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The Distribution and Spread of Sorghum Downy Mildew in Sorghum and Maize
Fields in Nigeria and Zimbabwe

Article  in  European Journal of Plant Pathology · October 2002

DOI: 10.1023/A:1020828419923 · Source: OAI

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Downy Mildew of Sorghum drought tolerance and produces a yield where other crops
such as maize may succumb due to lack of moisture.
C H Bock1 and M J Jeger2 ( 1. Natural Resources Sorghum is also an ancient crop, having been cultivated
Institute, Central Avenue, Chatham Maritime, Chatham, for at least the last 5000 years. It was probably originally
Kent, ME4 4TB, England, UK; Present address: domesticated in northeastern A f r i c a (Mann et al. 1983).
International Crops Research Institute for the Semi-Arid Sorghum suffers from many diseases, several of which
Tropics, Patancheru 502 324, Andhra Pradesh, India; 2. have an adverse effect on yield. Investment in studying
Department of Phytopathology, Agricultural University these pathogens can lead to disease control through well-
of Wageningen, AOB 8025, 6700 EE, The Netherlands) informed disease management strategies. This in turn
contributes to sustainable food production in epidemic-
prone areas, particularly those that support a burgeoning
Introduction
population. Sorghum downy mildew, or S D M , (Per-
Sorghum (Sorghum bicolor L. Moench.) is an important onosclerospora sorghi (Weston and Uppal (C G Shaw)) i n -
crop for human consumption and animal fodder in many fects both sorghum and maize (Zea mays L.) and has
areas of the world where semi-arid conditions prevail, caused serious economic yield losses in these crops. A
including A f r i c a , Asia, and the Americas. In 1994 sor- major investment was made during the 1960's-1980's in
ghum was grown on 4.37 x 10 7 ha worldwide, which an attempt to control this disease.
compares w i t h 3.77 x 107 ha for pearl millet, the other Twelve years ago W i l l i a m s (1984) provided an excel-
major cereal grown in the semi-arid tropics (FAO lent and comprehensive review of the different gram-
Agrostat-PC, 1991-1996). The sorghum plant has good inaceous downy mildews, including P. sorghi. This

S o r g h u m / m a i z e infecting strain
Maize infecting strains

Figure I. Geographical distribution of Peronosclerospora sorghi showing regions where the sorghum/maize- and maize-infect-
ing strains occur (the maize strain in Thailand has recently been designated specific rank as P. zeae; Yao 1991).

ISMN 37,1996 33
report presents our current state of knowledge of S D M with maize, or w i l d hosts in at least 43 countries (Table 1). It is
respect to sorghum, taking into account advances since the thought to be an ' O l d W o r l d ' disease, originating in A f -
Williams review. Infection of maize or other hosts is only rica or Asia (Shaw 1981; W i l l i a m s 1984) and subse-
considered where deemed necessary, particularly if infor- quently spreading to theAmericas in the 1950's, where it
mation is lacking on a particular aspect for sorghum. was probably introduced (Frederiksen 1980a; Toler et al.
1959).
Crop loss
Sorghum downy mildew is particularly destructive be- Causal organism
cause systemic infection of the host generally results in a The following description of P. sorghi is based on that of
barren infloresence. The effect of infection on yield is Weston and Uppal (1932). The fungus produces asexual
best illustrated by reference to several reports in the liter- conidia (Fig. 2) and sexually produced oospores (Fig. 3).
ature. In a single season in the U S A , a S D M epidemic in The conidia are produced on the leaf surface on erect
grain sorghum in the coastal counties of Texas caused an conidiophores which grow out through stomata. The con-
estimated loss of US$ 2.5 m i l l i o n (Frederiksen et al, idiophore comprises a basal cell and a more or less c o m -
1969). Payak (1975) reported that in parts of India annual plex, usually dichotomously branched, expanded top
yield loss due to S D M was at least 105 t. In Venezuela, (Figure 4). The basal cell is knobbed or bulbous at the
crop loss was so severe in the early 1970's that a national bottom, then of fairly uniform diameter ( 7 - 9 μm) for a
emergency was declared (Frederiksen and Renfro 1977). length of approximately 100-150 μm. It is usually de-
In Israel both forage sorghum and maize were severely limited from the main axis by a complete septum. The
infected w i t h incidences of up to 5 0 % (Kenneth 1976), main axis has a diameter of 1 5 - 2 0 μm, and is usually 8 0 -
and in the U S A incidences of 9 0 % have been reported 150 μm long f r o m the septum to the beginning of the
(Frederiksen et al. 1969). The effect of systemic S D M is branch system. The conidiophore branches by a succes-
now more clearly understood, since models have been sion of short, stout dichotomies involving p r i m a r y , sec-
developed that show a linear relationship between inci- ondary, and tertiary branches. These terminate in
dence of systemic S D M and yield loss at normal sowing tapering sterigmata approximately 13 μm long. The
densities (Craig et al. 1989; Frederiksen et al. 1973; Tu- branches are arranged so the conidia borne on the sterig-
leen and Frederiksen 1981). mata lie in a hemispherical plane. Conidia are suborbicu-
lar (15.0-28.9 μm x 15.0-26.9 μm, most frequently
Taxonomic history 21.0-24.9 μm x 19.0-22.9 μ m ) , hyaline, w i t h a thin wall
and germinate directly by a hyphal germ tube.
A downy mildew infecting sorghum was first mentioned
in India by Butler (1907), who considered it to be Scle-
rospora graminicola. Subsequently, K u l k a r n i (1913) ob-
served the asexual phase germinated directly by means
of a germ tube f r o m conidia (rather than through zoo-
spores from sporangia), and p r i m a r i l y on this basis he
recommended designating it varietal rank - S. gram-
inicola var. Andropogonis-sorghi. Further investigation
of morphology and host range established the downy
m i l d e w infecting sorghum as S. sorghi (Weston and U p -
pal 1932). The differences observed in the mode of ger-
mination was deemed sufficient to eventually designate
the new genus Peronosclerospora to house those gram-
inaceous downy mildews, including P. sorghi, that pro-
duced conidia (Shaw 1976, 1978, and 1980). The genus
Sclerospora was retained for species that germinated by
means of zoospores from sporangia.

