by many fungi, either constitutively or inductively, and
probably facilitate inter- or intracellular invasion of plant tissue. The import
ance of cellulolytic, hemicellulolytic, and other enzymes in pathogenesis has
received scant attention although any or all of these enzymes may play a
significant role in maceration (Brown, 1965). The fungi that we classify as
macerative elicit typical symptoms of enzyme activity and frequently have
