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Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study of subterranean clover root diseases in the South-Wesf of Western Australia

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Subterranean clover (Trifolium subterraneum) is an important component of Mediterranean dryland pasture ecosystems, such as in the south-west of Western Australia, where it is utilised as a winter annual pasture that provides nitrogen as well as disease breaks for rotational crops. Necrotrophic soil-borne fungal pathogens dominate Mediterranean ecosystems because of the ease of survival of these pathogens on infested residues over the dry summer period, and because of low levels of microbial competition in the impoverished and nutrient-defi cient soils characteristic of these regions that predisposes plants to root diseases. In addition to herbage and seed yield losses from soil-borne fungal and nematode pathogens, changes in botanical composition, in the number of regenerating plants, their persistence, and factors affecting feed quality are signifi cantly affected. Further, where the causal organisms of the diseases on subterranean clover are also common on other rotational crops, the impact of these soil-borne pathogens appears far wider in Mediterranean ecosystems than previously considered. Under these conditions, soil-borne pathogens pose a serious threat to the productivity of this self-seeding pasture legume, to the extent that reseeding may become necessary. Pathogens such as Phytophthora clandestina, various Pythium species particularly Pythium irregulare, Aphanomyces sp., Rhizoctonia solani, one or more Fusarium species, Phoma medicaginis and Cylindrocarpon didymium are of concern, as are the nematode parasites from the genera Meloidogyne, Heterodera, Pratylenchus, Trichodorus and Radopholus. In this ecosystem, root pathogens operate together as disease complexes and the challenge therefore has been to source host genotypes with resistance to multiple pathogens. In addition to plant nutrition, environmental factors, in particular rainfall (soil moisture) and soil temperature, have a marked effect on both the disease severity caused by individual pathogens and on the interactions that occur between the different root pathogens. Approaches to disease control in this region include a range of management strategies. Cultural control strategies, including manipulation of grazing and rotations, offer some benefi ts. Manipulation of soil fertility also offers scope as this can enhance root physiology related to host resistance, overall plant growth and vigour, and also to improve the effective biological buffering against the pathogens. Fungicide treatments and manipulation of management practices may have a place in an integrated control system incorporating cultivars with useful resistance to root diseases. Clearly, host resistance offers the most cost-effective, long-term control, especially as resistance to several of these soil-borne pathogens has been identifi ed. The Mediterranean Basin, which is the centre of origin of this pasture legume, has proved to be a productive source of resistance to soil-borne necrotrophic pathogens and is likely to be a source of new subterranean clover cultivars.
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239
Phytopathol. Mediterr. (2007) 46, 239–258
REVIEW
Key words: necrotrophic pathogens, management, fungi, nematodes.
Management of root diseases of annual pasture legumes in
Mediterranean ecosystems - a case study of subterranean clover root
diseases in the south-west of Western Australia
MARTIN BARBETTI
1,3
, MINGPEI YOU
2,3
, HUA LI
2
, XUANLI MA
1
, and KRISHNAPILLAI SIVASITHAMPARAM
2
1
School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia,
Nedlands WA 6009 Australia
2
School of Earth and Geographical Sciences, Faculty of Natural and Agricultural Sciences, The University of
Western Australia, Nedlands WA 6009 Australia
3
Department of Agriculture and Food Western Australia, Baron-Hay Court, South Perth, WA 6151, Australia
Summary. Subterranean clover (Trifolium subterraneum) is an important component of Mediterranean dryland
pasture ecosystems, such as in the south-west of Western Australia, where it is utilised as a winter annual pasture
that provides nitrogen as well as disease breaks for rotational crops. Necrotrophic soil-borne fungal pathogens
dominate Mediterranean ecosystems because of the ease of survival of these pathogens on infested residues over the
dry summer period, and because of low levels of microbial competition in the impoverished and nutrient-de cient soils
characteristic of these regions that predisposes plants to root diseases. In addition to herbage and seed yield losses
from soil-borne fungal and nematode pathogens, changes in botanical composition, in the number of regenerating
plants, their persistence, and factors affecting feed quality are signi cantly affected. Further, where the causal
organisms of the diseases on subterranean clover are also common on other rotational crops, the impact of these soil-
borne pathogens appears far wider in Mediterranean ecosystems than previously considered. Under these conditions,
soil-borne pathogens pose a serious threat to the productivity of this self-seeding pasture legume, to the extent that
reseeding may become necessary. Pathogens such as Phytophthora clandestina, various Pythium species particularly
Pythium irregulare, Aphanomyces sp., Rhizoctonia solani, one or more Fusarium species, Phoma medicaginis and
Cylindrocarpon didymium are of concern, as are the nematode parasites from the genera Meloidogyne, Heterodera,
Pratylenchus, Trichodorus and Radopholus. In this ecosystem, root pathogens operate together as disease complexes
and the challenge therefore has been to source host genotypes with resistance to multiple pathogens. In addition to
plant nutrition, environmental factors, in particular rainfall (soil moisture) and soil temperature, have a marked effect
on both the disease severity caused by individual pathogens and on the interactions that occur between the different
root pathogens. Approaches to disease control in this region include a range of management strategies. Cultural
control strategies, including manipulation of grazing and rotations, offer some bene ts. Manipulation of soil fertility
also offers scope as this can enhance root physiology related to host resistance, overall plant growth and vigour, and
also to improve the effective biological buffering against the pathogens. Fungicide treatments and manipulation of
management practices may have a place in an integrated control system incorporating cultivars with useful resistance
to root diseases. Clearly, host resistance offers the most cost-effective, long-term control, especially as resistance to
several of these soil-borne pathogens has been identi ed. The Mediterranean Basin, which is the centre of origin of
this pasture legume, has proved to be a productive source of resistance to soil-borne necrotrophic pathogens and is
likely to be a source of new subterranean clover cultivars.
Corresponding author: M.J. Barbetti
Fax: +61 8 64887077
E-mail: mbarbett@cyllene.uwa.edu.au
Phytopathologia Mediterranea
M. Barbetti et al.
240
Introduction
Necrotrophic pathogens dominate regions with
a winter-dominant rainfall, including those with a
Mediterranean-type climate, because of the ease
of survival of these soil and trash-borne pathogens
on infested residues through the dry summer
periods. The impoverished and nutrient-de cient
soils across many parts of these regions predispose
the plant host to these pathogens as there is often
little microbial competition with the necrotrophic
pathogens (Sivasithamparam, 1993). Hence, it is
not unexpected that necrotrophic fungal patho-
gens provide signi cant challenges to productive
utilisation of subterranean clover in such regions.
As global warming leads to climate change, there
may well be signi cant changes in the relative
importance of necrotrophic diseases, especially in
some regions of Australia with Mediterranean-type
climates, such as south-west Western Australia and
signi cant areas of South Australia and Victoria
(Chakraborty et al., 1998). Any increase in sum-
mer rainfall that occurs in conjunction with global
warming will lead to increased rates of breakdown
on infested residues and a more rapid decline in
inoculum levels of necrotrophic pathogens. Since
the widespread adoption of minimum tillage prac-
tices across south-west Western Australia, burial
and/or disposal of residues through tillage is now
not common and has led to greatly increased quan-
tities of infested host residues remaining, which
increase disease pressure as has occurred for the
trash-borne necrotrophic pathogen Leptosphaeria
maculans (Barbetti et al., 2000; Sivasithamparam
et al., 2005), that is responsible for blackleg disease
on oilseed rape across southern Australia.
Over 400 fungal, bacterial, viral, mycoplasma
and nematode diseases are known to affect the
productivity of pastures (Haggar et al., 1984) and
are known to play a role in affecting productivity
of predominately annual pastures in Australia
(Murray and Davis, 1996). The literature on the
productivity of pasture legume species such as
subterranean clover has been previously reviewed
in relation to root disease research undertaken
up to the mid 1980s (Barbetti et al., 1986). Plant
pathogens result in losses in subterranean clover
that can adversely affect animal feed availability.
Such losses affect industries such as wool, meat,
dairy or grain production, and these losses have
been reviewed to at least some extent previously
in Australia (e.g., Johnstone and Barbetti, 1987;
Barbetti et al., 1996). It is noteworthy that before
1970, diseases of pastures in Australia were not
considered to be a signi cant problem and therefo-
re were not thought to warrant control measures
(Sloane et al., 1988).
This review i), discusses the key characteristics
of the agricultural ecosystems of Mediterranean
regions and the relevance of pastures therein; ii),
de nes the role of subterranean clover in Mediter-
ranean ecosystems in south-west Western Austra-
lia and the challenge posed to it from diseases; iii)
addresses the impact of soil-borne fungal and ne-
matode pathogens in these ecosystems in Western
Australia and the dif culties in assessing their true
impact; iv) describes the signi cance of the disease
symptoms and the major fungal pathogens involved;
v) describes the environmental in uences on biotic
stress imposed by fungal root diseases; vi) outlines
the key soil-borne plant parasitic nematodes and
their response to environmental conditions; vii) di-
scusses the interaction of plant nutrition and soil-
borne pathogens; viii) addresses the implications of
diseases of Mediterranean ecosystems for rotational
pasture and cropping systems; and, ix) addresses
the approaches on the disease management made
to date using chemicals, cultural practices, and host
resistance. For this review, we have based our de-
nition of the term “necrotroph” on that of Agrios
(2004), to mean an organism that has at least one
part of its life cycle on dead host/tissue and that can
grow on arti cial nutrient media.