Origins and geographic distribution Figure 2. The asexual phase of Peronosclerospora sorghi.
Conidia are sub-orbicular, hyaline and thin-walled. Some
The geographic distribution of S D M is illustrated in Fig- conidia are in the process of germinating by a single, un-
ure 1. The pathogen has been reported to infect sorghum, branched hyphal germ tube.

34 I S M N 37,1996
 Oospores are produced w i t h i n the leaf mesophyll bet-
ween the fibro-vascular bundles (Fig. 5). They are spher-
ical, the majority being 31.0-36.9 μm in diameter,
extremes range f r o m 2 5 . 0 - 4 2 . 9 μm. The wall color is a
light shade of Mars Yellow, and is 1.1-2.7 μm thick
(extremes range from 0.3-4.3 μm). The oospore contains
finely granular material w i t h masses of oil globules. The
oospore germinates by means of an unseptate, usually
branched, hyaline germ tube, averaging 4.4 μm in w i d t h ,
extremes ranging f r o m 2 . 5 - 8 . 3 μm.

Table 1. Countries from which Peronosclerospora

sorghi has been reported 1 . Figure 3. The sexual phase of Peronosclerospora sorghi.
Oospores are spherical and thick-walled.
Region or continent Country

Africa Benin, Botswana, Burundi, Peronosclerospora sorghi is an obligate parasite. Re-

Egypt, Ethiopia, Ghana, cently, however, P. sorghi has been successfullygrown in
Kenya, M a l a w i , dual culture with host tissue on a modified White's me-
Mozambique, Mauritania dium (Kaveriappa et al. 1980). Bhat and Gowda (1985)
(Frison and Sadio, 1987), later described an improved method for obtaining con-
Nigeria, Rwanda, Somalia, taminant free dual cultures, but the inherent problems of
South A f r i c a , Sudan, maintaining these cultures has prevented them being
Swaziland, Tanzania, widely used and most culture maintenance depends on
Uganda, Zimbabwe, inoculating seedlings of the host w i t h conidia or oospores
Zambia (de M i l l i a n o 1992) and using infected plants as a source of inoculum.
Asia 2 Bangladesh, China, India,
Japan, Pakistan, Philippines Disease symptoms
Australia Queensland, Western
These are well described (Frederiksen et al. 1973; W i l l -
Australia
iams 1984). T w o types of symptoms can develop as a
North America M e x i c o , U S A (Alabama,
Arkansas, Georgia, Illinois,
Indiana, Kansas, Kentucky,
Louisiana, Minnesota,
Montana, Nebraska, New
M e x i c o , Oklahoma,
Tennessee, Texas)
Central A m e r i c a and El Salvador, Guatemala,
the West Indies Honduras, Panama, Puerto
Rico
South A m e r i c a Argentina, Bolivia, Brazil,
Colombia (Burtica et al.
1992), Uruguay, Venezuela
M i d d l e East Israel, Iran, Yemen

1. Unless otherwise indicated, all reports were obtained from the

Commonwealth Mycological Institute Distribution Maps of Plant
Disease, Map no. 179, Edition 5, Issued 1 Apr 1988.
2. Previously a maize-infecting strain of P. sorghi was thought to occur
Figure 4. A mature conidiophore of Peronosclerospora sor-
in Thailand (Bonman et al. 1983). This race is now considered a
ghi showing the basal cell, the main body of the con-
separate species, P. zeae (Yao 1991).
idiophore and the conidia attached to the sterigmata.

ISMN 37,1996 35
 result of infection, either systemic symptoms (Fig. 6)
resulting from an early infection and colonization of the
growing point, or local lesions (Fig. 7) resulting from
localized infection of the leaf lamina by conidia.

Systemic infection

Systemic infection resulting from infection by conidia or

oospores can manifest itself at any stage from about one
week after emergence. The symptoms are first seen as
chlorotic areas emanating from the leaf base of the first
leaves showing the infection. This chlorosis often covers
half the lamina (called the ' h a l f - l e a f ' symptom, Figure
8). Progressively greater proportions of the lamina of
Figure 5. Oospores of Peronosclerospora sorghi are typ- younger leaves show this symptom until the whole lam-
ically produced in parallel bands between the hbro-vaseular ina is chlorotic. As the plant ages, white or pale yellow
strands of the leaf. streaks develop from the base of the younger leaves (Fig.
9), which turn reddish brown as the inter-veinal tissue
dies and the oospores develop. As the streaks turn brown
they start to shred into long strips along the fibro vascular

Figure 6. A sorghum plant showing typical symptoms of

systemic sorghum downy mildew infection. The leaves ex- Figure 7. Typical symptoms of local lesions on sorghum
hibit chlorosis with some pale streaking in the younger caused by infection with conidia of Peronosclerospora sorghi.
leaves; the leaves tend to be narrow, and the plant has an The local lesions can be seen as discrete chlorotic to purple-
upright habit. tan areas on the leaf lamina.

36 I S M N 37,1996
 parallel edges ( 1 - 4 mm x 5-15 mm). In cool, humid
weather conidia are produced on the leaves of sytemically
infected plants and on local lesions during the night, par-
ticularly on the abaxial surface. This gives infected parts
of the plant a white down-like appearance (Fig. 11).

Epidemiology and biology

The life cycle of P. sorghi is shown in Figure 12. Conidia

of P. sorghi are produced in large numbers, they are thin-
walled, ephemeral, and can cause the rapid build up of an
epidemic. Oospores are tough walled, long-lived, and
provide a perennating stage for the pathogen, as well as a
mechanism for long-distance transport.

