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ALTERNARIA PANAX CONIDIAL CONCENTRATIONS
AND EVALUATION OF
TOM-CAST FOR MANAGEMENT OF ALTERNARIA BLIGHT
ON AMERICAN GINSENG

presented by

SHAUNTA NICHELLE HILL

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EPIDEMIOLOGY OF ALTERNARIA PANAX ON AMERICAN GINSENG AND
EVALUATION OF A DISEASE FORECASTER

By

Shaunta Nichelle Hill

A DISSERTATION

Submitted to
Michigan State University
in partial fulfillment of the requirements
for the degree of

DOCTOR OF PHILOSOPHY

Plant Pathology

2009

ABSTRACT

EPIDEMIOLOGY OF ALTERNARIA PANAX ON AMERICAN GINSENG AND
EVALUATION OF A DISEASE FORECASTER

By

Shaunta Nichelle Hill

Alternaria panax Whetzel, an annual problem for ginseng growers, incites
blighting of the foliage and drupes of cultivated American ginseng (Panax quinquefolium
Linnaeus). An epidemiological study investigated the influence of air temperature,
duration of leaf wetness, rain, and relative humidity on atmospheric conidial
concentrations of A. panax. Commercial ginseng gardens were monitored in central
Wisconsin from mid-May to September for four growing seasons. Hourly concentrations
of airborne A. panax conidia were enumerated using a Burkard volumetric spore sampler.
Fungicides were not applied. Numbers of infected plants were assessed in predetermined
portions of the ginseng garden. Disease pressure in the plots was severe, and significant
concentrations of A. panax conidia were detected in the atmosphere from late May
through September yearly. Conidial concentrations were greatest following rain events
and periods of decreasing relative humidity.

Disease forecasting systems are developed based on weather variables in
conjunction with the epidemiology of the pathogen. TOM-CAST, originally developed
to predict leaf blight caused by A. solani on tomato, was evaluated for management of A.

panax in commercial gardens. For three years, fungicide sprays initiated by TOM-CAST

(using 10 and 15 disease severity value thresholds) were compared with sprays applied at
7- and 10-day intervals. Three fungicide programs were evaluated, and included
chlorothalonil alone or in alternation with pyraclostrobin, and pyraclostrobin alternated
with copper hydroxide. Although select TOM-CAST treatment programs were
comparable to the 7-day schedule in limiting foliar disease, only the 7-day applications

adequately protected seed yield and quality.

ACKNOWLEDGEMENTS

I would like to express my gratitude and appreciation to Dr. Mary Hausbeck, my
major professor. I am grateful for the professional and academic guidance and
encouragement. To my committee members, Drs. Ray Hammerschmidt, Annemiek
Schilder and Larry Olsen, thank you for the support, advice and critical analysis of my
work.

A special thank you to Blair Harlan, Dan Rief, and Sheila Linderman for their
technical assistance in the field and laboratory. I appreciate all the assistance and
friendship provided by the following individuals: Priscilla Clark, Abigail Morris,
Meaghan Callahan, and Dr. Catarina Saude.

I wish to express gratitude to members of the Ginseng Board of Wisconsin, and
Wisconsin Ginseng Growers Association. Without their encouragement, assistance and
donation of samples, this research would not have been possible.

Finally to my family and friends thank you for your continued support throughout

my academic journey.

iv

TABLE OF CONTENTS

LIST OF TABLES ..................................................................................................... vi
LIST OF FIGURES ................................................................................................... vii
LITERATURE REVIEW .......................................................................................... 1
American ginseng (Panax quinquefolium) ................................................................ 2
Alternaria panax ........................................................................................................ 8
Disease Management for Alternaria panax ............................................................... 12
Disease Forecasting ................................................................................................... 14
Research Priorities ..................................................................................................... 17
Literature Cited .......................................................................................................... 18
CHAPTER ONE ........................................................................................................ 24
Abstract ...................................................................................................................... 25
Introduction ................................................................................................................ 26
Materials and Methods ............................................................................................... 28
Results ........................................................................................................................ 32
Discussion .................................................................................................................. 43
Literature Cited .......................................................................................................... 46
CHAPTER TWO ....................................................................................................... 49
Abstract ...................................................................................................................... 51
Introduction ................................................................................................................ 52
Materials and Methods ............................................................................................... 54
Results ........................................................................................................................ 58
Discussion .................................................................................................................. 65
Literature Cited .......................................................................................................... 68
PROPOSAL FOR FUTURE RESEARCH ................................................................ 71
Literature Cited .......................................................................................................... 74

LIST OF TABLES

CHAPTER ONE: Factors influencing atmospheric conidial concentrations of Altemaria
panax in cultivated American ginseng gardens

Table 1. Atmospheric monitoring dates for Altemaria blight caused by
Altemaria panax in commercial Wisconsin ginseng gardens 2005
through 2007 ........................................................................................................ 35

Table 2. Pearson correlation coefficients testing the relationship between hourly
conidial concentration, rainfall, leaf wetness, relative humidity and temperature in
commercial Wisconsin ginseng gardens from 2005 through 2007 ...................... 36

CHAPTER TWO: Evaluation of TOM-CAST in timing fungicide sprays for management
of Altemaria blight on American ginseng

Table 1. Effect of fungicide programs and application schedules on the number
of infected plants and the area under disease progress curve (AUDPC) values

for management of Altemaria panax on ginseng during the 2005 to 2007
growing seasons. .................................................................................................. 60

Table 2. Effects of fungicide programs and application schedule in management
of Altemaria panax on drupe and seed weight in 2007 ...................................... 61

Table 3. Effect of fungicide programs and application schedules on recovery of
Altemaria spp. from drupe, seed coat and endosperm tissues in 2007 ................ 62

vi

LIST OF FIGURES

LITERATURE REVIEW:

Figure 1. American ginseng cultivated on raised beds (A) under a wood (B) and
shade cloth (C and D) canopies. (Images are presented in color.) ...................... 4

Figure 2. Altemaria blight lesions caused by Altemaria panax on American ginseng
stem (A), drupes (B and C), progression foliar infection (D — F and observation of
foliar lesions in contact with straw mulch (G). (Images are presented in color.)
.............................................................................................................................. 9

CHAPTER ONE: Factors influencing atmospheric conidial concentrations of Altemaria
panax in cultivated American ginseng gardens

Figure 1. Spore trap equipment and conidia of Altemaria panax. (Images are
presented in color.) .............................................................................................. 31

Figure 2. Hourly average concentration of airborne conidia of Altemaria panax in
Wisconsin ginseng gardens from 2005 to 2007 ................................................... 37

Figure 3. Atmospheric Altemaria panax conidial concentrations occurring in
commercial Wisconsin ginseng gardens during the 2005 — 2007 growing seasons for
3- yr crops (A and B-2005) and 4-yr crops (B-2006) and (C) and occurrence of 85%
(V) and 100% (V) crop defoliation. Shaded bars represent weeks where spore traps
malfunctioned ...................................................................................................... 38

Figure 4. Association of daily atmospheric Altemaria panax conidial concentrations,
temperature, relative humidity and rainfall in a ginseng garden ......................... 40

Figure 5. Relationship between atmospheric conidia of Altemaria panax and relative
humidity averaged from 2005 - 2007 ................................................................... 41

Figure 6. Disease progression resulting from infection by Altemaria panax in
Wisconsin ginseng gardens during the 2005 - 2007 growing seasons ................. 42

vii

LIST OF FIGURES

CHAPTER TWO: Evaluation of TOM-CAST in timing fungicide sprays for management
of Altemaria blight on American ginseng

Figure 1. Disease progress curves for Altemaria panax infection of 4-year-old
ginseng plants not treated or treated with the fungicide chlorothalonil (0.68 kg
a.i.fha), chlorothalonil (0.68 kg a.i./ha) alternated with pyraclostrobin (0.07 kg
a.i./ha), or copper hydroxide (0.73 kg a.i./ha) alternated with pyraclostrobin
(0.07 kg a.i./ha). Fungicide programs were scheduled during the 2006 growing
season every, A, 7 days, B, 10 days, or according to the TOM-CAST disease
forecaster using, C, 10 DSV or D, 15 DSV. F ungicide programs were scheduled
during the 2007 growing season every, E, 7 days, F, 10 days, or according to the
TOM-CAST disease forecaster using, G, 10 DSV or H, 15 DSV ....................... 63

viii

LITERATURE REVIEW

American ginseng (Panax quinquefolium)

Ginseng is a member of the family Araliaceae and placed in the genera Panax.
Of the several species included in the Panax genus, Oriental ginseng (Panax ginseng,
Meyer) and North American ginseng (Panax quinquefolium, Linnaeus) are most
important for trade. Oriental ginseng refers to plants native to North Korea and China,
while American ginseng is native to Canada and the eastern half of the United States. In
the Midwest, the cultivation season for ginseng is late April through late October (25, 47,
48).