Key relevant characteristics of the agricultural
ecosystems of Mediterranean regions and the
relevance of pastures there-in
The Mediterranean climate can best be described
as “a transitional-regime temperate and dry tropical
climate characterised by a concentration of rainfall
in winter, occurrence of a distinct summer drought
of variable length, high variability in precipitation
from year to year, mild to warm or hot summers,
and cool to cold winters with an absence of continen-
tal thermic excursion, and intensive solar radiation
especially in summer” (Sivasithamparam, 1993).
Even in spring, high rates of evaporation and high
winds can lead to large de cits for agricultural
activities (Cooper et al., 1987).
While the Mediterranean regions are predomi-
nantly characterised by brown earths, brown and
241
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Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
red Mediterranean soils and cinnamon soils (Bri-
dges, 1970), variations in soil formation processes
in these regions have resulted in a mosaic of soil
types. It is mainly on the basis of different conten-
ts of plant nutrients in the soil that two groups of
Mediterranean lands have been differentiated, viz.,
the moderately fertile soils of Chile, California and
the Mediterranean Basin, and the infertile soils of
South Africa and Australia. In these latter two
countries, soils have developed from nutrient-poor,
very old parent materials or infertile siliceous san-
ds, have been highly weathered, and highly leached,
and their levels of macro- and micro-nutrients have
been greatly reduced (Sivasithamparam, 1993).
Annual pasture species, including subterra-
nean clover, play an important agronomic role in
dryland farming in Mediterranean-type regions
where they are often an integral component of ro-
tational grazing systems and/or cropping systems.
They are particularly important in these regions,
including the Mediterranean ecosystems of south-
west Western Australia, much of South Australia
and parts of Victoria, which not only have a typi-
cal Mediterranean-type climate, but where pasture
legumes grow as winter annuals for animal feed
that also provide both nitrogen and disease breaks
for rotational crops, especially cereals and oilseed
rape. Ley farming has been the traditional crop
rotation system in Western Australia (Underwood
and Gladstones, 1979), whereby the pasture phase
is reliant on self-regeneration of annual legumes
from hardseeds which remain dormant during a
cropping phase of 1 or 2 years. Since the 1970s grain
legumes, particularly lupins, eld peas and faba
beans, have been increasingly incorporated into
many of these cropping rotations in place of pasture
legumes (Nichols et al., 2007). In higher rainfall and
irrigated areas, pastures tend to be permanent or
semi-permanent, supporting meat, wool and dairy
production (Nichols et al., 2007).
Role of subterranean clover in the Mediterranean
ecosystems of south-west Western Australia and the
challenge from diseases
Rainfed subterranean clover is the most impor-
tant pasture legume in the Mediterranean regions
of southern and eastern Australia (Morley, 1961;
Powell, 1970; Gladstones and Collins, 1983) par-
ticularly between latitudes 30 to 39°S and were
sown over an estimated area of 16 million ha or
more of dryland pasture (Gladstones, 1975; Cocks
et al., 1978; Collins and Gladstones, 1984) by the
mid-1970’s. The area sown has more recently been
revised upwards to over 22 million ha in Australia
(Sandral et al., 1997). Subterranean clover is the
main basis of the improved pastures upon which
southern Australia’s animal industries depend and
the nitrogen it xes is the foundation for much of the
country’s cereal industry (Gladstones and Collins,
1983). Even in the Mediterranean ecosystems of
south-west Western Australia, by the mid 1970’s
some 6 million ha of subterranean clover were sown
(Gladstones, 1975).
Particular advantages of subterranean clover as
an annual pasture legume include substantial in-
creases in stock carrying capacity, and increases in
yields of subsequent cereal crops as a consequence
of their ability to x nitrogen. Other advantages
include its ability to tolerate a variety of pasture
management practices, including heavy continuous
grazing, and its outstanding effectiveness in pre-
venting soil erosion. Additionally, the dense, rather
shallow root system is highly effective for building up
soil nitrogen, organic matter and physical structure.
A nal advantage of subterranean clover is its relati-
ve tolerance of water-logging (Gladstones, 1975).
In recent years, there has been a growing em-
phasis on improving the productivity of annual su-
bterranean clover-based pastures by intensifying
grazing and feed-base utilisation systems (Barbetti
et al., 1996). Intensive grazing management often
leads to increases in disease-induced losses in feed
as production levels come closer to the limit of both
pasture and the individual cultivar potentials. This
is particularly noticeable in areas where the uti-
lisation of monocultures or near-monocultures in
short leys is increasing, for while such cultures
often increase yield, they do not provide the buffe-
ring bene ts that result from having other genera
present, and consequently losses from diseases are
exacerbated.
Losses in subterranean clover from foliar disease
(Barbetti, 1987; Barbetti and Nichols, 1991; Bar-
betti, 1996) have generally been better quanti ed
than those for soil-borne diseases. Direct losses
from disease in subterranean clover can include
diminished plant growth (i.e., decreased herbage),
nutritional value (e.g., protein, individual amino
acid and water-soluble carbohydrate content, and
dry matter digestibility), palatability, seed set
Phytopathologia Mediterranea
M. Barbetti et al.
242
and seed viability, and increased toxin production
(e.g., tannins, phenols, mycotoxins) (Barbetti et
al., 1996). Indirect losses include diminished host
persistence, residual xed nitrogen, utilisation of
inputs to plant growth (e.g., inef cient fertiliser and
water use), and animal productivity, and also the
increased cost and side-effects of control (Barbetti
et al., 1996). In particular, mycotoxins produced
by necrotrophic soil-borne fungal pathogens (e.g.,
Phoma medicaginis [Mortimer et al., 1977; M.J.
Barbetti, unpublished data], F. acuminatum and
F. avenaceum [Barbetti and Allen, 2005, 2007]),
associated with legume pastures in south-west
Western Australia pose a signi cant threat to feed
quality in this Mediterranean ecosystem because
of their effects on animal productivity and, as a
consequence, potentially to human food quality.
The full extent of these threats from mycotoxins
has yet to be assessed.
Pasture legumes such as subterranean clover
contribute to the saprophytic survival of fungal pa-
thogens, including those of rotational crops, by pro-
viding the soil nitrogen necessary for saprophytic
growth and colonisation. In particular, soils with
low C:N ratios tend to favour saprophytic survival
of several soil-borne cereal and legume pathogens
(Garrett, 1970).
It has been established that pathogen complexes
have a synergistic effect on the severity of the di-
seases they cause on legumes. Diseases of pasture
species caused by such complexes warrant special
management strategies as the responses of indivi-
dual pathogens to fungicides and cultural practices
differ.
One of the major challenges is to manage such
disease complexes under the traditional rotation
systems utilised under Mediterranean ecosystems
where there can be both long pasture legume phases
and/or rotation with different crop species that are
also hosts to these same pathogens on pasture legu-
mes. This aspect is addressed further in a speci c
section of this review.
Impact of soil-borne fungal and nematode
pathogens in Mediterranean ecosystems in Western
Australia and the dif culties involved in assessing
the nature of the impact
Root rot has seriously affected production from
subterranean clover pastures in Mediterranean eco-
systems in south-west Western Australia for several
decades (Johnstone and Barbetti, 1986) and some
of the impacts have been de ned in earlier reviews
(e.g., Barbetti et al., 1986).
In south-west Western Australia, pasture decline
was rst recognised by Shipton (1967). Large areas
were found to be affected by pasture decline due
to root rot (MacNish et al., 1976; Gillespie, 1983c),
with heavy production losses resulting from severe
root rot in situations where a large percentage of
seedlings were killed even prior to emergence, and
where emerged seedlings died from root rot in the
rst few weeks of the growing season (Barbetti and
MacNish, 1983). Wong et al. (1985b) reported that
seedling losses in the eld from damping-off could
exceed 90%. Barbetti (1984e) showed an inverse re-
lationship between the severity of rotting of the tap
root system and plant size. The greatest reduction
in plant size from root rot occurred from 6 to 7 weeks
after emergence till 16 to 17 weeks into the growing
season. Such reductions often exceeded 70%, sugge-
sting that yield from pastures with severe tap root
rot may be very poor. Barbetti (1984e) showed that
rotting of the lateral root system had little effect on
plant size, probably because most plants can rapidly
produce new lateral roots to offset those damaged
or lost from root rot.
While there is a considerable amount of in-
formation on soil-borne pathogen-induced losses
in subterranean clover, a signi cant proportion
of this only comes from experiments involving
glasshouse or controlled environment conditions
(e.g., Barbetti and Sivasithamparam, 1987). While
showing the capacity of a pathogen to cause da-
mage, such studies are done under conditions that
are not directly related to what happens in grazed
commercial subterranean clover pastures and the
information provided cannot be reliably extrapola-
ted to such pastures. There is a need to assess soil-
borne fungal and nematode-induced losses in eld
situations that allow the data obtained to be used
to make rational disease management decisions
and economic assessments. Grazed monoculture
rst year swards could provide such information,
providing more relevant data than those obtained
under glasshouse or controlled environment condi-
tions. Relatively little work has been done to date
in regenerated commercial subterranean pastures.
This is probably because their use involves more
complex assessments, mainly due to the presence
of more than one plant species in these pastures.