Conidia production, dispersal, and infection

Peronosclerospora sorghi has exacting environmental re-

quirements for asexual reproduction and infection

Figure 8. The typical 'half-leaf' symptom first manifested in

a sorghum plant systemically infected with sorghum downy
mildew. The lower part of the leaf is infected and chlorotic,
while the upper portion remains green and non-infected.

strands of the leaf resulting in the symptoms of 'leaf-

shredding' (Fig. 10). Plants that are systemically infected
as seedlings can remain stunted and often die. Systemically
infected plants are upright in habit, with narrowing of the
foliage, and are generally barren, although some grain
might be produced. Occasionally, a plant can recover and
produce normal panicles with healthy, viable grain (symp-
tom remission), but the basis for this phenomenon is un-
known (Singh and de M i l l i a n o , 1989a and b).

Local lesions
Local lesions of S D M can occur on any leaf of a sorghum Figure 9. The downy appearance of leaves infected with
plant. Such lesions develop as discreet chlorotic to purple- sorghum downy mildew resulting from the asexual sporula-
tan areas, variable in size, but generally elongate with tion of Peronosclerospora sorghi.

ISMN 37,1996 37
(Bonde 1982), Prior to conidiation in the dark, the host
must be subject to a m i n i m u m period of 4 h of high light
intensity (Schmitt and Freytag 1974). In maize, con-
idiophores form from w i t h i n stomata under suitable envi-
ronmental conditions over a period of about 6 h (Lal
1981). H i g h relative humidity ( R H ) is crucial. Shetty and
Safeeulla (1981a) found that systemieally infected sor-
ghum leaves held in the dark at 20°C produced a m a x i -
m u m of 10,800 conidia cm - 2 at 100% R H , but only 3,600
conidia cm -2 at 8 5 % R H . None were produced at 8 0 %
R H . The optimum temperature for sporulation of an
A m e r i c a n isolate on maize was between 15°C and 23°C
(Bonde et al. 1985). The optimum temperature for ger-
mination was 15°C and for germ tube growth was 22°C.
However, germination was good at 10-19°C and germ
tube growth rapid at 1 4 - 2 2 ° C . A dew period temperature
of 10-33°C is required for 4 h for infection (Bonde et al.

Figure 11. 'Leaf-shredding' typically observed in older sor-

ghum plants systemieally infected with sorghum downy mil-
dew. As the oospores reach maturity the leaves start to
shred along the fibro-vascular strands, releasing the oo-
spores into air currents; this probably allows them to be
dispersed from the host.

1978). Conidial production in the field has a marked peri-

odicity of release, and has a close relationship w i t h tem-
perature and moisture. Conidia are produced between
midnight and 0500 h when temperatures are about 20°C
and the RH > 8 5 % (Shenoi and Ramalingham 1979).
Conidia of S D M can be dispersed in air currents as far as
80 m (Rajasab et al. 1979). Germination occurs when
conidia arc mature. The germ tubes grow at random over
the leaf surface until encountering a stomata, when an
appressorium forms over the stomatal opening (Jones
1971). The penetrating structure enlarges to f o r m an oval
shaped sub-stomatal vesicle, which gives rise to one or
more infection hyphae. In susceptible cultivars, systemic
colonization progresses by the development of haustoria
Figure 10. The typical pale, chlorotic streaking in the youn- that have up to eight finger-like tubes. Hyphal growth
ger leaves of a sorghum plant systemieally infected with proceeds through the intercellular spaces of the meso-
sorghum downy mildew. This symptom is indicative of the phyll cells (Mauch-Mani et al. 1989). If a systemic infec-
early stages of oospore production. tion develops, hyphae proceed to the apical meristem of

38 I S M N 37,1996
 Intercellular mycelium
Conidiophore produces oospores in
and conidia leaf tissues

Infected sorghum
plants and collateral
hosts
Foliar and systemic
infection

Germinating
conidium

Leaves shred
and release
oospores into soil

Oospore germinates Oospore

and infects roots of host

Figure 12. The disease cycle of Peronosclerospora sorghi. Whereas sexually produced oospores will generally provide only one
cycle of infection per season, the asexually produced conidia from an infected plant can infect fresh hosts within the same
season allowing rapid build up of an epidemic of sorghum downy mildew.

the plant and invade the developing leaves and flowering adhering to feet or implements (Williams 1984). They
parts; the symptoms being manifest after at least 7 days. can survive passage through the digestive tract of a cow
Plants are most vulnerable to systemic infection caused and thus dispersal in manure is implicated (Safeeulla
by conidia for approximately 20 days after emergence, 1976). Seed transmission of oospores can also occur
after which time only local lesions are produced (Jones (Bain and A l f o r d , 1969). They can also be dispersed by
1978; Shetty and Safeeulla 1981b). Local lesions develop w i n d (Bock et al. 1995), and by water (Rajasab et al.
approximately 7 days after infection (Cohen and Sher- 1979). Oospores can survive adverse conditions for sev-
man 1977). In resistant cultivars necrosis occurs at the eral years (Safeeulla 1976). In soils the greatest incidence
penetration site (Mauch-Mani et al. 1989). of infection was observed when the temperature was
25°C and the soil moisture potential 0.2 bar (Schuh et al.
1987). Soils w i t h a high sand content support greater
Oospore production, dispersal, and infection
infection (Pratt and Janke 1978; Schuh et al. 1987). Host
Oospores of S D M develop subsequent to the fusion of and nonhost roots can stimulate germination of oospores
oogonia and antheridia initials in the mesophyll of sor- (Pratt 1978), the germ tube growing towards the mer-
ghum leaves (Safeeulla and Thirumalachar 1955). Oo- istematic region of the root where it forms an ap-
spores can be dispersed by man or animals in soil pressorium and infection peg (Safeeulla, 1976). Despite