Ginseng is an erect perennial plant with a canopy that can reach 30 to 40 cm in
height (49). The canopy of a mature ginseng plant consists of three or four compound
leaves arranged in a whorl. Each leaf contains five ovate, saw-toothed leaflets with the
upper three leaflets being larger than the lower two. An immature plant has one or two
leaves and adds an additional leaf every year until maturity. Generally, first year
seedlings have one leaf with three leaflets.

Ginseng has a single umbelliferous inflorescence that forms at the terminus of the
stem (54). The umbel has <50 small, white, perfect flowers (54) that are self—fertile.
Each flower is capable of producing a green kidney-shaped drupe after fertilization. The
drupes ripen and turn crimson red in late summer (48). Each drupe contains two seeds
that are approximately 0.5 cm in diameter and slightly longer than they are wide.
Stratification of the seed is required and is generally 18 to 22 months in duration (18, 50).
During stratification, the endocarp of the seed remains tightly closed, opening slightly

along its suture a month or so before germination (54). The series of warm and cold

temperatures over the 18- to 22- month stratification period is necessary for the embryo
to grow and mature (24, 51, 54).

Ginseng has a fibrous taproot (2). The outer skin of the root is generally light to
golden brown and the interior is white to light yellow in color. The root is fleshy and
wrinkled with a rhizome at the crown. It is on this rhizome that the bud for the next
year’s shoot develops during the spring with the bud expanding so that the stem, rather
than the leaves, is seen first (54). During the winter months the bud is dormant (24).
Root age can be determined by counting the rings (scars from winter dormancy and
annual abscission of the foliage) on the crown of the root. Root length at maturity can

range from 7 to 13 cm (2).

Cultivation and range for American ginseng

American ginseng is an understory plant, requiring only 30% of full sunlight (49),
and grows within USDA plant hardiness zones 3 to 9. In northeastern North America, it
is most often found growing under sugar maple while in the Southeast it is often found
under tulip poplar or black walnut. In the Midwest it occurs beneath several different
hardwood species including oak (3).

Ginseng can be grown as a woods- or field-cultivated crop (Figure 1). Woods-
cultivated ginseng is grown in a hardwood forest with the area cleared to remove existing
understory plants and leaf litter that would naturally compete with or hinder ginseng
growth. Cultivated ginseng is grown under woven panels providing 80% shade that are
suspended via 2.4- to 3.0- m posts in a cleared field. Under both canopy types, ginseng is

sown into plant beds that are generally 1.5 m wide and 2.7- to 3.7- m high (26). Each

cultivation method requires intensive maintenance including mulch such as straw or hay,

weeding, and ftmgicide use.

 

Figure 1. American ginseng cultivated on raised beds (A) under a wood (B) and
shade cloth (C and D) canopies. (Images are presented in color).

Ginseng grows best in loamy, light textured, well-drained soil with a pH of 5.5 to
6.5 (48). The crop also requires 0.5 to 1.52 m of precipitation annually and a minimum
cold period (<9° C) of sixty days to break dormancy each spring (48). Following seed
planting, 15 cm of straw mulch is generally applied to ginseng beds. In winter, straw
mulch can prevent temperatures from dropping below the freezing point for roots (around
-10° C) and in summer keeps soil temperatures 5 to 10° C below that of an open grassed
area (61). Mulch also eliminates the need for irrigation as it prevents excessive moisture
loss from the soil throughout the season (61). In addition to straw, ginseng growers may
use saw dust as mulch (26).

American ginseng has been cultivated in Wisconsin for more than 100 years.
Currently, more than 95% of the cultivated commercial ginseng in the US. is grown in
Wisconsin (1). Canada is also a significant producer of ginseng with approximately
8,000 acres grown in Alberta, British Columbia, and Ontario (2). Several states including
West Virginia (62), North Carolina (18), New York (22), Washington (11), and Oregon
(55) have small but thriving ginseng industries. Production for each of these areas is
primarily under shade cloth. Most of Michigan’s ginseng production is located in the
Upper Peninsula. Michigan has approximately 135 acres of woods-grown ginseng and

15 acres of field-cultivated ginseng (25).

Cultivation costs and profits
Cultivation of ginseng requires that growers make a large initial investment in
mechanized equipment, shade materials, land, labor and crop stock (44). Approximate

input costs for a new half-acre woods-cultivated garden is $24,135 (44). Approximate

input costs for a new half-acre garden under shade cloth is $33,500 including seed and
labor costs (44). Field cultivated ginseng is currently valued at $20/lb (26). Current
prices for woods-cultivated ginseng range between $80 and $320/1b. In addition to root
profits, ginseng seeds are also a source of revenue for ginseng growers. Current market
prices for stratified seed are $55/lb. With an average seed yield of 336 kg/ha, each ha

represents a value of $18,537 (26).

Pathogens affecting ginseng

Ginseng is susceptible to a number of pathogens that can cause foliar blights and
root rots. Some of the most devastating foliar pathogens include Altemaria panax
(Whetzel) and Botrytis cinerea (Pers: Fr.). Important root rot pathogens include
F usarium spp. (Booth), Cylindrocarpon destructans (Zinssmeister) Scholten, and
Phytophthora cactorum (Leb. et Cohn) Schroet (26). American ginseng seeds are also
susceptible to pathogens. Commercial seeds from Wisconsin and Canada have been
found to be contaminated with spores of Altemaria, Cylindrocarpon, Phytophthora, and
F usarium spp. (27, 28), all of which are capable of reducing plant stands. Mucor and
T richoderma spp. have also been recovered from stratified ginseng seeds in the US (67).

P. cactorum is favored by cool and wet weather (16, 19, 48, 53). Infected roots
develop a brown discoloration (5) and a loss of turgidity gives the tissue a spongy texture.
Foliar infections of P. cactorum may also occur and result in dark green, water-soaked
lesions on the leaves (19). Disease can progress rapidly down the main stem (21, 24),
resulting in plant collapse and death (25). If not controlled, this pathogen may destroy an

entire ginseng garden in just a few weeks (2, 16, 25).

Rusty root of ginseng is a complex of pathogens and includes Cylindrocarpon
destructans, Rhexocercosporidium panacis sp. nov (Reeleder) and F usarium spp. C.
destructans can cause damping-off, crown and root rot of ginseng (26, 59). Infection
normally starts near the root tip, progressing upward, and often destroying the entire root.
A classic symptom of C. destructans root rot is “disappearing root,” whereby the root
tissue disintegrates due to rot. Another symptom of C. destructans rot is a reddish to dark
brown canker on the root. These cankers are often dry and cracked (29). R. panacis
lesions are superficial, but the outer layer of root tissue ruptures and sloughs off, giving
roots a scabbed appearance (59). Infection by F usarium spp. can cause stem and crown
infections, although root rots are most common, resulting in red streaking of the tissue.
When F usarium root rot is advanced, the foliage wilts and becomes reddened.

Botrytis cinerea is extremely common and can survive on virtually any dead plant
material found in a ginseng garden (10). Traditionally, ginseng growers considered B.
cinere'a a pathogen of flowers and fruits only, resulting in reduced seed yields (26).
Frequently, berries will not develop if the flower has been infected. Green berries turn
brown after infection and a gray fitzzy mold may appear on mature or immature berries.

Typical foliar symptoms include water-soaked, tan lesions that often have
concentric rings, giving them the appearance of a bull’s eye. Lesions often start at the
leaf tips and proceed back along the leaf midrib (11, 25). B. cinerea can infect stems late
in the growing season and may form small sclerotia on afi‘ected tissues that allow the

fungus to overwinter (26).