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Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
There are a number of issues that, if addressed,
should lead to improvement in the assessment of
soil-borne fungal and nematode pathogen-induced
losses in subterranean clover occurring across sou-
th-west Western Australia. It is desirable that the
level and impact of individual soil-borne fungal and
nematode pathogens and their complexes be de ned
throughout as much as possible of the geographic
range of the pasture species they infect, within
and between years, and include periods when feed
is a limiting factor. Herbage and seed yield losses
should be assessed in grazed monoculture swards
or, wherever possible, in mixed species swards or
grazed commercial pastures, along with pathogen-
induced changes in botanical composition, numbers
of plants regenerating, persistence after the rst
year, rotational effects (such as nitrogen availa-
bility) and factors affecting feed quality (such as
production of phyto-oestrogens and mycotoxins).
There would be signi cant bene t from improve-
ment of economic evaluation packages or models,
from making them more user-friendly, and in
particular from employing them more widely in
relation to pasture diseases (Barbetti et al., 1996).
There should be wider appreciation of the need for
better management of soil-borne pathogens and the
bene ts to subterranean clover pastures that could
be derived from such management.
Signi cance of disease symptoms and fungal
pathogens involved
Root rots of subterranean clover are widespread
in the Mediterranean ecosystems of south-west
Western Australia. The above-ground symptoms
of root rots in subterranean clover vary in different
locations across this region, most likely because of
peculiar environmental and/or nutritional diffe-
rences (Barbetti and MacNish, 1983). Root disease
on subterranean clover disease can be evident as
stunted yellow-green, yellow-red, or red-purple
plants (Barbetti, 1983c; Barbetti and MacNish,
1983) scattered among apparently healthy plants,
or the affected areas may occur in distinct patches
(Barbetti and MacNish, 1983). In some situations,
restricted areas of subterranean clover within a
paddock may be diseased (Barbetti and MacNish,
1983), while in others whole paddocks may be af-
fected (Barbetti and MacNish, 1983). The internal
and external tissues of diseased roots are usually
brown and discoloured. In south-west Western
Australia, Barbetti and MacNish (1983) noted root
symptoms involving part or all of the root system
with the tap root usually being more severely da-
maged than the laterals. This is possibly because
the tap root is the rst root system to be established
on subterranean clover seedlings and it has to pe-
netrate the upper soil layers that contain most of
the pathogen inoculum in these ecosystems. This
perhaps also explains why MacNish et al. (1976)
reported a rot of the tap root con ned to 10 to 20 mm
below the crown in subterranean clover. Sometimes
affected plants produce new lateral roots above the
lesions on the tap root, and these plants may slowly
recover (Barbetti and MacNish, 1983) if there are
suf cient rainfall events for this to occur. Plants
with severely damaged root systems frequently
show stress symptoms (e.g., yellow or red colour of
foliage, wilting), and these symptoms are frequently
exacerbated by the infrequent rainfall associated
with Mediterranean ecosystems.
A number of soil-borne fungi have been shown
to have varying degrees of direct involvement in
causing root disease of subterranean clover in the
Mediterranean ecosystems of south-west Western
Australia. These include C. didymum (Barbetti,
2005), F. oxysporum (Shipton, 1967; Barbetti and
MacNish, 1978; Wong et al.,1984; Wong et al.,1985b;
Wong et al., 1986f), F. avenaceum (Shipton,
1967; Wong et al.,1984; Wong et al.,1985b), F.
graminearum (Shipton, 1967), F. moniliforme
(Shipton, 1967), F. culmorum (Wong et al.,1985b),
F. equiseti (Wong et al.,1985b), M. phaseoli (Wong
et al.,1985b), Phoma medicaginis (Wong et al.,1984;
Wong et al.,1985b), Pythium irregulare (Barbetti
and MacNish, 1978; Wong et al.,1984; Wong et
al.,1985b), P. debaryanum (Barbetti and MacNish,
1978), P. acanthicum (Barbetti and MacNish, 1978),
P. middletonii (Barbetti and MacNish, 1978), P.
spinosum (Wong et al.,1985b) Phytophthora
clandestina (Taylor et al., 1985a; Wong et al., 1985b,
Wong et al., 1986b,c), Rhizoctonia spp. (Barbetti
and MacNish, 1978; Wong and Sivasithamparam,
1985; Wong et al., 1985b), in particular
R. solani
(Wong et al., 1984; Wong and Sivasithamparam,
1985; Wong et al., 1985b) but also R. cerealis
(Wong and Sivasithamparam, 1985), and Waitea
spp. (Wong and Sivasithamparam, 1985; Wong
et al., 1985b). You et al. (2005d) characterised
a total of ten races of P. clandestina. Also in
south-west Western Australia, fungi such as F.
Phytopathologia Mediterranea
M. Barbetti et al.
244
avenaceum, Leptosphaerulina trifolii, Myrothecium
verrucaria, and P. medicaginis, commonly isolated
from subterranean clover foliage, are all reported
to cause some root disease under non-competitive
conditions (Barbetti, 1984c), in environments
commonly associated with the impoverished soils
of this region.
In south-west Western Australia, Barbetti and
MacNish (1978) showed that three frequently
isolated fungi; viz. P. irregulare in particular, P.
acanthicum, and F. oxysporum caused the most
severe root rot and most strongly reduced seedling
emergence, particularly following inoculation
with two or more fungi in combination rather
than a single fungus. Similarly, Wong et al.
(1984) showed that various combinations of F.
avenaceum, P. irregulare, R. solani, F. oxysporum
and P. medicaginis, increased the severity of root
disease and decreased plant survival and plant
weight more than when these pathogens were
tested singly. Wong et al. (1984) also showed that
P. clandestina interacted with F. oxysporum to
produce more severe root rot than did either fungus
alone. Root rot of clover clearly involves a complex
of fungi which interact not only with each other
but also with the biotic and abiotic environment
surrounding them. A range of different fungi is
normally associated with diseased subterranean
clover roots and no one fungus has been able
to reproduce the whole range of different eld
disease symptoms observed in different locations.
Investigations which implicate a single fungus as
the cause of a disorder have often been conducted
solely with that particular fungus. That a number
of different fungi are present on diseased roots,
and that they interact to enhance disease has
been demonstrated and more research needs
to be conducted into these interactions and
associations. We believe that at the current
state of investigations the most important fungi
associated with subterranean clover root rot are,
in order of importance, Phytophthora clandestina,
Pythium irregulare, Aphanomyces sp., Rhizoctonia
species and F. avenaceum. However, it is likely that
additional fungi and fungal complexes will be found
associated with diseased roots in the future as new
isolation procedures are applied. Pathogens such
as P. clandestina and Aphanomyces sp. are rarely
isolated in routine isolations even from sites known
to harbour these pathogens. Molecular probes are
expected to be more reliable indicators of the
activity of these pathogens in clover roots.
Enhanced pathogenesis due to phytotoxins
and/or mycotoxins in the soil has been reported for
a variety of pathogens (Harris and Kimber, 1983)
and this may also have a role in the predisposition
of subterranean clover to root disease, as could
mycotoxins produced by individual pathogens. For
example, where C. didymum is found in south-
west Western Australia, the frequently observed
stunted appearance of the tap and lateral roots of
C. didymum-affected subterranean clover could
possibly be a consequence of the highly toxic
mycotoxin brefeldin A produced in the root tissue
by this pathogen (Barbetti, 2005).
Certain fungi associated with root rots of
subterranean clover can be seed-borne, including
Fusarium spp. and R. solani (MacNish, 1977).
Seed-borne infestation is important for biotrophs
but less important for necrotrophs where seed-
borne infections are important only in relation to
the introduction of new pathogens or their races
to new areas. This is largely because necrotrophs
in Mediterranean ecosystems readily establish
during the pasture and/or cropping season, and their
inocula are conserved over the dry summer period
in the soil organic matter, and in some instances
in infested plant residues above ground. The lack
of any relationship between root rot incidence and
fungi associated with seed is an indication that seed
transmission is unimportant in the aetiology of root
rots of subterranean clover in south-west Western
Australia (MacNish, 1977). This view is supported by
Barbetti (1984a) who showed that removal of fungi
from subterranean clover seed had no in uence on
the severity of root diseases after sowing.
Environmental in uences on biotic stress imposed
by fungal root diseases
There have been a number of attempts to relate
environmental factors to the severity of root disea-
ses of subterranean clover ecosystems in south-west
Western Australia. For example, analysis of clima-
tic data for centres along the south coast from 1972
to 1975 showed that 1973, a particularly severe root
disease year, had signi cantly heavier and more
frequent rain after the break of season than did the
other years when root disease severity was much
lower (MacNish et al., 1976). This is not surprising,
as key oomycete pathogens such as P. clandestina,
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Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
Aphanomyces and various Pythium spp. are all
strongly favoured by wet soil conditions.
Also in south-west Western Australia, Wong et
al. (1984) investigated how soil moisture (45% water
holding capacity [WHC], 65% WHC, and ooding)
interacted in relation to the pathogenicity of F. ave-
naceum, F. oxysporum, P. medicaginis, P. irregulare,
and R. solani, both alone and in combination. It is
noteworthy that these fungi and their combinations
caused root disease particularly over the range of
soil moisture conditions that approximated to those
occurring in root rot-affected elds in south-west
Western Australia. The most severe root rotting
occurred at 65% WHC, with less at 45% WHC, and
least under ooding conditions. Conditions of 65%
WHC would frequently be expected to occur in the
higher rainfall zones of the south-west Western
Australian Mediterranean ecosystem, favouring
the oomycete pathogens. In contrast, drier soils
favoured pathogens such as Fusarium spp. and R.
solani. While signi cant rainfall events may trigger
serious attack by oomycete pathogens, these same
rainfall events are also needed for compensatory
root growth following attack by one or more soil-
borne pathogens. Wong et al. (1986e) showed that
an osmotic water potential of -12 bars prevented
mycelial growth and that optimal growth for P.
clandestina was 0 bar. Hence it was not surprising
that You et al. (2006) found that rainfall levels were
important determinants of the race distribution for
P. clandestina, with the majority and most diverse
of P. clandestina races occurring in the high rainfall
zone with 700–1000 mm annual rainfall. Such an
association of races of this pathogen with a parti-
cular rainfall zone is important in relation to the
selection/breeding and the deployment of subterra-
nean clover cultivars for particular rainfall zones
in south-west Western Australia. While other root
pathogens such as Pythium spp. and R. solani, are
also found across these same rainfall zones, Pythium
spp. appear to do most damage in the higher rainfall
zones while Rhizoctonia spp. do more damage in
the medium to lower rainfall zones (M.J. Barbetti,
unpublished data).