ISMN 37,1996 39
these investigations, oospore germination and the factors using healthy seed, producing seed in areas not prone to
that affect it remain among the least well understood epidemics of S D M , breeding resistant hybrids, and ob-
aspects of S D M . serving strict quarantine legislation are all practises that
can be used to avoid seed infection. Checking seed sam-
ples using molecular probes and D N A hybridization can
Seed transmission
also be used to check for seed transmission, of P. sorghi
In the U S A , Bain and A l f o r d (1969) illustrated external (Yao et al. 1990).
transmission of oospores w i t h sorghum seed. Studies in
India have indicated that P. sorghi could be transmitted
internally in sorghum and maize seed either as mycelium Collateral hosts
(Kaveriappa and Safeeulla 1978) or as oospores ( U p -
adhyay 1987). M y c e l i u m was reported in both reproduc- Collateral hosts, common in many areas where sorghum
tive structures and in the endosperm of sorghum seed and maize crops are grown, are known to act as reser-
f r o m systemically infected plants and a direct correlation voirs for infection (Malaguti 1977). They can act either as
was observed between seed transmission and embryo i n - a source of conidia early in the season or as a source of
fection (Prabhu et al. 1983; Upadhyay 1987). Frederiksen oospores that can infest the soil. Several species of gram-
(1980b) discussed ways in w h i c h oospore contamination inae from the tribes Andropogonac, Maydae, and Panicae
and internal mycelial transmission of S D M can be are reported to be susceptible to P. sorghi and are poten-
avoided. Seed d r y i n g to below 2 0 % moisture content, tial collateral hosts (Table 2).

Table 2. Host range of Peronosclerospora sorghi

Host Author

Panicwn trypheron Shult. McRae(1934)

Pennisetum americanum (L.) Leeke Castellani(1939)
Para-sorghum sp. Karunakar et al. (1994)
Sorghastrum rigidifolium Stapf. Karunakar et al. (1994)
Sorghum aethiopicum (Hack.) Stapf. Karunakar et al. (1994)
Sorghum x aImum Perodi. Tarr(1962)
S. arundinacium (Willd.) Stap. Karunakar et al. (1994)
S. b i c o l o r x S. sudanense (Piper) Stapf. Futrell and B a i n (1967)
S. bicolor ( L . ) Moench. Bonde and Freytag (1979)
S. c o n t r o v e r s u m (Steud.) Snowden Karunakar et al., 1994
S. drummondii (Steud.) Millsp. & Chase. Karunakar et al. (1994)
S. halepense ( L . ) Pers. Frederiksen et al. (1965)
S. hewisonii (Piper) Longley Bonde and Freytag (1979)
S. lanceolatum Stapf. Bonde and Freytag (1979)
S. miliaceum (Roxb.) Snowden Karunakar et al. (1994)
5. niloticum (Stapf. ex Piper) Snowden Bonde and Freytag (1979)
S. plumosum (R. Br.) Beauv. Nagarajan et al. (1970)
S. propinquum (Kunth.) Hitch. Bonde and Freytag, (1979)
S. pugionifolium Snowden Bonde and Freytag (1979)
S. purpurea-serecium ( A . Rich.) Aschers. & Schwcrf. Karunakar et al., 1994
S. sudanense (Piper) Stapf. Nagarajan et al. (1970)
S. verticilliflorum (Steud.) Stapf. Tarr(1962)
S. controversion (Steud.) Snowden Bonde and Freytag (1979)
S. usamberance Snowden Karunakar et al. (1994)
S. versicolor Anderss. Bonde and Freytag (1979)
S. virgatum (Hack.) Stapf. Nagarajan, et al. (1970)
Zea mais ssp. mexicana ( L . ) (Schrad.) litis. Uppal and Desai (1932)
Zea mais (L.) Bonde and Freytag (1979)

40 I S M N 37,1996
Table 3. Identification of pathotypes I, I I , and III of Peronosclerospora sorghi in the USA by the differential
reaction of four sorghum inbred lines 1 .

Reaction to infection with Reaction to infection w i t h Reaction to infection w i t h

Sorghum variety pathotype I 2 pathotype II pathotype I I I

Tx412 S S S
Tx430 R R S
CS 3541 R S S
QL 3 R R R

1. Source; C r a i g and F r e d e r i k s e n , 1983.

2. S = susceptible to i n f e c t i o n , R - resistant to i n f e c t i o n .

Seasonal disease development as separate species. For example, P. heteropogonii was

designated specific rank after studies of a maize strain of
An understanding of the factors that contribute to disease
P. sorghi showed it to be ,n a different species (Siradhana et
initiation and epidemic development is necessary if ap-
al. 1980). Similarly, recent studies suggest that a maize
propriate control methods are to be recommended.
strain of P. sorghi from Thailand should be given specific
Studies of infection of sorghum and maize crops in sev-
rank as P. zeae (Bonde et al. 1992; Yao 1991). Molecular
eral geographic regions indicate that oospores and con-
and biochemical tools have proven useful for investigat-
idia vary in importance as causal agents of infection. In
ing the variability of these species (Bonde et al. 1984,
parts of India where weather conditions are conducive to
Micales et al. 1988, Yao 1991). Further observations indi-
asexual spore production conidia are responsible for
cate that at least one other maize strain of P. sorghi oc-
most of the infections, and early sowings can escape
curs in A f r i c a (Anaso ct al. 1987; Fajemisin 1980).
disease (Rajasab et al. 1980; Ramalingham and Rajasab,
Further work is needed to confirm its identity.
1981). In other areas, including the U S A , oospores are
The first indication of pathogenic variability of P. sor-
the major source of infection (Schuh et al. 1987). Soil
ghi on sorghum was observed in the U S A in the late
temperature, moisture, and texture are likely to influence
1970's when a previously resistant and popular sorghum
the incidence of systemic infection in these regions. In
hybrid was observed to be infected w i t h S D M (Craig and
South America collateral hosts are thought to be an i m -
Frederiksen 1980). Subsequently three distinct pa-
portant source of disease each season (Malaguti, 1977).
thotypes were identified on sorghum in the U S A from the
Although it has not been applied to downy mildew of
differential reaction of the inbred lines Tx412, T x 4 3 0 , CS
sorghum, Drepper et al. (1993) illustrated the potential
use of modeling epidemics to identify conditions condu- 3541, and QL 3 (Table 3, Craig and Frederiksen 1983).
cive to epidemic development of the maize downy m i l - Other pathotypes have also been identified in Brazil (Fer-
dew in Thailand. This could provide a useful tool for nandes and Schaffert 1983), Honduras (Craig and O d -
understanding the conditions that support epidemics of vody 1992), and Zimbabwe where there are reports of the
S D M at different locations. resistant variety QL 3 being susceptible (de M i l l i a n o and
Veld, 1990). Pawar et al. (1985) tested 75 sorghum v a r i -
eties for their reaction to 16 isolates from different geo-
Variability within Peronosclerospora sorghi graphic regions. They found that differential reactions
identified each of the isolates as a different pathotype.
Morphological variability between isolates of P. sorghi is
Those from A f r i c a (Nigeria and Ethiopia) and Asia had
limited (Bock 1995). Adaptation to specific environmen-
greater virulence than those from the Americas.
tal conditions is not apparent either. There appears to be
little variability in environmental requirements between
isolates f r o m diverse locations (Bock 1995; Bonde et al. Control
1985). Chemical control
Variability is thought to occur at the host range level. Prior to the late 1970's several different fungicides had
As a result, P. sorghi has been subdivided into'sorghum/ been used in an attempt to control the graminaceous
maize' and ' m a i z e ' infecting strains. However, as more downy mildews (Balasubramanian 1975; Singh et al.
information has become available on the affiliations of 1970). None of these had proved effective. However, in
the maize strains, most have eventually been designated the late 1970's the discovery of the acyl-alanine fungicide