Altemaria panax

The most common foliar disease of ginseng is Altemaria blight incited by
Altemaria panax Whetzel (43). This disease is a yearly problem for ginseng growers in
Wisconsin (43) and Michigan (26). Altemaria blight also occurs in other ginseng-
growing regions including Alberta, Canada (13,14), West Virginia (62), North Carolina
(19), Oregon and Washington (55).

Typical foliar symptoms include necrotic lesions with dark brown margins and
yellow-green halos (43). Brown lesions often develop on the stem just above the soil line
and cause girdling (9). Infected drupes may develop a water-soaked appearance followed
by the development of gray mycelium and pathogen sporulation. Infection of the root by
A. panax is rare (43); however, root weight can be reduced when blighting of the leaves

and stem causes premature defoliation.

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Altemaria infections are especially devastating under favorable environmental
conditions with blight development and conidial production occurring within 5 to7 days
(64). If not managed, Altemaria blight can reach epidemic proportions within a month
after plant emergence and destroy all of the foliage. Young plantings are especially
susceptible to infection and entire gardens can be destroyed. For maturing crops, loss of
foliage and repeated outbreaks in consecutive years could result in reduced root yields
(9). Wisconsin growers have experienced yield loss 75 to 100% when Altemaria blight is
uncontrolled (20).

A. panax historically was known to only infect members of the Araliaceae,
specifically ginseng (15, 56), however infections of the Umbrella Tree (Schefllera
actinophylla, and False Aralia (Schefilera elegantissima) have been reported in Hawaii
(64). On ginseng, Altemaria blight is characterized by target spot lesions with dark
brown margins and yellow halos. As the disease progresses, a dark mat of conidia
develops within the lesions. Stem infection results in the production of elongated,
reddish to dark brown lesions (9, 56). The potential for repeated, widespread and
devastating epidemics is great because large numbers of conidia are produced on the
surface of diseased leaves and stems. Outbreaks of A. panax in one season may greatly
increase the potential for epidemics in subsequent seasons, since the fimgus overwinters
(26). A. panax can survive as conidia or as mycelium in infected plant residue, on straw
mulch or in and on seeds (26, 34).

In the spring, overwintered conidia can spread to the newly emerging healthy
plants by rain or splashing water and begin the disease cycle for the new growing season

(26). In addition, overwintering conidia can be a source of stem infection as plants

10

emerge through the infested mulch in the spring (26). Currently, there are no practical
methods to reduce overwintering inoculum levels on the mulch or on infected crop
residue.

A. panax is noted to have a wide range of conidial morphology (15). Conidia are
obclavate, and typically 150 to 160 by 12 to 20 pm (9) with 1 to 2 vertical and 9 to 11
transverse septa (52). A. panax conidia germinate within 1 to 2 h of contact with host
tissue with 70% relative humidity (57) by producing several germ tubes. The formation
of bulbous appressoria on the end of germ tubes was found to occur 6 h after conidial-
host tissue contact (57). Conidia may penetrate through the leaf surface either over
epidermal cells or at sites of cell junctions and indirectly through stomatal openings (5 7).
Conidiophores are geniculate (9).

Conidia are introduced into gardens via air currents, resulting in spread of A.
panax from a diseased garden to nearby healthy gardens. Altemaria can also be moved
into gardens on equipment (23). High humidity and warm weather can influence disease
severity and under favorable conditions, blight development and conidial production can
occur in 5 to 7 days (64). Optimtun conidial production occurs with temperatures
ranging from 18 to 25° C (9, 64). Optimum mycelial growth occurs at 24 to 27° C (15,
17).

Many Altemaria spp. produce host-selective toxins that diffuse ahead of the
fungus. These toxins are usually associated with the yellow halo that fades into the
healthy tissue surrounding the lesion (34). When an A. panax isolate recovered from an
Ontario ginseng garden was used to inoculate various hosts (members of Cruciferae,

F abaceae, Solanaceae, Graminae and Araliaceae); water-soaked, chlorotic lesions

11

followed by necrosis were only produced within Araliaceae, and only on ginseng (56).
Analysis of the germination fluid showed that it contained a phytotoxic, 35- kDa
monomer (56, 57). This monomer, named AP-toxin, was later shown to be produced by
several Altemaria isolates from Ontario, British Columbia and Wisconsin (57).

The production of the AP-toxin by A. panax, (like Deoxyradicin produced by A.
helianthi and AB-toxin produced by A. brassicicola and A. brassicae) is likely induced
by host-related factors during the early host-pathogen interactions (40, 56). Despite the
germination of conidia and detection of germination fluid on other hosts, AP-toxin is only
produced by A. panax on ginseng. Temperature can affect the activity of the AP-toxin.
If the toxin is held at 45° C for 15 minutes, activity is significantly reduced and is
inactivated at 80° C. The toxin activity at 4, 22, 30 and 37° C was similar, and when
tested for activity at the respective temperatures, lesions diameters ranged between 15

and 20 mm (56).

Disease Management of Altemaria

Altemaria blight is currently managed through cultural methods and fungicide
use. Cultural practices such as avoiding dense plantings and garden sites with poor air
circulation may help limit disease. The destruction and removal of infected plant debris
and the replacement of straw mulch is also recommended to reduce subsequent epidemics
(19). Unfortunately, these strategies are not practical and would not preclude the
reintroduction of inoculum via air currents.

In the interest of adapting Integrated Pest Management (1PM) strategies for
managing pests on ginseng, previous researchers have investigated use of biocontrols as

alternatives to traditional fungicides. Burkholderia cepacia AMMD (Pseudomonas

12

cepacia strain AMMD) was found to effectively inhibit Altemaria leaf and stem blight
under growth chamber conditions. However, the agent was not adequate in reducing
disease under field conditions due to poor survival on leaf surfaces (32, 41, 42).

When disease pressure is high, fungicides are necessary to maintain plant health.
Crop protection can be difficult as plants emerge through infested mulch. It has been
estimated that Altemaria blight would infect 80 to 100% of ginseng plants without
effective chemical control (42). Currently, azoxystrobin and pyraclostrobin are relied
upon in disease management programs (25, 26). Azoxystrobin is classified by the
Environmental Protection Agency as reduced-risk chemistry. Reduced-risk products
have a low impact on human health, low toxicity to non target organisms (birds, fish, and
plants), low potential for groundwater contamination, lower use rates, low pest resistance
potential, and compatibility with 1PM (65). These Quinone outside Inhibitors (QoI)
fungicides function by inhibiting fungal respiration. Mobility differs for the two
fungicides as azoxystrobin is xylem mobile, while pyraclostrobin is locally systemic.

There is a high resistance risk for strobilurin fungicides, and so they must be used
in alternation with protectant fungicides (i.e., mancozeb and chlorothalonil) to delay the
development of pathogen resistance (25). Chlorothalonil and mancozeb have been
available to Wisconsin and Michigan ginseng growers through yearly Section 18
Emergency Exemption labels. Mancozeb is a broad-spectrum dithio-carbamate,
ftmgicide. Chlorothalonil is a broad-spectrum organochlorine.

Iprodione, a dicarboximide, was very effective in controlling Altemaria on
ginseng. However in mid season of 1987, after applications of iprodione in an

experimental plot for two consecutive seasons, the fungicide was found to be ineffective

13

against A. panax (58). Laboratory tests (5 8) confirmed the existence of an Altemaria
population which had become resistant to iprodione. Other Altemaria spp. with
documented dicarboximide resistance include A. alternata pv. citri (63), A. alternata (30,
37), and A. brassicicola (31). Although iprodione has been used for many years to
control various fungal pathogens causing plant diseases, the mode of action and the
resistance mechanisms are not well known (35).

Resistance of A. panax to iprodione has not been documented since the first
report. Few growers now use the product because of its expense, although recent studies
have indicated that it is effective in controlling Altemaria blight (25). In 1988, copper
hydroxide (inorganic chemistry) was available for a tank mix with iprodione; however,
the mixture was found inadequate for disease control throughout the growing season, and

the combination appeared to reduce the seed yield of treated plants (25).

Disease Forecasting

Since the mid 19003, the concept of predicting disease occurrence has been
explored (66). Disease predictive or forecasting systems are developed based on weather
variables (66), in conjunction with the biology and epidemiology of the pathogen to
predict infection or development periods for the disease on a particular host (33).