Barbetti (1984b) demonstrated the importance of
temperature on the severity of root rot developed in
pathogenicity tests, and that the temperature thre-
sholds vary with different pathogens and/or their
combinations. Wong et al. (1985b) showed that the
growth rate of P. clandestina increased with the
progressive increase of the incubation temperature
up to 20°C. Wong et al. (1986e) showed that sa-
prophytic survival of P. clandestina in pasteurised
soil was greater under cooler conditions (5–10°C),
and°C). Wong et al. (1986c) found that the most
severe root disease occurred at a soil temperature
of 10°C, followed by 15 and 20°C, coinciding with
autumn/early winter conditions of the Mediterra-
nean ecosystems of south-west Western Australia.
More recently, Barbetti (2005) demonstrated that
C. didymum caused most disease at the cooler tem-
perature regime of 15/10°C, a temperature regime
that would closely approximate eld soil tempera-
tures in the high rainfall coastal area of south-west
Western Australia during the winter months when
this pathogen appears to be most common.
There was a signi cant interaction between tem-
perature and moisture for the various fungi and
fungal combinations tested in Western Australia
by Wong et al. (1984). These researchers looked at
how soil moisture and soil temperature interacted
in relation to the pathogenicity of F. avenaceum, F.
oxysporum, P. medicaginis, P. irregulare, and R. so-
lani, both alone and in combination. It is noteworthy
that these fungi and their combinations caused root
disease particularly with the combination of soil
moisture and temperature conditions that approxi-
mated to those occurring in root rot-affected elds in
south-west Western Australia during germination
and early growth. Subsequently, Wong et al. (1986c)
demonstrated that P. clandestina caused pre- and
post-emergence damping-off in subterranean clover
under a range of soil temperatures (10, 15, 20 and
30°C) and moisture conditions (65 and 100% WHC
and ooding), with the greatest reductions in see-
dling survival occurring in saturated and ooded
soil. Similarly, Wong et al. (1986b), showed that
there was a marked reduction in the growth of P.
clandestina with increasing water stress across
the range of temperatures that could be expected
in south-west Western Australia, suggesting that
for pathogens such as P. clandestina, water stress
is more important than the variations in tempe-
rature expected to occur in that region. Wong et
al. (1986e) showed that while saprophytic survival
of P. clandestina in pasteurised soil was optimal
under cooler conditions (5–10°C) at all water po-
tentials tested (-0.01, -0.026, and -0.063 bars), yet
at higher temperatures (15–32°C) P. clandestina
survived much better in wetter soil. Clearly there
Phytopathologia Mediterranea
M. Barbetti et al.
246
are different moisture-temperature interactions for
different individual pathogens.
In a study by Barbetti (1990), changes in the
soil pH (by the addition of lime) affected seedling
survival and the levels of rot of the tap and lateral
root systems by F. avenaceum, P. clandestina, P. ir-
regulare and R. solani. The different root pathogens
often responded differently to the addition of the
lime, and the relative cultivar resistance-rankings
to individual pathogens sometimes varied widely
depending on the amount of lime added. There was
a clear interaction between lime and cultivar and
between lime and pathogen for all parameters mea-
sured and lime shows potential for management of
root disease. Further evidence of the effect of pH
was provided by Wong et al. (1986b) who investiga-
ted the effects of temperature, pH and water poten-
tial on the growth or survival of P. clandestina and
found that while this pathogen grew on agar over
a pH range of 4–9 its growth rate increased as the
pH of the medium rose from 4 to 6 at temperatures
of 15, 20, and 25°C.
Studies on the detection of P. clandestina on in-
fected subterranean clover roots over time (Wong,
1986) showed that the pathogen was detected most
readily two weeks after germination, its activity
gradually declining after this phase. This is the
phase when the host is most susceptible and the
high incidence of the pathogen and the presence of
susceptible host (i.e., the plant and pathogen cycles)
coincide by the very nature of the Mediterranean
environment.
Wong et al. (1986a) studied the nature and
behaviour of P. clandestina in the soil and found
that the pathogen could only be recovered from
soil screenings containing small root fragments.
Exposure of P. clandestina inoculum to increasing
numbers of soil microbes reduced the severity of
root disease of subterranean clover, an indication
that P. clandestina is favoured by the relatively
poor biological buffering capacity of soils in south-
west Western Australia. Wong et al. (1986a) de-
monstrated that the most probable number for P.
clandestina propagules in a root rot-affected eld
in Western Australia was greater for the period Ja-
nuary to June than for July to December, and that
the number of propagules increased after January,
to peak in May, the month in which root rot is often
most severe (Wong et al., 1986b), coinciding with
the opening seasonal rains.
There may well be effects of herbicide applica-
tion upon the levels of root disease that occur in
subterranean clover. For example, Barbetti (1984d),
examining intact cores from Western Australian
root rot-affected elds, found that prior application
of a paraquat/diquat mixture in the form of com-
mercial Spray-seed
®
led to slight reductions in root
disease severity even though it had no effect on the
incidence of various soil-borne pathogens.
As outlined above, environmental factors such as
rainfall, soil moisture and soil temperature clearly
have a marked effect on both root disease severity
in subterranean clover caused by individual patho-
gens, and on the interactions that occur between
the different root pathogens. Further investigations
in this area may help explain some of the differen-
ces in symptoms, disease severity, etc. that occur
between different regions. Ideally, additional eld
studies should be undertaken, as has been done
for annual Medicago spp. by You et al. (1999) who
looked at how rainfall, cultural practices, soil and
plant nutrients in the eld affected root disease and
parasitic nematode numbers in south-west Western
Australia. In eastern Australia, Smiley et al. (1986),
using intact eld cores, showed that root disease
was mild on plants in continually moist cores at
10°C, and severe in cyclically wetted and dried co-
res at 10, 15 and 20°C. This is a further indication
that the uctuating soil temperature and moisture
conditions so common in Mediterranean ecosystems
have a signi cant impact upon the expression of
root disease in subterranean clover.
Key soil-borne parasitic nematodes and their
response to environmental conditions
Meloidogyne javanica, M. hapla, M. incognita,
Pratylenchus sp. and Radopholus sp. are potential
pathogens of subterranean clover in south-west
Western Australia (Shipton, 1967). More recently,
surveys of sites of subterranean clover root disease
in south-west Western Australia have indicated the
presence of the genera Meloidogyne, Heterodera,
Pratylenchus, Trichodorus and Radopholus (Pung
et al., 1988) in situations with strong evidence
for a signi cant role played by nematodes in root
disorders. For example, Pung et al. (1991a) inve-
stigated the role of M. arenaria and root rot fungi
in the decline of subterranean clover in infested
elds by soil application of the fungicide benomyl
and the nematicide aldicarb. M. arenaria appeared
247
Vol. 46, No. 3 December, 2007
Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
to be a signi cant cause of poor productivity of su-
bterranean clover, as aldicarb inhibited root-knot
nematodes and increased plant vigour.
The most comprehensive work on root-knot
nematodes and their association with fungal
root rot of subterranean clover was undertaken
in Western Australia by Pung and colleagues.
Pung et al. (1988) investigated Meloidogyne spp.
in subterranean clover in the lower south-west
of Western Australia and found that M. arenaria
occurred widely there. This was the rst record of
M. arenaria on subterranean clover in Australia
or elsewhere. They demonstrated a clear negative
relationship between gall and root disease on tap
roots and found that M. arenaria was particularly
pathogenic on subterranean clover at high inoculum
levels (> 16,000 eggs per pot).
Pung et al. (1992b) conducted pot experiments
to examine the effect that F. oxysporum and M.
arenaria, applied singly or in combination, had on
the root health and growth of subterranean clover.
They found that while M. arenaria had no effect on
root necrosis in either pasteurised or autoclaved
soil, it still adversely affected plant growth. Fur-
ther, Pung et al. (1991b) showed that the timing of
infection and the proximity of the root tips of the
host root system to infection with M. arenaria and
F. oxysporum appeared to be the major determining
factors of root growth and disease development in
plants exposed to these pathogens. For example,
they found that the induction of galls by the nema-
tode and early infection by F. oxysporum resulted
in severe inhibition of root growth, particularly of
the lateral roots.
The effect of environmental factors on M. are-
naria and its infectivity on subterranean clover
was also investigated both in a naturally infested
subterranean clover pasture and under control-
led conditions in a pot experiment by Pung et al.