I S M N 37,1996 41
metalaxyl-([N-(2-methoxyacetyl)-N-(2,6-xylyl)-DL-al- duced (Janke et al. 1983). It also reduces the source of
aninate) revolutionized the chemical control of these w i t h i n - season asexual spores. Roguing can also be
pathogens (Schwinn 1980). In India, seed treatments of 1 usefully applied to weed hosts so as to reduce the sources
g a i kg-1 of seed plus a foliar spray of 1 g a i L-1 40 days of external inoculum (Malaguti 1977).
after emergence ( D A E ) or foliar sprays of 2 g a i litre - 1 at
Sowing date. In Dharwad, India, late sowings of sor-
10 plus 40, or 20 plus 50 D A E gave complete control of
ghum had an increased incidence of S D M (Balasubrama-
systemic S D M (Anahosur and Patil, 1980, Venugopal and
nian 1974). Similarly in Israel, early sowings of sweet
Safeeulla, 1978). Seed treatment alone did not fully pro-
corn avoided the disease (Cohen and Sherman 1977).
tect the plant or nodal tillers f r o m systemic infection, and
This is because conidia produced in large quantities from
a spray regime was required to prevent a low incidence
plants that were infected early provided an increased inoc-
of late systemic infection developing and to control local
ulum pressure, resulting in a higher disease incidence on
lesions. However, in most cases it is unlikely that the
late-sown crops. However, where conidia are not the major
additional spray treatments are economic. Other studies
source of inoculum late sowings might not have a higher
in the U S A , where oospores constitute the bulk of sys-
disease incidence. Tuleen et al. (1980) found a lower inci-
temic infection, indicated concentrations of metalaxyl as
dence of systemic S D M in late sowings in the USA, where
l o w as 0.05 g a i kg-1 seed gave complete control, and
oospores were the principal source of infection.
concentrations greater than 1 g a i kg-1 seed caused seed-
ling death (Odvody and Frederiksen, 1984). T h e effect of host-plant nutrition. There is no clear
It remains a possibility that the graminaceous downy effect of nutrition on the incidence of systemic S D M .
mildews may develop resistance to metalaxyl, a view that Balasubramanian (1973) found that phosphorus added to
is supported by the fact that other oomycetes have devel- the soil increased the incidence of S D M on sorghum
oped resistance to this fungicide (Bruck et al. 1982; Geor- plants, but nitrogen levels had no effect. Gupta and Sir-
gopoulos and G r i g o r i u 1981). Judicious use of metalaxy adhana (1978) observed that the absence of phosphorous,
as a seed treatment is recommended, perhaps in conjunc- and deficiency of nitrogen reduced incidence of systemic
tion w i t h other means of disease control. Apart from the infection, but potassium deficiency caused greater inci-
use of metalaxyl, soil sterilization has also been shown to be dence of S D M on maize grown in a nutrient solution,
effective in reducing infection through soilborne oospores, Bonman and Pittipornchai (1984) found that in early-
but may not be practical or economic (Matocha et al. 1974). sown maize crops in Thailand the incidence of maize
downy mildew was lowered by the application of nitrogen
Cultural control or nitrogen plus phosphorus, but late-sown crops had a high
Cr op rotation. Roots of host and non-host plants cause incidence regardless of treatment. It is likely that the effect
germination of oospores (Pratt 1978) and 'bait crops' (e.g. of nutrition is associated with plant age, inoculum type and
Linum usitatissimum) grown in infested soil can reduce the pressure, and other environmental variables.
incidence of infection in susceptible sorghum crops sown in
the same soil (Tuleen et al. 1980). This w i l l have greatest Biological control
effect where oospores are the principal source of systemic
A chytrid fungus (Gaertennomyces sp.) was found to ef-
infection and infestation of the soils is severe.
fectively parasitize oospores (Kunene et al. 1990). It can
Deep tillage. Deep tillage effectively reduced both the reduce the incidence of infection in treated soils by up to
incidence of S D M and the oospore content in the upper 58%. However, field application of this organism has not
strata of infested soil (Tuleen et al. 1980; Janke et al. been developed and it is unlikely that bio-control of S D M
1983). However, it is an expensive operation and proba- w i l l become a practical reality in the near future. Other
b l y not a cost-effective means of control. parasites of oospores have also been observed although
they have not been studied in detail (de Diaz and Polanco
Over-sowing and roguing of diseased plants. By
1984, Lakshmanan et al. 1990a).
sowing up to 50% more than the recommended
agronomic o p t i m u m , the stand loss due to moderate dis-
Host-plant resistance
ease incidence leads to an acceptable plant density of
healthy plants at harvest (Frederiksen et al. 1973). A There are many reports in the literature of screening
disease incidence of 2 0 - 3 0 % can be borne at this level of sorghum lines for resistance to S D M . (Anahosur et al.
oversowing before yield is reduced. Roguing results in a 1984; de M i l l i a n o et al. 1990; Frederiksen et al. 1973;
reduced oospore population, and consequently the inci- Henzell et al. 1982; Kumar et al. 1979; Lakshrnananet al.
dence of systemic infection in subsequent crops is re- 1990b; Lu et al. 1990; Sarwar and Rao 1979; Shivana and