The benefits of utilizing disease forecasting systems are numerous. Primarily,
forecasting systems are useful for economically important diseases, especially those
which are variable between seasons and known to depend on specific weather factors (8).
Secondly, disease forecasting systems are suited for 1PM programs, as the timing of
fungicide applications are tailored, which minimizes environmental, human and animal

hazards. Forecasting systems also have a potential cost benefit to farmers who typically

14

apply ftmgicides based on a calendar program (usually every 7 to 14 days). By using a
forecasting system to account for disease potential and environmental factors, farmers
could reduce the total number of fungicide applications per season and lessen the chances
for pathogens to develop ftmgicide resistance (4, 7, 8, 60).

In 1978, a disease forecasting system was developed to identify environmental
conditions that would favor development of early blight on tomatoes and to enhance the
efficiency of fungicide use (3 6). The forecasting system FAST (Forecaster of Altemaria
solani on Tomato), uses disease severity values (DSVs) based on hours of leaf wetness
and mean temperature during leaf wetness to determine the first fungicide application.
Subsequent fungicide applications are then made based on daily values of leaf wetness,
mean air temperatures, rainfall and hours of relative humidity > 90% (36). Field studies
showed that the weather-prompted FAST program was as effective as calendar-based
fungicide applications (3 6).

The FAST system was modified by Pitblado in 1988 (45). The resulting system
TOM-CAST (Tomato disease forecasting), is a computer system that calculates DSVs
based on hours of leaf wetness and temperature. Sprays are based on cumulative DSV
thresholds. When a threshold is reached, a fimgicide is applied and the DSVs reset to
zero (46). TOM-CAST has been successfully implemented to manage early blight on
tomatoes (12, 46), purple spot on asparagus (3 8), foliar blights on carrots (7), and studies
have shown it to be useful on parsley (39) and celery (6).

Considering the crops where TOM-CAST based fungicide applications were
found to be a practical and economical alternative to calendar-based applications, ginseng

is most similar to celery. Like ginseng, celery is a high-value crop. In Michigan, the

15

value for processing and fresh market celery is $20,431/ha compared to $3,424 and
$2,420 for carrot and asparagus, respectively (6). Late blight incited by Septoria apiicola
must be managed as the marketable portion of the celery is affected and consumers
demand a blemish-free product (6). In comparing TOM-CAST with other disease
predictors, a lO-DSV program was found to provide control equivalent to traditional 7-
day applications (6).

TOM-CAST has been commercially implemented in Michigan for carrot (7) and
asparagus (3 8). Carrots, unlike celery, are able to tolerate specific levels of disease as the
marketed portion of the crop is not infected. Yield loss resulting from leaf blight occurs
when infected carrot petioles snap during mechanical harvest, leaving the roots in the
ground (7). Also, the pathogens causing late blight of carrot, Altemaria dauci and
Cercospora carotae, do not defoliate the crop in a relatively short time frame as A. panax
does with ginseng. Purple spot of asparagus, caused by Stemphylium vesicarium, can
result in premature browning and defoliation of the photosynthetic tissue. Since 2000,
TOM-CAST has been used to manage purple spot on the fern after spears have been
harvested. Following infection of the fern, there is decreased carbohydrate availability to
the crown which negatively impacts spear production. Asparagus, like ginseng is a
perennial crop. When foliar disease is not controlled on asparagus over consecutive
years, subsequent reductions in spear yields may result (38). There is a similar concern
for ginseng, as repeated epidemics of Altemaria blight can result in reduced root and seed
yields (26). For both asparagus and carrots, TOM-CAST with a 15-DSV threshold was

found to provide adequate disease control.

16

Research Priorities

Under current practices, ginseng growers apply fungicides for crop protection
from mid-May to early June until the middle of September (26). This is a concern as the
current chemical controls registered for Altemaria blight have limited seasonal
application allowances to reduce pathogen resistance potential. The products also should
not be applied sequentially.

Given the yearly potential crop losses resulting from Altemaria blight, ginseng
growers are interested in improving disease management in a cost-effective manner.
Specifically, growers are interested in learning (i) when is A. panax inoculum available,
(ii) when should control measures be initiated each season, (iii) what weather factors
influence conidial concentrations, and (iv) can TOM-CAST be used to prompt fungicide
sprays? In an effort to retain effective products, a reduction in seasonal fungicide
applications is sought based on inoculum detection and environmental factors. In hopes
of addressing these concerns, research utilizing current management tools were tested.

This paper details the summary of the results.

17

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23

CHAPTER ONE
Factors influencing atmospheric conidial concentrations of

Altemaria panax in cultivated American ginseng gardens

24

ABSTRACT

Factors influencing atmospheric conidial concentrations of Altemaria panax in cultivated
American ginseng gardens.

Leaf blight, caused by Altemaria panax, is the most common disease of cultivated
ginseng and is an annual threat. To determine the influence of weather parameters on
atmospheric conidial concentrations, 3- and 4-year-old commercial American ginseng
(Panax quinquefolium L.) gardens were monitored from mid-May to September for three
growing seasons. Hourly concentrations of airborne A. panax conidia were enumerated
using a Burkard volumetric spore sampler. The hourly averages of air temperature,
rainfall, and relative humidity were also collected. Fungicides were not applied. The
incidence of leaf blight was assessed in predetermined portions of each garden. In each
year, atmospheric conidial concentrations of A. panax were detected beginning in late
May and continued through the growing season. Daily conidial concentrations followed
a diurnal pattern and were greatest during periods of rapidly decreasing relative humidity.
A significant correlation was observed between hourly conidial concentrations and
temperatures greater than 18°C. Moisture negatively impacted hourly conidial
concentrations. Disease pressure fi'om A. panax was high each year and many plants

were dead by the end of the growing season.

25

INTRODUCTION

American ginseng (Panax quinquefolium L.) is a perennial herb grown primarily
for the medicinal properties of its root (23). Currently, more than 95% of the cultivated
commercial ginseng in the United States is grown in Wisconsin (1) with a revenue
totaling $50 to $75 million annually (12). Cultivated ginseng is grown on a raised plant
bed under a natural tree or artificial black woven polypropylene canopy (23). The shade
required by the crop and the dense plant spacing create a microclimate with limited air
movement and extended leaf wetness periods. The annual growing season for ginseng
occurs over 5 to 6 months with plant emergence beginning in mid to late April.

Altemaria blight incited by Altemaria panax Whetzel is the most common
disease of ginseng throughout the world (22). This disease is a yearly problem for
ginseng growers in Wisconsin and can be especially destructive, causing rapid defoliation
and plant death (11, 12, 13, 22). Altemaria blight also occurs in other ginseng-growing
regions including Alberta, Canada (3, 4), West Virginia (30), North Carolina (7),
Michigan (11, 12), Oregon and Washington (25).

Typical Altemaria blight symptoms include necrotic lesions on the foliage with
dark brown margins and yellow-green halos (22). Brown lesions often develop on the
stem just above the soil line and cause girdling (2). Infected drupes may develop a water-
soaked appearance followed by the development of gray mycelium and pathogen
sporulation (11, 12). Infection of the root by A. panax is rare (22); however, root weight
can be reduced when blighting of the leaves and stem causes premature defoliation (2).

A. panax conidia are produced in short chains of 2 to 3, but are more commonly

borne singly (2, 33). Although the morphology of A. panax conidia is variable (5),

26

conidia are typically obclavate, 150 to 160 by 12 to 20 um (2) with 1 to 2 vertical and 9
to 11 transverse septa (24). A. panax can survive as conidia or as mycelium in infected
plant residue, or in and on seeds (17). Lesion development and conidial production can
occur in 5 to 7 days under favorable conditions (3 3). Optimum conidial production and
mycelial growth occurs with temperatures ranging from 18 to 25° C and 24 and 27° C,
respectively (2, 5, 6, 33). Specific leaf wetness parameters for A. panax are unknown.