(1992a). In the field, the nematode population
density was affected by seasonal changes. The
hatching of M. arenaria was determined by the
germination of subterranean clover brought about
by the opening seasonal rains in April or May. The
rst generation of M. arenaria in subterranean clo-
ver roots developed and reproduced more rapidly
while the soil temperature was still relatively high
(> 15°C) in May–June, coinciding with the opening
seasonal autumn–winter rainfall events. The se-
cond generation developed as the soil temperature
increased between September and November and
as rainfall events rapidly decreased. These ndin-
gs were consistent with observations from the pot
experiment, in which M. arenaria gall production
and its development and reproduction in both the
tap and lateral roots was greater at 20/15°C and
25/20°C than at 15/10°C. These studies showed
that the timing of the opening seasonal rains and
soil temperatures were important determinants of
the severity of disease caused by M. arenaria in
Mediterranean ecosystems. Greater nematode in-
fection in the tap roots occurred at moisture levels
of pF 1.28 and 0.97, but not at 0.71, and this may
be related to better nematode mobility at the higher
soil moisture and its preference for tap roots under
more favourable conditions.
Interaction of plant nutrition and soil-borne
diseases
Nutritional de ciencies such as those that oc-
cur in the old, leached soils of the Mediterranean
ecosystems in south-west Western Australia are
known to reduce the natural resistance of crop
plants to disease (Graham, 1983). It is however
generally accepted that diseases, especially those
caused by soil-borne necrotrophs, are frequently
exacerbated across south-west Western Australia
by nutritional stress imposed on the plant hosts.
While a correction of these de ciencies in most cases
reduces the severity rather than limits the incidence
of the diseases, it still offers some opportunities for
exploitation. Plant nutrients can reduce the severity
of diseases by enhancing plant growth and disease
tolerance. Nutrients such as phosphates enhance
host resistance by stimulating the production of
phytoalexins (compounds produced by resistant
plants challenged by the pathogen) (Gottstein and
Kuc, 1989). The macro- and micro-nutrient status of
the plant affects disease severity (Sadasivan, 1965;
Graham, 1983) and this is an area that still remains
to be explored for subterranean clover.
It is clear that nutrients affect the severity of
disease, not only by in uencing root physiology and
host resistance, but also by affecting the interaction
between the host and the pathogen and/or the anta-
gonist, each of which can also be affected indepen-
dently by the availability of nutrients. Soil fertility
can also affect disease development by its effect on
the activities of the soil micro ora that inhibit the
soil-borne pathogens. Components of soil fertility
Phytopathologia Mediterranea
M. Barbetti et al.
248
have been associated with naturally occurring soil
suppressiveness (Cook and Baker, 1983; Mukerji
and Garg, 1988). For instance, a range of factors
including organic matter, Ca, NH
4
, water content,
soil pH and extracts from the rhizosphere of cer-
tain plants in uence the suppressiveness of certain
soils to Phytophthora (Cook and Baker, 1983) and
it is likely that the same applies to P. clandestina
attacking subterranean clover. Soils in south-west
Western Australia with relatively high levels of P,
NO
3
, or Fe were associated with an increased level
of tap root disease in annual Medicago spp., while
soils with a high pH were associated with reduced
disease in the tap roots (You et al., 1999). As illu-
strated in Fig. 1, soil nutrients can affect diseases
by their effects on the nutrition of the plant host or
on the microbial antagonist(s).
Pathogens such as R. solani are capable of ex-
tensive spread in the soil by utilising the available
organic debris for energy (Garrett, 1963). This has
been aptly termed ‘combative migration’ whereby
colonization occurs in the presence of, and often in
competition with, other soil micro-organisms. In the
soils of south-west Western Australia, which are
nutrient poor and low in microbial activity, even
pathogens such as the ‘take-all’ fungus (Gaeu-
mannomyces graminis var tritici), which has a low
saprophytic ability (Garrett, 1963), can succeed in
combative migration in a Mediterranean environ-
ment (Glenn et al., 1988). This certainly indicates
that the inoculum potential of certain soil-borne pa-
thogens during the saprophytic colonization phase
can be reduced by manipulating the nutrient and
microbial status of soils supporting subterranean
clover pastures in the Mediterranean ecosystems
of south-west Western Australia.
The use of nutrient amelioration to improve the
management of soil-borne diseases caused by ne-
crotrophic pathogens is an area that has signi cant
potential. Speci cally, the critical role of nutrients
and their effects on the severity of disease, the ex-
pression of host resistance, the interaction between
Fig. 1. Ways by which soil nutrients affect diseases by their effects on the pathogen, on the nutrition of the plant host
or on the pathogen and/or microbial antagonist(s) resident in the soil. (Adapted from Sivasithamparam, 1996).
249
Vol. 46, No. 3 December, 2007
Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
host and pathogen and/or antagonists, and the criti-
cal role of nutrients on the inoculum carry-over are
areas that need to be investigated. Such areas are
currently under-evaluated, to say the least, not only
in terms of their potential to enhance host growth
and defences, but also to provide appropriate nu-
trient levels that maximise the effective buffering
activity of the biological antagonists of pathogens
in the soils of the Mediterranean ecosystems of
south-west Western Australia. It is evident that
little is currently known about the interaction of
nutrition with the major soil-borne pathogens of
subterranean clover, and improved management of
major soil-borne pathogens of pasture species across
south-west Western Australia can be expected to
occur from to a better understanding the full po-
tential for manipulating nutrition for improved
disease control.
Implications that diseases of pasture legumes in
Mediterranean ecosystems have for rotational
cropping systems
The role played by necrotrophic soil-borne
fungal and nematode pathogens may in fact be
far wider and have greater impact than previou-
sly considered. This is because there are many
instances where diseases on subterranean clover
are common to other rotational pasture species
and/or crops. Examples of such shared pathogens
include Phoma medicaginis (Khan and Barbetti,
1987) and R. solani (You et al., 2008). P. medi-
caginis can cross-infect between pasture legume
and crop species (Barbetti and Khan, 1987; Siva-
sithamparam, 1993; M.P. You, unpublished data),
perpetuating pathogen survival in the absence of
a host during crop rotation cycles and reducing or
even eliminating the expected disease-break bene t
from rotating crop species. Similarly, some strains
of P. irregulare can readily cross-infect between
subterranean clover and one or more other pastu-
re legumes and/or crop species including cereals
(Sivasithamparam, 1993; M.P. You, unpublished
data). In addition, there is a signi cant number of
diseases that are common to subterranean clover
and other widely cultivated pasture legumes such as
annual Medicago spp. (Barbetti, 1989a,b; Tivoli et
al., 2006); they include those diseases that are cau-
sed by Pythium, Fusarium, Phoma, Rhizoctonia and
Phytophthora spp. In contrast, studies by Harvey
et al. (2001) showed that host-mediated selection
occurs in relation to cereal, annual Medicago spp.
and subterranean clover isolates of P. irregulare,
suggesting that there could actually be a limited
potential in some situations to reduce the impact
of such pathogens with a wide host range by the
manipulation of rotational practices.
Studies have recently been undertaken on R.
solani strains attacking subterranean clover and
newly introduced pasture legumes in south-west
Western Australia (M.P. You, unpublished data).
However, there is a need to know how rotational
crops and pasture species respond to eld strains
of each of the major soil-borne pathogens. Speci-
cally, we need to know, rst, how strains of key
pathogens such as R. solani on other rotational
crops affect subterranean clover and new pasture
legume species and, second, how highly susceptible
cultivars of subterranean clover and new legumes
affect inoculum levels of soil-borne pathogens that
are also virulent on rotational crops (faba bean,
lupin, chickpea, pea, etc.) that are sown following
the pasture phase of cropping.
Rotational crops also probably differ in the
extent to which they in uence the populations of
speci c rhizosphere organisms that compete, an-
tagonise or suppress pathogens. For example, Cot-
terill and Sivasithamparam (1988) showed in the
Mediterranean ecosystems of south-west Western
Australia that the reduction in take-all in cereals
with different crop rotations is not simply due to
depriving the pathogen of its natural host, and that
the biotic/abiotic factors associated with rotations
may vary between crops. It is likely that a similar
situation applies to subterranean clover pathogens.
This situation may not apply to all pathogens. For
example, Wong et al. (1986b) showed that subter-
ranean clover residues were the sole source of P.
clandestina inoculum in the pasture sward of mixed
plant species not containing other pasture legume
species. In this instance, while there were unlikely
to be adverse implications for rotational crops except
for annual Medicago spp. or visa versa, it was clear
that the length of the disease break without the
presence of subterranean clover may be important
in determining the extent of inoculum carryover to
the next subterranean clover pasture.
There are the side effects resulting from the pro-
duction of mycotoxins as a consequence of infection
by one or more necrotrophic soil-borne fungal pa-
thogens such as F. acuminatum, F. avenaceum, and
Phytopathologia Mediterranea
M. Barbetti et al.
250
F. graminearum associated with annual pasture
legumes in south-west Western Australia (Barbetti
and Allen, 2005, 2007). Such Fusarium spp. can
readily cross-infect between and across different
pasture (e.g., annual Medicago spp. subterranean
clover and lucerne) and crop (e.g., barley, wheat,
oat) host genera.
Disease management using chemicals
Various attempts have been made to control root
rot in subterranean clover. The response of clover
to fungicides has been quite unpredictable partly
because Mediterranean soils are conducive to a wide
range of soil-borne fungal pathogens (Sivasitham-
param, 1993). While some early attempts to control
root diseases of subterranean clover using fungici-
des in Western Australia were not encouraging (e.g.,
Barbetti, 1983a,b, 1984b, 1985) others were more
promising (e.g., Barbetti et al., 1987b).