42 I S M N 37,1996
Anahosur 1988; Shivana and Anahosur 1990; W i l l i a m s et
al. 1982). In India, the International Crops Research Insti-
tute for the S e m i - A r i d Tropics ( I C R I S A T ) has screened a
great deal of germplasm. Up to 1988, a total of 13,101
accessions from 73 countries had been screened in the
field for resistance to P. sorghi. Of these 46 accessions
were resistant to P. sorghi (Y D Narayana, personal com-
munication). These accessions were from geographically

Table 4. Origin and number of accessions of the

world collection of sorghum germplasm screened in
the field by ICRISAT from 1981-88 and found to be
resistant to sorghum downy mildew at Dharwad, Kar- Figure 13. The spreader row technique employed by
nataka, India. breeders to ensure effective screening of sorghum germ-
plasm against sorghum downy mildew. Note the older infee-
Number Number Number
tor rows sown to the left and right of the four rows of test
of coun of lines of lines material. The infector rows were sown about 3 weeks prior
Origin1 tries screened resistant to the test material.

Eastern A f r i c a 7 3345 18
Western A f r i c a 14 3324 4 diverse sources (Table 4). Many lines of germplasm have
Southern A f r i c a 9 930 2 also been screened in the U S A (Frederiksen et al. 1993).
Northern A f r i c a and In an attempt to screen sorghum cultivars and to iden-
the M i d d l e E a s t 8 252 0 tify stable resistance and differences in pathogen-
Indian subcontinent 5 3403 12 virulence between locations the International SDM
Southeast A s i a and the Nursery ( I S D M N ) was established in 1976 ( W i l l i a m s et
F a r East 8 218 0 al. 1980). Selected results of multilocational testing of
N o r t h and Central resistant sorghum accessions at I S D M N test sites are
America 7 1476 4 shown in Table 5 (Dr Y D Narayana, personal communi-
South A m e r i c a 3 19 0 cation). Although the results of the I S D M N did not i n i -
Europe 9 71 0 tially indicate pathogen variability of P. sorghi on
Eastern Europe - 40 0 sorghum, the existence of pathotypes of P. sorghi was
Australia and Oceania 2 23 6 subsequently reported (Craig and Frederiksen 1983;
Total 73 13101 46 Pawar et al. 1985). This indicates that durable, broad-
1. Eastern Africa: Ethiopia, Kenya, Sudan, Somalia, Tanzania, based resistance to this pathogen should be sought.
Uganda, Zaire.
Western A f r i c a : B e n i n , B u r k i n a Faso, C a m e r o o n , C o n g o , Central
Methods for screening for resistance. To identify re-
A f r i c a n R e p u b l i c , C h a d , G h a n a , G a m b i a , Cote d ' l v o i r e , M a l i , sistance reliably and to investigate the inheritance and
N i g e r i a , N i g e r , Sierra L o e n e , Senegal. genetics of resistance it has been necessary to develop
S o u t h e r n A f r i c a : A n g o l a , B o t s w a n a , Lesotho, M a l a w i , Malagasy effective screening methods:
R e p u b l i c , South A f r i c a , S w a z i l a n d , Z a m b i a , Z i m b a b w e .
• Natural infection (Anahosur and Hegde 1979). This
N o r t h e r n A f r i c a a n d the M i d d l e East: E g y p t , Israel, I r a n , I r a q ,
L e b a n o n , S y r i a , Saudi A r a b i a , Y e m e n .
method is probably the least effective as there is no
Indian subcontinent: Afganistan, Bangladesh, India, Nepal, attempt to ensure the exposure of different test mate-
Pakistan. rials to the same amounts of inoculum.
Southeast Asia a n d the F a r East: M y a n m a r , C h i n a , Indonesia, • Spreader rows as a source of asexual inoculum (Fig.
Japan, P h i l i p p i n e s , South K o r e a , T a i w a n , Thailand.
13; Cardwell et al. 1993; Anahosur and Hegde 1979).
N o r t h a n d C e n t r a l A m e r i c a : C u b a , E I Salvador, Gautamela, M e x -
i c o , Nicaragua, U S A , West Indies.
The spreader rows are generally inoculated to ensure a
South A m e r i c a : A r g e n t i n a , U r a g u a y , Venzuela. uniform and high level of infection (Cardwell et al.
E u r o p e : B e l g i u m , C y p r u s , France, Greece, H u n g a r y , I t a l y , P o r t u - 1993). The test material is sown approximately 3
gal, Spain, Turkey. weeks after the spreader rows. This allows the systemic
Eastern E u r o p e .
infections in the spreader rows to develop and produce
A u s t r a l i a a n d O c e a n i a : A u s t r a l i a , Papau N e w G u n i e a .
large quantities of asexual spores over the period when

I S M N 37,1996 43
Table 5. Sorghum downy mildew incidence in selected resistant accessions in the International Sorghum Downy
M i l d e w Nursery during 1 9 7 6 - 8 6 .