A. panax conidia may overwinter in mulch and crop debris providing initial inoculum
for emerging crops in the spring (12). Fifteen cm of straw mulch is generally applied to
ginseng beds during crop establishment. In the winter, straw mulch can prevent
temperatures from dropping below the freezing point of the roots (around -10° C) and
during the summer keeps soil temperatures 5 to 10° C below that of an open-grassed area
(29). Mulch also eliminates the need of irrigation as it prevents excessive moisture loss
from the soil throughout the season (29). Despite these benefits, the use of straw mulch
can also be problematic as A. panax mycelium can spread from plant to plant through the
mulch; the pathogen may also spread through the soil as a saprophyte until it contacts the
ginseng host (11, 15, 17).

In the absence of effective treatments for Altemaria blight, growers could
potentially lose $13,930/ha (current market price for ginseng root) (12). Since A. panax
also infect drupes, seed can also be threatened. With an average seed yield of 363
kg/hectare, growers could lose an additional $18,537/ha (current market value $55/lb)
due to Altemaria blight (12).

Cultural strategies to manage Altemaria blight include increasing plant spacing to
enhance air circulation, removing infected foliage and replacing straw mulch in affected

areas (7). Unfortunately, these strategies are not practical and would not preclude the

27

reintroduction of inoculum via air currents. The use of biocontrols as alternatives to
traditional fungicides has also been considered for Altemaria blight management.
Burkholderia cepacia AMMD (Pseudomonas cepacia strain AMMD) was found to
effectively inhibit Altemaria blight under growth chamber conditions. However, the
biocontrol agent did not adequately reduce disease under field conditions due to poor
survival on leaf surfaces (16, 20, 21).

Currently, growers rely on fungicides to protect their crOp from Altemaria blight
(11). Growers must apply fungicide sprays judiciously during the relatively long
growing season of May through September to protect the crop and comply with the
labeled seasonal application limits. To support the development of new management
strategies that are less dependent on fungicides, additional epidemiological information
for A. panax is needed. Ginseng growers would like to know when fungicide
applications should be initiated in the spring and what specific weather parameters are
associated with increased atmospheric conidial concentrations (ACCs). The objectives of
this study were to determine (i) when inoculum is available each season, (ii) when control
measures need to be applied and how long they should be maintained, and (iii) what

weather factors influence conidial concentrations.

MATERIAL AND METHODS
Plot establishment. Field studies were conducted in commercial cultivated
ginseng gardens located in Marathon County, WI. Gardens were established from
stratified seed that was broadcast planted into 1.5 m-wide, raised plant beds that were 22

to 30 cm high. Ginseng seeds were not planted on the lower portion (20 cm) of the beds.

28

After seeding, the entire plant bed was covered with 15 cm of straw mulch. Each year,
woven panels providing 80% shade were suspended via 2- to 3-m posts over the plant
beds to mimic wood-lot conditions. Weeds were hand pulled. Each year, plant
emergence began in March and plants were fully emerged by May 1.

Disease incidence. Garden sections for monitoring disease incidence were
identified prior to the start of spore trapping. The number of plants with one or more
lesions was determined in four 1.5 x 3-m sections located in the eastern half of each
garden. Fungicides were applied according to commercial standards to the areas
surrounding the monitored garden sections only. A 24-ft untreated buffer was maintained
between the monitored garden sections (untreated) and remaining commercial garden
treated according to industry practices.

Inoculum availability and atmospheric concentrations. Concentrations of
airborne A. panax conidia were monitored each growing season from 2005 to 2007 using
a 7-day volumetric spore sampler (Burkard Scientific, Uxbridge, UK) (Figure 1).
Monitoring began in either May or June (prior to the development of Altemaria blight
symptoms) and concluded in August or September (Table 1). Spore traps were located
on the eastern half of each garden, within the disease incidence monitoring area. Spore
traps were operated at a flow rate of 10 liters/min and the orifice was free to move with
changing wind direction. Conidia were collected on melinex tape (Burkard Scientific,
Uxbridge, UK) coated with an adhesive mixture of petroleum jelly and paraffin (9:1,
wt/wt) heated to 60° C and cooled overnight before being dissolved with sufficient
toluene to give a thick, liquid consistency. Prior to petroleum jelly and paraffin coating,

the melinex tapes were coated with a polyvinol alcohol (Airvol/Gelvatol, grade 603,

29

Burkard Scientific, Uxbridge, UK) and phenol mixture (35 g polyvinol alcohol, 25 ml
glycerol, 50 ml distilled water, heated to 40° C to combine, then cooled to 23° C before
adding 2 g of phenol) and allowed to dry overnight at 23° C. Prepared tapes were
maintained at 23° C until field use.

Tapes were removed from the spore trap weekly and cut into 48-mm lengths and
scored at 2-mm intervals corresponding to a 24 h day using a razor blade. Tape sections
were mounted onto 3x2 cm glass slides and stained with aniline blue (0.14 mg aniline
blue, 20 ml distilled water, 15 ml glycerol, 10 ml of 85% lactic acid). Slides were
covered with 22x50 mm coverslips and sealed using Cytoseal (Richard-Allan Scientific,
Kalamazoo, MI). Mounted slides were allowed to dry at 23° C for at least 24-h before
observation by light microscopy.

Hourly conidial counts were made using a compound light microscope. A. panax
was identified based on morphological characters (2, 24). Occasionally, conidia of A.
alternata (conidium 20-63 pm) and A. solani (conidia 150-300 um) (27) were observed
but were not included in hourly conidia counts. Hourly conidial counts were converted to
numbers of conidia per cubic meter of air sampled per hour (conversion factor= x/ 0.6).
PROC CORR (SAS Institute Inc., Cary, NC) was used to determine correlations among
hourly atmospheric conidial concentrations, rainfall, leaf wetness, relative humidity and
temperature for each growing season (10).

Weather monitoring. Hourly measurements of air temperature and relative
humidity were recorded using a data recorder (Watchdog series 450, Spectrum
Technologies, Inc., Plainfield, IL). An unpainted Watchdog leaf wetness sensor

(Spectrum Technologies, Inc.) was placed at a 45° angle facing north within the upper

30

25% of the ginseng canopy. Data were downloaded weekly to a laptop computer using a
computer program (Specware 6.01 and 7.01; Spectrum Technologies, Inc.). The program
was set to record temperatures between 0° and 100° C. Rainfall was measured hourly

using a tipping-bucket rain collector (series 3554WD, Spectrum Technologies, Inc.)

(Figure 1).

   

   

  

.\
Q

Figure 1. Burkard spore trap, tipping rain bucket (A), leaf wetness sensor and
temperature/humidity sensors (B) used to monitor weather parameters and
atmospheric concentrations of Altemaria panax conidia (C, D) within WI ginseng
gardens. (Images are presented in color.)

31

RESULTS

Conidial availability, diurnal pattern and atmospheric concentrations. Each
year, ACCs were detected at the onset of spore trapping and occurred daily throughout
the monitoring period. In 2005, ACCs during the first week of monitoring were < 1000
conidia/m3/h whereas in 2006 and 2007, the ACCs exceeded >1000 conidia/m3/h. When
hourly ACCs were averaged over the monitoring periods, peaks occurred at 1200 h in
2005 (53 conidia/m3/h), 1100 h in 2006 (233 conidia/m3/h), and 1300 h in 2007 (115
conidia/m3/h). Relatively few conidia were trapped between 0100 h and 0600 h, with an
average of 18, 49 and 29 conidia/m3/h in 2005, 2006 and 2007, respectively, (Figure 2).

When a commercial garden was monitored over two growing seasons, greater
hourly ACC totals were observed in the second year (4-year-old planting) compared with
the first year (3-year-old planting). Across all gardens monitored, the highest daily ACCs
were observed during the latter portion of each growing season (e. g. July 2005, garden B;
August 2006, gardens A, B and C) (Figure 3).

ACCs and weather effects. Weekly rainfall averaged 12.9, 9.9, 111.0, and 7.8
mm for gardens A, B (2005), B (2006) and C, respectively. Rain (%) /1eaf wetness (%)
varied across years and gardens occurring 4.2/ 15.2 (A), 3.0/21.3 (B-2005), 6.2/27.3 (B-
2006) and 3.8/24.9% (C) of the monitoring periods. Each year, hourly rainfall and leaf
wetness were negatively correlated to ACCs (Table 2). In all monitored gardens,
averages of 153112 conidia/ m3/h were detected when rain was absent. Whereas 7540
conidia m3/h (average) were present in the atmosphere during rain events. Despite a
negative correlation between hourly rainfall and ACCs; daily totals for ACCs following

rain events (1 to 3 days) were at least 50% greater than ACCs on the day of the rain event

32

(Figure 4). A positive correlation for ACCs occurring 16 h or more after a rain event was
detected (p20.05). In all gardens, the average hourly ACCs during no leaf wetness were
similar to periods without rainfall. Similar to the periods with rainfall, an average of S40
conidia on average were present in the atmosphere during hours when leaves were wet.