Some increases in seedling survival and small
reductions in root disease levels were obtained (e.g.,
Barbetti, 1984a) and in one experiment where seed
treatments with fungicides were tested in root rot-
affected elds in south-west Western Australia du-
ring the growing seasons of 1984 and 1985, large
increases in seedling survival and decreases in the
severity of root diseases were achieved. Treatments
with metalaxyl were the most promising; thiram
and propamocarb were less effective, and benomyl
and iprodione were ineffective (Barbetti et al.,
1987b). Metalaxyl and thiram showed a potential
for further development as commercial treatmen-
ts for increasing seedling survival in susceptible
cultivars being resown in areas affected with root
disease. However, this particular result contrasted
with results from another study (Barbetti, 1985) in
which six rates of metalaxyl seed treatments had no
signi cant effect on seedling survival, tap root rot,
or root dry weight in two eld sites of south-west
Western Australia.
In a eld trial in south-west Western Australia,
a single spray of Foli-R-Fos 20% applied 8 days
after the opening seasonal rains reduced both tap
and lateral root disease severity and the incidence
of P. clandestina on the tap roots of subterranean
clover (M.J. Barbetti, unpublished data).
When fungicide drenches of benomyl, metalaxyl,
iprodione, propamocarb or thiram were applied to
intact soil cores taken from elds with known root
disease in Western Australia, metalaxyl was the
most effective in reducing seedling damping-off
(Barbetti et al., 1987a). It was noteworthy that
in these studies the most effective fungicide for
reducing the level of disease in both the tap and
the lateral roots of surviving plants varied from
season to season at any one eld site, and also
between eld sites in any one season, with each of
the fungicides tested giving a signi cant reduction
in root disease on at least one occasion. Such results
strongly suggest that the root pathogens or patho-
gen complexes differed between seasons in any one
site, and between sites in any one season. In some
instances it appeared that the root pathogens or
pathogen complexes in the tap roots differed from
those on the lateral roots. Such ndings clearly de-
monstrate the dif culty in managing root disease
in subterranean clover ecosystems in south-west
Western Australia with fungicides.
Even if an effective fungicide was found, dren-
ches would not be practical or economic. However,
it is clear from the above studies that the develop-
ment of effective seed treatments is possible and
could be particularly helpful in reseeding and re-
establishing subterranean clover in the Mediterra-
nean ecosystems of south-west Western Australia
when pastures have deteriorated to the extent of
requiring reseeding. While this possibility needs
further investigation, with testing of the newer-ge-
neration fungicides, it is important to keep in mind
the costs associated with the purchase and appli-
cation of fungicides and the dif culties in knowing
which pathogen type or group to primarily target
in eld situations where pathogen complexes are
operating.
Disease management using cultural practices
Field experiments in the 1970’s in south-west
Western Australia demonstrated that appropriate
cultivation and cultural practices can signi cantly
reduce the levels of tap and lateral root rot for up
to two seasons following their application (Barbet-
ti and MacNish, 1984). The best treatments were
those of fallowing an area from August to March,
before cultivation and reseeding, or spring culti-
vation before sowing to oats followed by a March
cultivation and reseeding. However, because of the
lack of long-term persistence of root rot reductions,
the high levels of root rot still remaining even after
treatment, concern over reduced stand density, pro-
duction losses from fallowing, and greater damage
251
Vol. 46, No. 3 December, 2007
Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
from root knot nematodes following cultivation, no
cultivation or cultural practices were recommended
to farmers at that time as a means of reducing root
rot severity.
Reductions in root rot severity have been
obtained from inoculating seed with rhizobia
(Barbetti,1984a; M.J. Barbetti, unpublished data).
A strain of Rhizobium trifolii signi cantly reduced
root rot from F. avenaceum in glasshouse studies
(Wong, 1986).
The effects of soil nutrition and pH on root disea-
se are probably also important. The productivity of
pastures in southern Australia has improved over
the past fty years through the application of ferti-
lizers, particularly superphosphate. However, this
has led to increasing soil acidity problems in many
areas making conditions less favourable for plant
growth (Donald and Williams, 1954; Lee, 1980;
Williams, 1980) and more conducive to damage
from plant pathogens, particularly those causing
root disease (Stovold, 1983).
Manipulation of soil pH by the addition of lime
also should be further investigated as this can
in uence both seedling survival and the levels of
root disease. The pathogens F. avenaceum, P. clan-
destina, P. irregulare and R. solani often responded
differently to the addition of lime (Barbetti, 1990),
so on the whole disease complexes could potentially
be countered by altering the pH of the soil.
In two eld trials in Western Australia (Barbetti,
1991), complete removal of subterranean clover for
one season, or especially two seasons, signi cantly
reduced tap and lateral root disease in the year
immediately following, in which subterranean
clover was allowed to regenerate. However, after
two seasons of regeneration these effects were ei-
ther small or absent. Subterranean clover removal
was more effective in reducing lateral root disease
than tap root disease in regeneration pastures. It
is noteworthy that there were often large increa-
ses in plant size in regenerating pastures following
the complete removal of subterranean clover for
one season, or especially two consecutive seasons.
However, this effect also persisted only poorly
beyond the rst season of regeneration. Unfortu-
nately, the losses of subterranean clover herbage
and seed yield caused by removal were not offset
by the subsequent bene t from the reduction in
root disease. Removal of subterranean clover for
short periods (1 or 2 years) as an agronomic practice
may be useful in overcoming root disease problems
associated with this species in the high (> 750 mm)
rainfall zone, where severe root rot most frequently
occurs in south-west Western Australia, provided
that a suitable alternative pasture species can be
grown during the non-clover phase. This prospect
warrants further investigation.
Smiley et al. (1986) demonstrated that the remo-
val of seedling leaves to simulate grazing accentua-
ted root rot severity; hence it is likely that both the
timing and frequency of grazing will have an im-
pact on disease severity in Mediterranean regions
such as south-west Western Australia. Grazing in
this area is known to exacerbate the effects of root
disease, and in particular the recovery of pastures
from root rot following grazing can be extremely
poor (M.J. Barbetti, unpublished data). Hence, it
is likely that grazing could be timed to reduce the
impact of disease, especially at the early seedling
stages, when plants are particularly vulnerable to
root rot.
While fungicide treatments and manipulation
of management practices are not effective enough
on their own to make their use economically justi-
able for very susceptible cultivars, they may have
a place in an integrated control system incorpora-
ting cultivars with at least some resistance to root
rot. Integrated disease control is most likely to be
effective when host resistance is combined with
manipulation of cultural practices, and in some in-
stances, such as the reseeding of pastures, even the
application of fungicides may signi cantly improve
the level of overall disease control.
Disease management using host resistance
Extensive eld testing of subterranean clover
cultivars for root rot resistance in root rot-affected
areas of south-west Western Australia has been
conducted (Gillespie, 1979, 1980, 1983a). By the
early 1980’s, more than 500 introductions and
crossbreds had been tested and a wide range of
resistance observed. However, no fully resistant
clovers were identi ed at that time although many
tolerant lines were found (Gillespie, 1983b) then
and subsequently. Cultivars with a useful eld
resistance to root rot are Daliak (Gillespie, 1983a),
Dinninup (Gillespie, 1983a), Esperance (Nicholas,
1980), Junee (Nicholas, 1985a) and Karridale (Ni-
cholas, 1985b). Larisa has a moderate degree of eld
root rot resistance (Nichols et al., 1996) while that
Phytopathologia Mediterranea
M. Barbetti et al.
252
of Trikkala is less but still useful (Nicholas,1980c).
The clover cultivars Denmark (Nichols and Barbet-
ti, 2005b) York (Nichols and Barbetti, 2005h) and
Goulburn (Nichols and Barbetti, 2005d), released in
the 1990’s, all have resistance to the most commonly
occurring race of P. clandestina. The cultivars Gosse
(Nichols and Barbetti, 2005c) released in the 1990’s,
and Riverina (Nichols and Barbetti, 2005f), and the
more recently released cultivars Napier (Nichols
and Barbetti, 2005e) and Coolamon (Nichols and
Barbetti, 2005a), all have reliable resistance to
more than one of the most common races of P.
clandestina. Unfortunately, the recently released
cultivar Urana is quite susceptible to the two most
commonly occurring races of P. clandestina (Nichols
and Barbetti, 2005g).
There have been many attempts to improve the
screening of subterranean clover cultivars for root
rot resistance. Barbetti et al. (1986) screened 12
commonly grown cultivars under controlled con-
ditions for resistance to ve pathogens commonly
associated with root rot (F. avenaceum, F. oxyspo-
rum, P. medicaginis, P. irregulare and R. solani),
and under eld conditions for resistance to natural
root infections. All these cultivars showed lower
seedling survival (particularly with P. irregulare
and R. solani), an increase in tap and lateral root
disease (particularly with F. avenaceum, P. irregu-
lare and R. solani) and reduced plant size (particu-
larly with R. solani and P. irregulare). Individual
cultivars generally differed in their response to the
ve pathogens, and for any one pathogen there was
a range of cultivar susceptibilities. Cultivars with
the greatest resistance to individual root pathogens
were identi ed. However, the results for the ve
pathogens tested under controlled environment
conditions correlated with the eld data for only
some of the parameters measured, again highli-
ghting the challenge in effectively managing the
impact of disease complexes of root pathogens in
soils conducive to root diseases.