H i g h e s t disease i n c i d e n c e a t l o c a t i o n s ( % p l a n t s i n f e c t e d )

Entry Origin Mana1 Per Jab Sam Dha Mys Tex

IS 1317 Tanzania -2 0(1)3 - . 3(5) 0(3) 0(1)

IS 2 1 3 2 USA - 0(1) - - 0(5) 3(3) 0(1)
IS 2204 India - 0(1) - - 0(5) 6(5) 0(1)
IS 2473 USA - 0(1) - - 3(5) 6(3) 0(1)
IS 2482 USA - 0(1) - - 2(5) 6(5) 0(1)
IS 3443 Sudan 0(3) 3(4) 0(1) 0(1) 7(5) 6(6) -
IS 3546 Sudan - 0(1) - - 1(5) 6(3) 0(1)
IS 3547 Sudan 0(3) 0(4) 0(1) 0(2) 0(6) 0(3) -
IS 4696 India - 0(1) - - 0(5) 0(2) 0(1)
IS 5616 India - 0(1) - - 4(5) 0(3) 0(1)
IS 5628 India - 0(1) - - 5(5) 0(2) 0(1)
IS 5651 India - 0(1) - - 4(5) 0(2) 0(1)
IS 5665 India - 0(1) - - 0(5) 0(2) 0(1)
IS 5743 India - 0(1) - - 0(5) 0(2) 0(1)
IS 7528 Nigeria 0(3) 0(4) 0(2) 0(2) 5(5) 14(3) -
IS 8185 Uganda 0(3) 0(4) 0(2) 0(2) 3(6) 15(5) -
IS 8283 Uganda 6(2) 0(2) 0(1) 0(1) 2(5) 3(5) -
IS 8607 Uganda 3(3) 0(4) 0(2) 0(2) 5(6) 13(6) -
IS 14387 Zimbabwe - 0(1) - - 0(5) 2(2) 0(1)
IS 18757 Australia 0(4) 0(5) 0(2) 0(2) 0(11) 0(11) -
IS 22227 Australia 0(4) 0(5) 0(1) 0(2) 0(7) 12(4) -
IS 22228 Australia 0(4) 0(5) 0(1) 0(1) 4(7) 11(4) -
IS 22229 Australia 0(4) 0(5) 0(1) 0(1) 0(7) 28(4) -
IS 27042 India 0(2) 0(3) - 0(1) 0(5) 7(5) -
D M S 652 India 100(4) 36(5) 9(2) 100(2) 100(5) 100(5) 45(1)
(Susceptible
check)

1 . L o c a t i o n s : M a n f r e d i and Pergamino ( A r g e n t i n a ) , Jabaticobal ( B r a z i l ) , S a m a r u ( N i g e r i a ) , D h a r w a d a n d M y s o r e ( I n d i a ) , Texas ( U S A ) .

2. - not tested at that l o c a t i o n .
3. N u m b e r s in parentheses indicate n u m b e r of years tested at each l o c a t i o n .

the test materials are susceptible. Humidity can be in- • A combination of spreader rows and oospore-infested
creased by using sprinkler irrigation to provide ideal plots (de Milliano, personal communication). This tech-
conditions for asexual spore production as Williams and nique is used by 1CRISAT to screen for resistance to
Singh (1981) illustrated using pearl millet downy mildew. S D M both at Dharwad, in India, and at Matopos, in
Anahosur and Hedge (1979) compared five different Zimbabwe. As in the previous technique, infected sor-
methods, and found that the infector row technique was ghum is incorporated to increase the oospore content of
the most effective at producing a high and uniform inci- the soil. Spreader rows are also sown to act as a source
dence of infection in susceptible test materials. of conidial inoculum. The advantage of this system is
• Oospore infested plots as a source of sexual inoculum that plants are subject to infection by both oospores and
(Craig 1980). W i t h this technique monocropping and conidia, which have different sites of entry, and for
p l o w i n g in of infected sorghum from test plots and which there may be evidence of differential resistance,
spreader rows is used to increase the oospore content at least in maize (Frederiksen et al. 1973).
of the soil. Test material is then sown. The main source • Artificially applied asexual inoculum (Schmitt and
of infection is through the oospores in the soil. Freytag 1974; Craig 1976; Narayana et al. 1995). This