Within each 24-h period, ACCs peaked during periods of decreasing (20 to 80%)
relative humidity (RH) for all monitored periods (Figure 4). RH exceeding 80% was
negatively correlated to hourly ACCs for all gardens (Table 2). Hourly ACCs were
positively correlated to RH between 20 and 49%. For all monitoring years, ACCs were
greatest when RH was low (i.e. 20%) (Figure 5).

During 2005 and 2006, temperatures between 18 and 25° C were most common.
In 2007, overall temperatures were lower and were commonly within the range of 10 to
17° C (48.4 h/monitoring week). Temperatures rarely fell below 10° C, with fewer than
10 h/week on average recorded. Temperatures exceeded 25° C each year, with an
average of 19 to 24 h/week observed. The highest hourly temperature recorded in each
garden was 34.5 (A), 36.6 (B-2005), 44.4 (B-2006) and 34.0° C (C).

Temperatures of 18 to 25° C were positively correlated to hourly ACCs (Table 2).
In garden A, when hourly temperatures were predominantly between 18 and 25° C, an
average of 50 conidial/m3/h were observed. Similarly for garden C, when hourly
temperatures were predominantly between 18 and 25° C, an average of 69 conidial/m3/h
were observed. In garden B, ACCs averaged 16 and 113, in 2005 and 2006, respectively.
A significant correlation (p30.05) was also present for temperatures > 25° C. When
hourly temperatures were predominantly >25° C in each 24-h period, average hourly

ACCs were greater than 50 for all gardens except B in 2005 when the average hourly

33

ACC was 22. In garden B during 2005, the spore trap was inoperable for 3 weeks in
August.

Temperatures less than 18° C were negatively correlated with hourly ACC. When
hourly temperatures were predominantly <10° C within each 24-h period, the hourly
ACC averages were 3 25 for all gardens. When hourly temperatures were between 10°
and 17° C, average ACCs were 29 and 40 for gardens A and C, respectively. ACC
averages of 9 and 58 were collected in garden B for 2005 and 2006, respectively.

Disease incidence. For all years, disease increased throughout the growing
season resulting in significant levels of foliar blighting and death (Figure 6). The first
Altemaria blight lesions were observed on the foliage on 24 June, 20 June, and 27 June
of 2005, 2006, and 2007, respectively. A significant correlation (P=0.0048) between
weekly conidial concentrations and plant disease incidence was observed. Commonly,
high levels (85%) of crop defoliation were observed in early August (Figure 3). By the

end of the monitoring period, many of the garden sections were completely defoliated.

34

Table l. Atmospheric monitoring dates for Altemaria blight caused by
Alternariapanax in commercial Wisconsin ginseng gardens 2005 through 2007.

 

 

Year Gardenz Plant age (Year) Monitoring Period
2005 A 3 5/24 - 8/22

B 3 5/26 — 9/9*
2006 B 4 5/25 — 8/30
2007 C 4 6/1 — 9/20

 

zGarden size = 1.6 ha. * Spore trap malfunction 8/3 — 8/16 and 8/24-30

35

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36

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Figure 2. Hourly average concentration of airborne Altemaria panax conidia in
Wisconsin ginseng gardens A (91 monitoring days (md)), B-2005 (107 md), B-2006
(98 md) and 2007 (112 md).

37

Figure 3. Atmospheric Altemaria panax conidial concentrations
occurring in commercial Wisconsin ginseng gardens with 3-yr-old (A and
B-2005) and 4-yr-old plants (B-2006) and (C) and occurrence of 85% (n)
and 100% (V) crop defoliation. Black-filled bars represent weeks where
spore traps malfunctioned.

38

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bars represent the standard errors of means.

41

 

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in Wisconsin ginseng gardens during the 2005 - 2007 growing seasons.

42

DISCUSSION

Traditionally, ginseng growers apply fungicides for crop protection beginning
with plant emergence (approximately mid-May) until the middle of September (12). In
our study, A. panax conidia were detected at the onset of the growing season, prior to the
development of lesions, suggesting that growers should initiate fungicide sprays
immediately upon plant emergence as currently practiced. The detection of conidia
throughout the growing season into late August and early September indicates that
growers should continue fungicide sprays through September into mid October
depending on weather conditions and harvest date.

Atmospheric concentrations of A. panax conidia in ginseng gardens were
correlated with specific weather factors. ACCs were greatest during periods of
decreasing relative humidity. While conidia were detected during periods of high relative
humidity, concentrations were low and a significant negative correlation was found. This
suggests that conidia of A. panax are not actively released under high humidity
conditions. Despite a negative correlation between hourly rainfall and ACCs, a positive
correlation was detected for ACCs following 16 h or more after rainfall. The rainfall
events may temporarily remove conidia from the air, but the coincident leaf wetness
period provides favorable conditions for sporulation (14). The reduced ACCs during rain
events is likely attributed to rain scrubbing from the atmosphere (9). Optimum conidial
production of A. panax occurs with temperatures ranging from 18 to 25° C (2, 33). In our
study, significant ACCs were observed within that range and 225° C.

Similar correlations between ACCs and weather parameters reported in our study

have been reported for other Altemaria spp. A. solani conidia in controlled

43

 

environmental chambers were released with abrupt increases or decreases in relative
humidity, vibration, and rain events (8). Conidia of A. tenuis on banana are released
during a shift from wet to dry. During surface drying air bubbles are formed on conidial
chains of A. tenuis causing the conidial chains to twist and resulting in the release of
conidia (l9). Conidia of A. tenuis are also released following both an increase and
decrease in relative humidity (18). Conidia of A. alternata on tangerine similarly are
released following sudden increases or decreases in relative humidity and with simulated
rainfall events (32). While moisture is important for sporulation of Altemaria, most
Altemaria species including A. panax, are able to survive longer and reproduce faster,
and cause greater infection in drier (16 to 20° C) conditions (28, 32, 33).

Uncontrolled outbreaks of A. panax in one season may increase the potential for
epidemics in subsequent seasons, since the fungus overwinters in infested plant debris
and mulch. Each year, as ginseng prepares for dormancy, the stem collapses at the
rhizome. Premature defoliation as a result of foliar disease may also occur. Ginseng
growers practice a no-till cultivation system and mulch and plant debris are not removed
during the life of the crop (23 years). Seasonally infected crop material can become
integrated into the plant beds.

In the spring, overwintered inoculum from previously infected tissues spreads to the
newly emerging healthy plants via rain or splashing water and initiate the disease cycle for
the new growing season (12). In addition, overwintering conidia and/or mycelium can be a
source of stem infection as plants emerge through the infested mulch in the spring (26).
The overwintering of conidia on crop residue which serve as primary inoculum in the

spring, has similarly been observed for A. alternata (27, 34). Currently, there are no

44

practical methods to reduce overwintering inoculum levels on the mulch or on infected
crop residue (17).

Leaf wetness is a common and important component of disease models and
forecasters (31). The leaf wetness sensor in our study was placed within the top 25% of
the canopy, 25 cm from the bed gutter. As plants located on top of the bed were likely
exposed to increased air movement, the detection of leaf wetness could have been
compromised. Future studies should incorporate multiple leaf wetness sensors to detect
leaf wetness on the sides of the ginseng beds, where the plant canopy tends to remain wet
longer due to limited air movement. Additional studies including in vivo analysis of
conidial response to weather parameters should be conducted. In particular, determining
leaf wetness parameters for A. panax infection, and sporulation, and confirming the
temperature ranges for conidial sporulation and survival is important. Assessing the

effect of crop age on sporulation may also be helpful.

45

10.

11.

12.

LITERATURE CITED

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occurrence of ginseng diseases in Alberta in 1996. Can. Plant Dis. Surv. 77:78-
80.

Chang, K.F., Howard, R.J., Gaudiel, R.G., Hwang, SR, and Blade, SF. 1998.
Diseases of ginseng in Alberta in 1997. Can. Plant Dis. Surv. 7 8:89-91.