Barbetti (1989c) reported that the most resi-
stant cultivars to Western Australian isolates of
P. clandestina, at a time when the race status of
the pathogen was still unknown, were Karridale,
Dinninup, Larisa, Daliak and Trikkala. More re-
cently, 84 genotypes, including 71 T. subterraneum
subsp. subterraneum and subsp. yanninicum bree-
ding lines of subterranean clover and 13 commonly
used cultivars were screened by You et al. (2005b)
in a glasshouse for resistance to root rot caused
by the two races of P. clandestina that occur most
widely. This study established that 51 advanced
lines and 11 cultivars were sources of resistance to
P. clandestina race 001, and 36 lines and 4 cultivars
were resistant to race 173, and among these, 36
lines and 4 cultivars were resistant to both races.
Subsequently, You et al. (2006) demonstrated that
the cv. Denmark was highly resistant to races 001,
101, 141, 151 and 143, and moderately resistant to
race 121, while the cv. Meteora was highly resistant
to race 151, moderately to highly resistant to races
001 and 101 and moderately resistant to races 121,
141 and 143.
The recent work of You et al. (2005d) cha-
racterised a total of ten races (in contrast to the
5 recognized previously) and presented the rst
clear picture of the racial distribution of P. clan-
destina in south-west Western Australia. This will
be important to both plant breeders and farmers.
Differences in the distribution of race populations
(You et al., 2006) will provide a sound basis for the
selection/breeding of appropriate cultivars for the
Mediterranean ecosystems in south-west Western
Australia to counter the predominant race popula-
tions in speci c localities.
You et al. (2005c) also recently screened subter-
ranean clover breeding lines for resistance to root
rot caused either by F. avenaceum or P. irregulare.
Only one of the tested lines showed good resistance
to root rot caused by P. irregulare but this is a signi-
cant nding as effective resistance to this patho-
gen is extremely rare. High levels of resistance to
F. avenaceum were identi ed in 8 midseason lines
and 5 late season lines of T. subterraneum subsp.
subterraneum and 6 late season lines of subsp.
yanninicum. These sources of resistance will be
of signi cant value to breeding programs aimed
at developing new more resistant cultivars in par-
ticular to P. irregulare as few sources of useful
resistance to this pathogen have been identi ed
in subterranean clover. Signi cantly, seedling
survival in 14 late season and 15 midseason lines
of T. subterraneum subsp. subterraneum and in
1 line of late season subsp. yanninicum were not
adversely affected by F. avenaceum. Similarly,
seedling survival in 5 late season and 6 midsea-
son lines of T. subterraneum subsp. subterraneum
was not adversely affected by P. irregulare. More
importantly, these researchers found 4 late ma-
253
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Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
turing and 6 midseason T. subterraneum subsp.
subterraneum lines that showed no significant
reduction in seedling survival in the presence of
either P. irregulare or F. avenaceum and genotypes
carrying such seedling survival resistance to multi-
ple pathogens are rare. It is noteworthy that speci c
resistance to root disease caused by either of these
pathogens was not linked to survival levels of the
seedlings. This indicates that the selection of lines
for eld performance should not only rely on speci c
resistance to root disease but also on the overall
ability or tolerance of the seedlings to survive in the
presence of these pathogens, making the manage-
ment of disease complexes even more challenging.
Resistance identi ed to either pathogen could be
utilized to develop new cultivars for areas prone to
the root rot caused by these pathogens or used as
parental materials in breeding programs.
The most promising avenue for disease control
so far has clearly been the development and use
of subterranean clover cultivars with increased
eld resistance to root disease. Identifying sources
of resistance to individual root pathogens should
allow the development of cultivars with further
enhanced resistance to soil-borne disease. Identi -
cation of resistance to more than one pathogen in
a single clover line or cultivar is ideal. Besides the
example given above for resistance to P. irregulare
and F. avenaceum (You et al., 2005c), when You et
al. (2005a) screened 100 subterranean clover ge-
notypes including 72 advanced breeding lines from
T. subterraneum subsp. subterraneum and subsp.
yanninicum and 28 T. subterraneum commercial
cultivars in the eld for resistance to race 2 of the
foliage pathogen Kabatiella caulivora, they found
that these resistances were related to the known
resistance to major root pathogens occurring in
Mediterranean ecosystems in south-west Western
Australia. The unique importance of that study
was that the resistance of 12 genotypes of subter-
ranean clover was related to the resistance of one
or more of P. clandestina, P. irregulare, and F. ave-
naceum. The availability of genotypes with such
resistances to multiple pathogens is expected to be
particularly valuable for the breeding/selection of
subterranean clover in relation to the development
of new cultivars with effective resistance to a range
of pathogens that commonly occur in the legume-
based pasture ecosystems of south-west Western
Australia. The search for genotypes with resistan-
ce to multiple pathogens needs to be intensi ed if
there is to be improved management of diseases
where several different pathogens occur together
in the eld, which is almost always the case not
only with subterranean clover but also with other
pasture species.
It is noteworthy that the Mediterranean region
has proved to be a productive source of host germ-
plasm with excellent resistance to one or more foliar
and soil-borne necrotrophic pathogens. The value
of this region as a source of resistance to important
diseases of subterranean clover in Australia is hi-
ghlighted by the four instances of subterranean clo-
ver germplasm from Sardinia that were introduced
as new cultivars into Australia in the early 1990’s,
viz. the cultivars Denmark, Goulburn, Leura, and
York. Two of these cultivars had good resistance
to both race 1 and race 2 of K. caulivora, two had
good resistance to Uromyces trifolii-repentis, three
had resistance to Cercospora zebrina and all four
had outstanding resistance to the original race of
P. clandestina (M.J. Barbetti, unpublished data).
This is despite the fact that these diseases only
occur infrequently (e.g., C. zebrina and U. trifolii-
repentis) or are non-existent in Sardinia (e.g., K.
caulivora and P. clandestina), highlighting the
importance of seeking out further sources of resi-
stance to necrotrophic soil-borne pathogens from
the Mediterranean centre of origin, even if the
particular diseases of interest do not occur there
(Barbetti, 1996; Nichols et al., 1996; M.J. Barbetti,
unpublished data). It is essential that germplasm
from these Mediterranean regions be targeted in the
search for new cultivars of subterranean clover with
improved host resistance to both soil-borne fungal
and nematode diseases.
Conclusions
A large number of nematode and necrotrophic
soil-borne pathogens are associated with productivi-
ty decline in subterranean clover in the Mediterra-
nean ecosystems of south-west Western Australia.
They cause a wide range of symptoms, and together
pose a serious threat to subterranean clover to the
extent that reseeding of the self-seeding pasture le-
gume component may become necessary. Pathogens
such as P. clandestina, various Pythium species in
particular such as P. irregulare, Aphanomyces sp.
R. solani, and one or more Fusarium species such
Phytopathologia Mediterranea
M. Barbetti et al.
254
as F. avenaceum in particular but also F. acumi-
natum, are of concern. Other important soil-borne
necrotrophic pathogens on subterranean clover
include P. medicaginis and C. didymum in speci c
locations. Plant parasitic nematodes such as Me-
loidogyne, Heterodera, Pratylenchus, Trichodorus
and Radopholus also probably play a signi cant
role in root disorders in some localities. Across the
Mediterranean ecosystems of south-west Western
Australia, root pathogens operate together as di-
sease complexes and the challenge is to develop
management strategies to control these pathogen
complexes and to locate host genotypes with resi-
stances to multiple pathogens.
There are also signi cant challenges in assessing
the true extent of the losses from root disease. While
there is a considerable amount of information on
soil-borne pathogen-induced losses in subterranean
clover, a signi cant proportion of this comes only
from experiments involving glasshouse or controlled
environment conditions perhaps not directly related
to what happens in grazed commercial subterra-
nean clover pastures, providing information that
cannot be reliably extrapolated to the pastures.
There is a need to assess soil-borne fungal and
nematode-induced losses in eld situations that
allow the data obtained to be done to make ratio-
nal disease management and economic decisions.
More work needs to be utilized utilising regenera-
ted commercial subterranean clover pastures. In
addition, there is a need to assess the full array
and extent of both direct and indirect losses from
soil-borne pathogens, including the threat to animal
productivity, and as a consequence also to human
food quality, from mycotoxigenic soil-borne fungi
in this ecosystem.
Environmental factors such as rainfall (soil
moisture) and soil temperature have been shown
to have a marked effect on both disease severity
in subterranean clover from individual pathogens
and on the interactions that occur between the
different root pathogens. Further investigations in
this area may help explain some of the differences
in root disease symptoms and severity that occur
between different areas across south-west Western
Australia and the unreliable responses to fungici-
dal applications. These differences are a clear in-
dication that the uctuating soil temperature and
moisture conditions so common in Mediterranean
ecosystems have a signi cant impact upon the ex-
pression of root disease in subterranean clover.
It is evident that soil fertility affects the severity
of disease on subterranean clover, by in uencing
root physiology and host resistance. Improved ma-
nagement of root diseases of subterranean clover
by utilising nutrient amendments is possible, in
particular by enhancing plant growth and defences
and also by providing the nutrient bases for the
activity of the resident microbial populations that
offer biological buffering against major pathogens.
It is evident that little is currently known about
how plant nutrition affects the major soil-borne
pathogens of subterranean clover. Overall, there is
signi cant potential for the improved control of the
major soil-borne pathogens of subterranean clover
ecosystems if the full implications of host nutrition
can be determined.