44 I S M N 37,1996
 system is generally used in a controlled environment. Puttarudrappa et al. 1972). Quantitative inheritance has
Seedlings of test material are either whorl- or spray- also been observed by some authors. Puttarudappa et al.
inoculated w i t h a suspension of mature conidia. The (1972) suggested that two complementary genes con-
advantage of this system is that optimal conditions can trolled resistance. Bhat et al. (1982) concluded that a
be maintained and the amount of inoculum is regu- primary dominant gene with either one or two duplicate
lated. It can also provide a rapid technique for screen- genes and three complementary genes contributed to re-
ing large quantities of material in a short time. The sistance. Nider et al. (1974) reported polygenic control.
ephemeral nature of conidia of P. sorghi means they Craig and Schertz (1985) illustrated that the resistance to
must reach the host w i t h i n a short time of maturation S D M expressed by the inbred line SC414-12 was confer-
so as to ensure infection. Craig (1987) utilized the red by a single dominant gene. This resulted in an incom-
natural infection cycle of S D M to develop a system for patible host-pathogen interaction that inhibited pathogen
producing and storing conidia, that could later be used development and sporulation on inoculated leaves. G i m -
to inoculate material. However, the most successful enes-Fernandes et al. (1984) found that resistance was
long-term storage technique was developed by Gale et conferred by one or two dominant or partially dominant
al. (1975) and L o n g et al. (1978). Maize seedlings genes that were different. Neither author detected cyto-
could be infected w i t h conidia of various Per- plasmic factors of inheritance. Sifuentes and Frederiksen
onosclerospora spp. after more than 2 years storage in (1988) investigated the inheritance of resistance to three
10% dimethyl sulphoxide held in liquid nitrogen. pathotypes of P. sorghi. Their results indicated that the
• Tissue culture. Currently this method of screening for resistant variety QL 3 has two dominant genes condition-
resistance to S D M does not have a practical applica- ing resistance to each of the three pathotypes. Reddy et
tion. Mauch M a n i et al. (1989) found that callus cul- al. (1992) also found resistance in QL 3 dominant to
tures of resistant cultivars were not infected by conidia susceptibility: a two loci model w i t h independent seg-
of P. sorghi, while those of susceptible cultivars were. regation and a combination of complementary and inhibi-
However, Gowda and Bhat (1992) obtained a viable tory inter-allelic interaction appeared to be the most
dual culture when they applied asexual inoculum to the appropriate in explaining the inheritance pattern they ob-
callus of a SDM-resistant cultivar of sorghum, al- served. Further investigations are needed to characterize
though a second resistant line remained uninfected by the inheritance of resistance to S D M in other sorghum
P. sorghi in culture. This system needs to be investi- lines, and the mechanisms of resistance, which remain
gated in greater depth before it can be used as a tool in poorly understood. Resistance, preferably of a durable
resistance breeding. nature needs to continue to be incorporated into
agronomically suitable varieties. Recently symptom re-
Assessment methods. For comparing host reactions it mission has been observed in systemically infected
is necessary to develop an effective (both accurate and plants. It might be that this is another resistance mech-
precise) assessment method. Scoring of systemic infec- nism that could be utilized (Singh and de M i l l i a n o , 1989a
tion is straightforward. The incidence of systemically i n - and b).
fected plants can be recorded on at least two occasions
during the season; This should provide a realistic esti- Integrated control
mate of the incidence of systemic infection ( W i l l i a m s
Integrated control involves the use of two or more
1984). Assessment of local lesions requires that both inci-
methods of control to bring about a reduction in the
dence and severity data be recorded. In the past a 1-5
incidence of the disease (Odvody et al., 1983). The suit-
scale has been used to score this type of infection
ability of the methods used depends on the local condi-
(Singburaudom and W i l l i a m s 1978; Frederiksen 1980a).
tions. Thus, a good knowledge is needed of the
Shenoi and Ramalingham (1976) developed a 1-4 scale
epidemiology of the disease and control options available
to assess the severity of local lesion infection.
to a farmer in a given area before an integrated package
Genetics and inheritance of resistance. Sorghum is a can be implemented. Integrated control can involve
self-pollinated species which means genetic uniformity chemical control (for example, metalaxyl seed treatment),
can be attained (Frederiksen et al. 1973). However, it can cultural control (for example, deep plowing or crop rota-
be induced to cross-pollinate. Studies of the inheritance tion) and the use of host-plant resistance. The combina-
of resistance in sorghum undertaken by various authors tion of control methods can be mutually beneficial. For
suggest that it is dominant to susceptibility (Rana et al. example, Odvody and Frederiksen (1984) suggest the use
1978; Sifuentes and Frederiksen 1988) although earlier- of a resistant variety and seed treatment could extend the
workers found dominance of susceptibility ( M i l l e r 1966; life of the host resistance and prevent development of

ISMN 37,1996 45
fungicide resistance in the pathogen. The final methods Balasubramanian, K.A. 1973. Influence of nitrogen and
chosen must depend on their effectiveness in a particular phosphorus fertilizers on the expression of downy m i l -
situation and the farmer's ability to use them. dew of sorghum. Plant and Soil 3 8 : 4 7 7 - 4 7 9 .

Balasubramanian, K.A. 1974. Role of date of seeding,

In conclusion soil moisture, temperature and pH on the incidence of
downy mildew of sorghum. Plant and Soil 41:223-241.
A great deal of work has been done to increase our
knowledge base of downy mildew of sorghum during the Balasubramanian, K.A. 1975. Chemical control of
last 30 years. The availability of a number of different downy mildew of sorghum. Plant and Soil 3 8 : 4 7 7 - 4 7 9 .
disease management strategies attests to the success of
Bhat, M.G., Gowda, B.T.S, Anahosur, K . H . , and
this investment. However, there are aspects of this patho-
Goud, J.V. 1982. Inheritance of plant pigmentation and
gen that remain poorly understood. Further investigation
downy mildew resistance in sorghum. S A B R A O Journal
may enhance our understanding and contribute to the
14:53-59.
continued control of S D M . The pathogen remains a threat
to the production of sorghum (and maize) in A f r i c a , Asia, Bhat, S.S., and Gowda, P.S.B. 1985. An efficient method
and the Americas. The breakdown of resistance to S D M for culturing downy mildew fungi on host callus. Trans-
in the U S A in the late 1970's suggests we should not be actions of the British Mycological Society 84:161-162.
too complacent. However, host plant resistance probably
Bock, C . H . 1995. Studies of the epidemiology, vari-
offers the best solution to the control of S D M , as well as
ability and control of sorghum downy mildew (Per-
being the most environmentally sound method for the
onosclerospora sorghi [Weston and Uppal] C.G. Shaw) on
future management of this disease.
sorghum and maize in Africa. Ph. D. thesis. University of
Reading U K .
Acknowledgments
Bock, C . H . , Jeger, M . J . , Fitt, B.D.L., and Sherington,
We appreciate the financial support of the Associate Pro- J. 1996. The effect of w i n d on the dispersal of oospores
fessional Officers Scheme of the Overseas Development of Peronosclerospora sorghi (Weston and Uppal) C.G.
Administration, U K , for the first author. Dr Y D Shaw from systemically infected sorghum leaves. The
Narayana (ICRISAT) kindly provided information on the Downy Mildews Newsletter 9:9.
I C R I S A T sorghum breeding program and Figures 8 and
14. Dr R Bandyopadhyay ( I C R I S A T ) provided Figure 5. Bonde, M . R . 1982. Epidemiology of downy mildew dis-
eases of maize, sorghum and pearl millet. Tropical Pest
Management 2 8 : 4 9 - 6 0 .
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