CSL. 2001. Pest risk analysis for Altemaria panax. Online publication. Last
accessed 3/12/2009. http://www.defra.gov.uk/planth/pra/alternariapanax.pdf.

David, J .C. 1988. Altemaria panax. CMI descriptions of pathogenic fungi and
bacteria. No. 955. Mycopathologia 103 (2): 105-124.

Davis, J. and Shoemaker, RB. 1999. Ginseng disease control Phytophthora and
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University.

Gottwald, T. R., Trocine, T. M., and Timmer, L. W. 1997. A computer-controlled
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Phytopathology 87:1078-1084.

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Hatcher, L. 1994. A step-by-step approach to using the SAS system for factor
analysis and structural equation modeling. SAS Publishing.

Hausbeck, M. K. 2004. Pest management in the future. A strategic plan for the
Michigan and Wisconsin ginseng industry. USDA Regional IPM Centers, Center
Products, PMSPs, Ginseng, archived, 04/13/2004. Online publication. Last
accessed 3/12/2009. http://www.ipmcenters.org/pmsp

Hausbeck, M. K. 2007. Pest management in the future. A strategic plan for the

Michigan and Wisconsin ginseng industry. USDA Regional IPM Centers, Center
Products, PMSPs, Ginseng, 12/14/2007. Online publication. Last accessed
3/12/2009. http://www.ipmcenters.org/pmsp

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Hill, SN. and Hausbeck, MK. 2008. Evaluation of TOM-CAST in timing
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Dis. 92:1611-1615.

Hirst, J .M. and Stedman, DJ. 1963. Dry liberation of fungus spores by rain
drops. J. Gen. Microbiol 33: 335-344.

Howard, R.J., Garland, J .A., and Seaman, W.L. 1994. Ginseng. Pages 294-299 in:
Diseases and Pests of Vegetable Crops in Canada. Canadian Phytopathological
Society and Entomological Society of Canada, Ottawa, Ontario, Canada.

Joy, A. E. and Parke, J. L. 1995. Biocontrol of Altemaria leaf blight on
American ginseng by Burkholderia cepacia AMMD. Pages 93-100 in: The
Challenges of the let Century - Proceedings of the International Ginseng
Conference, Vancouver, 1994. W. G. Bailey, C. Whitehead, J. T. A. Proctor, and
J. T. Kyle, eds. Simon Fraser Univ., Burnaby, BC, Canada.

Laemmlen, F. 2001. Altemaria diseases. Publication No. 8040. Regents of
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Leach, C. M. 1975. Influence of relative humidity and red-infrared radiation on

violent spore release by Drechslera turcica and other fungi. Phytopathology
65:1303-1312.

Meredith, D. S. 1963. Violent spore release in some fungi imperfecti. Ann. Bot.
27:39-47.

Parke, J. L. and Gurian-Sherman, D. 2001. Diversity of the Burkholderia
cepacia complex and implications for risk assessment of biological control
strains. Annu. Rev. Phytopathol. 392225-258.

Parke, J.L. and Joy, A.E. 1994. Patent No. US00536060A. Biological inoculant
effective against Altemaria.

Parke J .L. and Shotwell, KM. 1989. Diseases of cultivated ginseng. University
of Wisconsin-Madison. Agricultural Experiment Station. Publication no. 3465,

16 pp.

Pritts, K. D. 1995. Ginseng how to find, grow and use America’s forest gold.
Stackpole Books. Mechanicsburg, PA. 160 pp.

Pryor, B. 2003. Altemaria online. University of Arizona. Online publication.
Putnam, M. L. and du Toit, L. J. 2003. First report of Altemaria blight caused by

Altemaria panax on ginseng (Panax quinquefolium) in Oregon and Washington,
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Quayyum, H. A., Gijzen, M., and Traquair, J. A. 2003. Purification of a
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Altemaria panax. Phytopathology 932323-328

Reis, R. F., de Goes, A., Mondal, S. N., Shilts, T., Brentu, F. C., and Timmer, L.
W. 2006. Effect of lesion age, humidity, and fungicide application on sporulation

of Altemaria alternata, the cause of brown spot of tangerine. Plant Dis. 90:1051-
1054.

Rotem, J. 1994. The genus Altemaria: Biology, epidemiology and pathogenicity.
APS Press St. Paul, MN.

Schooley, J. 2003. Ginseng Production in Ontario OMAFRA Ginseng Series.
Online publication. Last accessed 3/12/2009.
http://www.omafra.gov.on.ca/english/crops/facts/gpak.htrn.

Scott, J. A., Rogers, 8., Cooke, D., and Fry, B. L. 1995. Woods-grown ginseng.
West Virginia Univ. Ext. Service, Agriculture, Field Crops. Online publication.

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wetness duration sensor: why it should be painted. Int. J. Biometeorol. 48:202-
205.

Timmer, L.W., Solel, Z., Gottwald, T. R., Ibaflez, A. M., and Zitko, S. E. 1998.
Environmental factors affecting production, release, and field populations of

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88:1218-1223.

Uchida, J. A. 2003. Crop Knowledge Master: Altemaria panax. Online
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Whiteside, J. O. 1988. Altemaria brown spot of mandarins. Page 8 in:

Compendium of Citrus Diseases. J. O. Whiteside, S. M. Garnsey, and L. W.
Timmer, eds. American Phytopathological Society, St. Paul, MN. 92 pp.

48

CHAPTER TWO

Evaluation of TOM-CAST in timing fungicide sprays for

management of Altemaria blight on American ginseng

49

NOTICE
This chapter has been published as: Evaluation of TOM-CAST in Timing Fungicide
Syravs for Management of Alternafria Blight on American Ginseng. The manuscript may

be found in Plant Disease, published by the American Phytopathological Society

Citation: 'Hill, SN, and Hausbeck, MK. 2008. Evaluation of TOM-CAST in timing
fungicide sprays for management of Altemaria blight on American ginseng. Plant Dis.

92:1611-1615.

50

ABSTRACT

Evaluation of TOM-CAST in timing fungicide sprays for management of
Altemaria blight on American ginseng.

By

Shaunta Nichelle Hill

Altemaria panax incites blighting of the foliage, peduncles, and drupes of
cultivated American ginseng (Panax quinquefolium). A disease forecaster (TOM-
CAST), originally developed to predict leaf blight caused by A. solani on tomato, was
evaluated for management of A. panax in commercial ginseng gardens. For three years,
fungicide sprays initiated by TOM-CAST (using 10- and lS-disease severity value
thresholds) were compared with sprays applied at 7- and 10—day intervals. Three
fungicide programs were evaluated: (i) chlorothalonil alone, (ii) chlorothalonil alternated
with pyraclostrobin, and (iii) copper hydroxide alternated with pyraclostrobin. As many
as 10 fewer fungicide applications were made when using TOM-CAST or the 10-day
programs. Although select TOM-CAST treatment programs were comparable to the 7-
day schedule in limiting foliar disease, only the 7-day applications adequately protected
drupe and seed yield. Both A. panax and alternata were recovered from drupe tissues
and seed coats. Only A. alternata was recovered from endosperrn halves. Ginseng seed

yield and quality is an important consideration when assessing fungicide programs.

51

INTRODUCTION

American ginseng (Panax quinquefolium) is a perennial herb grown primarily for
the medicinal properties of its root (24). Currently, more than 95% of the cultivated
commercial ginseng in the United States is grown in Wisconsin (1), totaling $50 to $75
million annually (11). Ginseng is grown on a raised plant bed under a natural tree or
artificial black woven polypropylene canopy (24). The shade required by the crop and
the dense plant spacing create a microclimate with limited air movement, increased
temperatures, and extended leaf wetness periods that are favorable for foliar pathogens.

The most common foliar disease of ginseng is Altemaria blight, caused by
Altemaria panax Whetzel (22). This disease is a yearly problem for ginseng growers in
Wisconsin (22) and Michigan (11). Altemaria blight also occurs in other ginseng
growing regions, including Alberta, Canada (7, 8), West Virginia (28), North Carolina
(9), Oregon, and Washington (25). Typical foliar symptoms include necrotic lesions with
dark-brown margins and yellow-green halos (22). Brown lesions often develop on the
stem just above the soil line and cause girdling (5). Infected drupes may develop a water-
soaked appearance followed by the development of brown mycelium and pathogen
sporulation. Infection of the root by A. panax is rare (22); however, root weight can be
reduced when blighting of the leaves and stem causes premature defoliation.

