Erysiphe cichoracearum (also called Golovinomyces
cichoracearum (Belanger et al. 2002) is a powdery mildew that infects four
major cucurbit crop species at CASFS and world wide: melon (Cucumis melo),
cucumber (Cucumis sativus), squash (including guards, pumpkins, and
zucchini) (Cucurbita pepo, C. peop ssp. ovifera, C. pepo
ssp. fraterna), and watermelon (Citrullus lanatus) (Belanger
et al. 2000). It has over 300 hosts (Westcott 2001), mostly cucurbits and composites
including Helianthus spp. (Sunflower) at CASFS. Other hosts include
lettuce, endive, Jerusalem artichoke, pepper, potato, salsify, Echinacea, eucalyptus,begonia,
calendula, chrysanthemum, clematis, coreopsis, phlox, salvia, stokesia and zinnia.
Agrios (1997) estimates that among crops and ornamentals, losses due to reduced
photosynthesis, plant growth, and crop yield (by as much as 20 or 40 percent)
by powdery mildew are probably greater than losses caused by any other single
type of plant disease.
Symptoms
E. cichoracearum, along with all powdery mildews, is an obligate biotroph
and thus does not kill the hosts. Rather, the fungus utilizes host nutrients
and in the process reduces growth and yield by impairing photosynthesis and
increasing respiration and transpiration (Agrios 1997).
Besides these symptoms, signs of powdery mildew are most apparent. White mycelium
and conidiophores with long chains of white conidia grow on the sunny host surface,
as though the surface was sprinkled with white powder (Macrophoto
4a).
Life History and Epidemiology
Conidial germination is sparked by the separation of the conidia from the condiophore
and by the chemical recognition of having landed on a suitable host (Belanger
et al. 2002). Many studies have been done on the development of E. pisi, so
for the purpose of this description it is assumed to have a similar development
to E. cichoracearum. Conidia germinate to produce a germ tube that
elongates to form a septum which then differentiates into an appresorium (Kunoh
et al. 1979; Sing and Singh 1983, Carver et al. 1996). A penetration peg then
develops from the appresorium that penetrates the host cuticle and into the
epidermal cell (Belanger et al. 2002). After penetration, the tip of the hyphal
penetration peg enters the cell and forms a specialized absorption structure
termed the haustorium, which is partially responsible for the transport of nutrients
from the host into the haustorium (Spencer-Phillips and Gay 1981, Gay et al.
1987). Meanwhile, on the leaf surface of the host, nutrients taken up by the
haustorium contribute to the white mycelium that continues to grow and develop
conidiophores with oblong shaped conidia attached in chains (Microphoto
4A-B). Conidia are air-dispersed and ready to be liberated and infect more
host tissue. On an individual leaf, powdery mildew distribution can either occur
as small patches or to uniformly blanket the leaf.
The powdery mildews are common in cool or warm, humid areas, but are most pervasive
in warm, dry climates (Agrios 1997). This is possible because germination can
occur without any moisture on the leaf surface, as long as the relative humidity
is high. When conditions become very dry, cleistothecia are produced on the
leaf surface (Microphoto 4C). Powdery mildew
species are most easily differentiated by the morphology of the cleistothecium.
E. cichoracearum produces a cleistothecium of about 100 micrometers in diameter
with non-ornamented appendages. Each cleistothecium contains asci containing
two ascospores (Belanger et al. 2002).
Disease Management
Resistant Cultivars. Powdery mildew resistant varieties of
Cucumis spp. and summer and winter squash (Cucurbita spp.)
are available in seed catalogues (Belanger et al. 2000). Successful breeding
for resistance in Cucurbita have stemmed partially from the transfer
of dominant resistant genes in a wild tropical species (C. lundelliana into
C. pepo (Rhodes 1959). One of the highest degrees of resistance ever
reported was in a cross between Cucummis okeechobeensis ssp. martinezii
and C. moschata ‘Butternut’(Munger 1976) which created
the progenitors of all commercial resistance now in use in C. pepo and
C. moschata (Belanger 2000). Tolerant hybrids are produced by crossing
a highly resistant with a less resistant species, however total resistance is
only achieved when both parents are highly resistant (Belanger et al. 2000).
Taste tests have ranked powdery mildew resistant cucurbita varieties as being
“sweeter and better tasting than susceptible parents” (Munger, Moriarty,
and Jahn, unpublished data in Belanger et al. 2000. p.246).
Organic Products
Elemental sulfur is effective against powdery mildew (Belanger et al. 2000,
Agrios 1997, Westcott 2001), but it can also interfere with other agroecological
goals such as maintaining natural herbivore predators. It may also be phytotoxic
in a greenhouse environment with temperatures above 27 degrees C (Bellanger
et al. 2000).
Biological
The bacterium Bacillus subtilis is registered and commercially available
(as Serenade company) and has been shown to be parasitic on powdery mildew or
to activate induced resistance in the host (Highland 2000).
The fungus Ampelomyces quisqualis, registered and commercially available
(AQ-10), has been shown to be a very effective control of several species of
Erysiphales (Sztejnbert et al. 1989, Kiss 1997), and especially under
very high humidity. Jarvis and Slingsby (1997) proposed combining application
of A. quisqualis with water spraying in dryer conditions. A. quisqualis
parasitizes powdery mildew by colonizing hyphae and conidiophores and forming
pycnidia within the conidiophores (Hashioka and Nakai), and possibly within
the cleistothecia (of E. necator (syn. Uncinula necator) (Kiss 1997).
Other products
Paraffin oil and other oils act as a protectants (Phillip et al. 1990, McGrath
and Shishkoff 2000).
Detergents act as protectants and fungicides (Cohen et al. 1996).
Plant extracts of Reynoutria sachalinensis (Mildana) and compost extracts
have also been shown to induce host resistance (Daayf et al. 1995, Samerski
and Weltzien 1988).
Other inorganic products include potassium bicarbonate, baking soda, soluble
silicon, and clay (Belanger et al. 2000).
Future Prospects
A number of additional fungi are also parasitic on powdery mildew and show potential
for augmentative biological control, these include: including Verticillium
leanii, Cladosporium spp., Acremonium alternatum, Tilletiopsis spp.,
Pseudozyma rugulosa, and P. flocculosa (Sporodex). The arthropod
Orthotydeus lambi is also parasitic.
CASFS Notes:
In an interview, Jim Leap (CASFS Farm Manager, 2003) commented that in a bad
year, a 50% yield may be lost to powdery mildew. Furthermore, he mentioned that
late August fogs and late plantings (after June 1st ) noticeably worsen the
infection.
Literature cited
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features on development of Erysiphe graminis and Erysiphe pisi. Pages 255-266
in: Plant Cuticles-An Integrated Functional Approach. G. Kersteins, ed. BIOS
Scientific Publishers, Oxford.
Cohen, R., Shtienbert, D., and Edelstein, M. 1996. Suppression of powdery mildew
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