The role played by nematodes and necrotrophic
fungal soil-borne pathogens is almost certainly far
wider and more important in Mediterranean ecosy-
stems than previously thought, as there are many
instances where pathogens on subterranean clover
are also common to other rotational crops. Further
investigations in this area are needed.
Disease control requires a range of management
strategies that have been utilised to varying de-
grees to control necrotrophic soil-borne pathogens
of subterranean clover, Cultural control strategies,
including grazing, manipulation of nutrition and
rotations, offer useful advantages. In particular, the
timing and frequency of grazing can be manipulated
to reduce the impact of disease in the unique Medi-
terranean ecosystem. While fungicide treatments
and the manipulation of cultural practices are not
suf cient by themselves to make their use economi-
cally justi able for very susceptible cultivars, they
may have a place in an integrated control system
incorporating cultivars with at least some resi-
stance to root disease. Indeed, there appears to be
considerable potential for developing and applying
integrated management strategies for root diseases
of annual pasture legumes in Mediterranean ecosy-
stems, particularly where the primary component
of such a control strategy is based on deploying the
best available host resistance and then capturing
additional bene ts by combining host resistance
with a manipulation of cultural practices and, in
some instances (such as the reseeding of pastures)
even the application of fungicides.
It is host resistance in particular that offers the
255
Vol. 46, No. 3 December, 2007
Management of root diseases of annual pasture legumes in Mediterranean ecosystems - a case study
most cost-effective, long-term control, particularly
as resistance to a number of these diseases has been
identi ed. It is noteworthy that the Mediterranean
Basin, from which this climate takes its name, has
proved to be a productive area for sourcing subter-
ranean clover germplasm with excellent resistance
to soil-borne necrotrophic pathogens, even if the
particular diseases themselves frequently do not
occur in the Mediterranean Basin. It is essential
that germplasm from the Mediterranean region be
targeted in the search for new cultivars of subter-
ranean clover with improved host resistance to both
soil-borne fungal and nematode diseases and this
may be the most cost-effective way to develop new
subterranean clover cultivars containing multiple
resistance/tolerance.
This review identi es various biotic stresses and
related abiotic factors that impact upon the produc-
tivity of subterranean clover as a pasture legume
in Mediterranean ecosystems. While it provides
information on aspects of root diseases caused by
soil-borne fungal pathogens and nematodes, it still
remains to be investigated how these factors impact
directly on the productivity of subterranean clover
under eld conditions, where productivity tends
to vary according to the geographical location and
seasonal effects.
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Accepted for publication: September 19, 2007
... The quality of subterranean clover establishment over the last four decades has been severely affected across Western Australia (Burnett et al. 1994;Foster et al. 2017;O'Rourke et al. 2009), which has encouraged research to investigate the key underlying causes. Soilborne pathogens have been reported to cause severe economic losses, thereby threatening the viability of this forage crop (Barbetti et al. 2007;Barbetti et al. 1986;Wong et al. 1985a), and four major soilborne pathogens-namely, Phytophthora clandestina (Simpson et al. 2011;You et al. 2005b), Pythium irregulare (Wong et al. 1984(Wong et al. , 1985b, Rhizoctonia solani (Maughan and Barbetti 1983;Wong et al. 1985a;You et al. 2008), and Aphanomyces trifolii (Ma et al. 2008;You et al. 2016You et al. , 2018-have been reported to cause root rot of subterranean clover. The severity of the disease caused by these soilborne pathogens mainly depends on cropping system (e.g., cultivar Fig. 3. Attribute scales of Crop Establishment SIMulator (screenshot of the DEXi software). ...
... choice) or seedbed soil and weather characteristics (e.g., soil texture, structure, moisture, temperature, and rainfall) (Barbetti and MacNish 1984;Hochman et al. 1990;Wong et al. 1985a,b;You and Barbetti 2017a,b;You et al. 2017a,b). In addition, there are also other components affecting the quality of subterranean clover establishment such as the impact of animal pests such as nematodes (Barbetti et al. 2007;Pung et al. 1988). ...
... The quality of crop establishment under field conditions is affected by several factors and their interactions, depending on cropping practices and production situations . For example, drought represents the most important limiting factor to cover crop establishment in southern France (Constantin et al. 2015), whereas soilborne pathogens are the major limiting factor for the establishment of forage crops across Southern Australia (Barbetti et al. 2007;Foster et al. 2017;You and Barbetti 2017a, b;You et al. 2018). However, in both cases, these abiotic and biotic factors interact not only (Continued on next page) a The impact of each attribute on the value of the immediate descendant attribute in the hierarchy is represented by Local weights while the influence of each attribute on the value of the final attribute is defined by Global weights. ...
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Under changing climate, plants need combined ability to cope with co‐occurring biotic/abiotic stresses. Understanding simultaneous plant responses to multiple stresses offers unique insights towards developing effective strategies to mitigate effects of such stresses in plants. qRT‐PCR was used to determine and compare relative gene expression ratios (RGER) of three disease resistance related genes, CHs, GAP, PAL, and three abiotic stress related genes, RPK, HSP, TrVSP, across seven time durations in relation to infection by the root pathogen Pythium irregulare under three temperature regimes in three Trifolium subterraneum varieties of varying resistance. Temperature and genotype drove biotic and abiotic stress related gene expression in Pythium‐infected plants. RGER of tested genes and their relationships differed across varieties, temperatures and infection duration (ID). For example, RGER most upregulated were CHs then PAL and RPK at 25°C and detected by 2hr ID, while that of GAP, HSP and TrV were detected by 6hr ID at all temperatures. These are the first studies to report expression of defence related genes in relation to either biotic or abiotic stress in subterranean clover. The current study not only demonstrated how RGER of tested genes and their relationships differed across varieties, temperatures and ID, but also highlight as yet unexploited opportunities to together utilize these biotic/abiotic‐related genes to develop new varieties with combined biotic/abiotic stress resistances in forage legumes that are suitable for changing climate scenarios. Examples could include RGER of PAL to identify ‘temperature‐stable’ disease‐resistant varieties, and RGER of RPK to eliminate susceptible and temperature‐sensitive genotypes.
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Studies were undertaken to examine the potential for manipulating the ecosystem by altering forage species composition, intensity of grazing or by adding Rhizobium, to enhance productivity of subterranean clover (Trifolium subterraneum) forages affected by the soilborne pathogens Pythium irregulare and Rhizoctonia solani. Levels of tap and lateral root disease on clover and its productivity were differentially and significantly affected by the relative proportions of clover to annual ryegrass (Lolium rigidum). In the presence of P. irregulare, both tap and lateral root disease decreased as % clover composition increased (R²=0.58, 0.59, respectively); but there was no such significant effect in the presence of R. solani (R²=0.08, 0.18, respectively). Increasing and maintaining high clover content in forage offers a means to both reduce root disease and increase productivity and forage legume stand persistence. With simulated grazing studies, continuous (i.e., intensive) grazing in the presence of P. irregulare resulted in the most severe tap and lateral root disease, poorest nodulation and smallest roots and shoots compared with intermittent grazing. Hence, reducing grazing intensity also offers potential for significantly increasing productivity of root‐rot‐affected clover forage. For Rhizobium studies, nodulation was reduced in the presence of P. irregulare or R. solani, the extent of this was dependent upon which pathogen and the clover variety. Overall, these different studies highlight significant potential for manipulating the ecosystem to better manage soilborne pathogen complexes and improve productivity and persistence in annual legume forage systems adversely affected by soilborne oomycete and fungal pathogens. This article is protected by copyright. All rights reserved.
Article
Subterranean clover (Trifolium subterraneum) is an important forage legume in Mediterranean regions worldwide. Aphanomyces damping-off and root disease (Aphanomyces trifolii) poses significant threat to its persistence and productivity. Studies were conducted to define how environmental explanatory variables (temperature, soil type, moisture, nutrition) and variety, influence disease severity and consequent forage productivity and persistence. Relationships were modelled using linear and generalised linear models and boosted regression trees. Linear modelling highlighted complex relationships between environmental variables and each dependent variable (emergence, tap and lateral root disease, dry shoot and root weight). All environmental variables produced significant interaction and/or main effects within each dependent variable. Boosted regression trees supported the complex nature of relationships in linear models, with temperature and either soil or variety most, and nutrition least, influential. Heat maps showed more disease for low temperatures. Least tap root disease was under high temperatures, while least lateral root disease was under medium or high temperatures, low moisture, and in sand-based soil. These are the first studies utilising modelling approaches to reveal the complexities of how fluctuating soil temperature, moisture and nutrition conditions, and soil type and variety, determine Aphanomyces damping-off and root disease severity and resultant adverse impacts on forage legume productivity and persistence. Outcomes are widely applicable across soilborne oomycete pathogens of forage legumes. Studies highlighted how warming temperatures and drying climate associated with climate change should reduce future impact and importance of this and other soilborne oomycete diseases of forage legumes favoured by cold temperatures and wet and waterlogged conditions. This article is protected by copyright. All rights reserved.
Chapter
This chapter traces the development of Subterranean clover (Trifolium subterraneum L.) plant from a roadside weed to its present role as one of the most valuable plants in Australia and describes its cultivation and usage, its taxonomy, physiology, and techniques of improvement. Subterranean clover is an unimpressive plant in grass gardens compared with many other pasture legumes. It should not be judged by its appearance but by its ability to produce energy, to fix nitrogen, to enrich the soil, and to establish and persist despite heavy grazing and unfavorable seasons. These attributes and its potential contribution to agriculture, are not readily assessed in grass gardens.