A. panax can survive as conidia or mycelia in infected plant residue, on straw
mulch, or in and on seed (16). In the spring, overwintered conidia may spread to and
infect emerging healthy plants via rain splashing or air currents. Under favorable
conditions, blight development and conidial production can occur in 5 to 7 days (30).

Optimum conidial production occurs with temperatures ranging from 18 to 25°C (5, 30).

52

Leaf wetness parameters for A. panax are unknown. However, researchers have shown
that conidia can germinate on leaf tissue within 1 to 2 h when incubated at 25°C and 70%
relative humidity (26).

Cultural strategies to manage Altemaria blight include increasing plant spacing to
enhance air circulation, removing infected foliage, and replacing mulch in the affected
area (9). However, these strategies are not practical and would not preclude the
reintroduction of inoculum via air currents. Previous researchers have investigated the
use of biocontrols as alternatives to traditional fungicides. Burkholderia cepacia AMMD
(Pseudomonas cepacia strain AMMD) was found to effectively inhibit Altemaria leaf
and stem blight under growth-chamber conditions. However, the biocontrol agent did not
adequately reduce disease under field conditions due to poor survival on leaf surfaces
(14, 21).

Currently, the strobilurin fungicides azoxystrobin and pyraclostrobin are used in
alternation with either chlorothalonil or mancozeb (11). Chlorothalonil and mancozeb
have been available to Wisconsin and Michigan ginseng growers through yearly Section
18 Emergency Exemption labels. Iprodione is also registered for the control of Altemaria
blight on ginseng and can be effective. However, following control failure in 1987, an
iprodione-resistant Altemaria population was identified in Wisconsin (27) and use of this
product declined.

Managing Altemaria blight is a priority of the ginseng industry in Michigan and
Wisconsin (11). When Altemaria blight is not controlled, complete defoliation of
ginseng can occur (12, 31). Using a forecasting system to assess disease potential

associated with environmental conditions may reduce the number of fungicide

53

applications needed per season (3, 4), lessen the chances for pathogens to develop
fungicide resistance, and reduce grower costs. Disease-forecasting systems use weather
variables (32) in conjunction with information about the biology and epidemiology of the
pathogen to predict when conditions favor infection or disease development (15). TOM-
CAST (developed for tomato disease forecasting) is a disease forecasting system that
calculates daily disease severity values (DSVs) based on cumulative hours of leaf
wetness and temperature. When the predetermined DSV threshold is reached, a fungicide
is applied and the DSV is reset to zero (23). TOM-CAST has been successfully
implemented to manage early blight on tomato (6, 23), purple spot on asparagus (l 8), and
foliar blights on carrot (3), and studies have shown it to be useful on crops such as
parsley (19) and celery (2).

Growers have expressed interest in identifying the environmental conditions that
favor blight development and testing the TOM-CAST forecasting system as a tool to
assist in timing fungicide applications (10). The objective of this study was to compared
the TOM-CAST disease forecasting system with a calendar-based spray schedule using
various fungicide programs for Altemaria blight control. The impact of these treatment

programs on seed yield and health was also of interest.

MATERIAL AND METHODS
TOM-CAST plot establishment. Field studies were conducted in a 3-year-old
(2005) or 4-year-old (2006 and 2007) commercial ginseng garden located in Marathon
County, WI. Each research site was 1.6 ha in area and consisted of a silt loam soil.

Ginseng gardens were established from seed planted into 1.5-m-wide raised beds that

54

were 22 to 30 cm high. After seeding, beds were covered with 15 cm of straw mulch.
Each year, woven polyethylene or polypropylene cloth panels providing 80% shade were
suspended via 2- to 3-m posts over the plant beds to mimic woodlot conditions. Weeds
were hand pulled. Treatment plots consisted of 1.5- by 3-m raised beds, with 0.60-m
buffers on each end. Treatments were replicated four times in a randomized complete
block design. Fungicides were applied with a C02 backpack boom sprayer equipped
with four 8006 nozzles spaced 45.7 cm apart, operating at 275.8 kPa, and delivering
467.7 liter/ha.

Weather monitoring and DSV calculation. Hourly measurements of air
temperature and relative humidity were recorded using a WatchDog data recorder (series
450; Spectrum Technologies, Inc., Plainfield, IL). An unpainted WatchDog leaf wetness
sensor (Spectrum Technologies, Inc.) was placed at a 45° angle facing north within the
upper 25% of the ginseng canopy. Data were downloaded weekly to a laptop computer
using a computer program (Specware 6.01 and 7.01; Spectrum Technologies, Inc.). The
program was set to record temperatures between 0 and 100°C and to detect leaf wetness
whenever moisture was present on the grid. Rainfall was measured hourly using a
tipping bucket rain collector (series 3554WD, Spectrum Technologies, Inc.).

For the TOM-CAST treatments, the hours of leaf wetness and the average air
temperature during the periods of leaf wetness were used to determine a daily DSV
ranging from 0 to 4, corresponding to environmental conditions unfavorable to highly
favorable for disease development, respectively (23). To accurately reflect the duration
of a morning dew period, a 24-h monitoring period of 1100 h to 1100 h was used. Daily

DSVs were accumulated until a threshold of 10 or 15 was reached, thus prompting a

55

fungicide spray. After each fungicide application, the DSV was reset to zero for both of
the TOM-CAST treatment programs.

Fungicide programs and application schedules. Fungicide programs included
chlorothalonil (Bravo Weather Stik 6SC, 0.68 kg of active ingredient [a.i.]/ha; Syngenta
Crop Protection, Inc., Greensboro, NC), chlorothalonil (0.68 kg a.i.lha) alternated with
pyraclostrobin (Cabrio 20EG, 0.07 kg a.i.lha; BASF Ag Products Research Triangle Park,
NC), and copper hydroxide (Kocide 2000 54DF, 0.73 kg a.i./ha; DuPont Crop Protection,
Wilmington, DE) alternated with pyraclostrobin (0.07 kg a.i./ha). Fungicide programs
were initiated on 26 May 2005, 26 May 2006, and 5 June 2007. Subsequent applications
were scheduled according to a calendar based interval of every 7 or 10 days or according
to the TOM-CAST disease forecaster using 10- or lS-DSVs. Fungicide programs were
terminated on 9 September 2005, 13 September 2006, and 30 August 2007.

Disease assessment. Disease was assessed by counting the number of A. panax-
infected plants in a 3-m section of the bed on 31 August and 14 September 2005; 20 July,
3, 16, and 24 August 2006; and weekly from 3 July to 4 September 2007. Data were
subjected to analysis of variance (ANOVA) and a Student-Newman-Keuls least
significant difference test (P = 0.05) was used to compare treatment efficacy (Statistical
Analysis Software [SAS] 9.1.3; SAS Institute, Inc., Cary, NC) (20). The area under the
disease progress curve (AUDPC) was calculated according to the methods of Shaner and
Finney (29) to express the yearly cumulative numbers of infected plants throughout the
seasons. The cumulative AUDPC values for each fungicide program and application

interval were subjected to ANOVA and a Student- Newman-Keuls significant difference

56

test (P = 0.05; SAS 9.1.3) was used to compare treatment efficacy. Treatments were also
assessed for phytotoxicity.

At the completion of the 2007 TOMCAST trial, drupes within the treatment and
control plots were harvested. After recording the fresh weights for each plot, 20 drupes
per replicate of each treatment and control were selected for fungal assessment. The
remaining drupes were placed in 3.8-liter plastic zip bags and stored at 37°C for 2 weeks.
Selected drupes were soaked in a 70% ethanol solution for 1 min and allowed to air dry
in a sterile laminar flow hood. Portions of drupe tissue were aseptically excised and
embedded in water agar (16 g agar/liter) plates (100 by 15 mm) amended with ampicillin
(2 ml/liter) and incubated at 25°C under fluorescent lighting.

Seed of the respective drupe samples were also soaked in a 70% ethanol solution
for 1 min and allowed to air dry in a sterile laminar flow hood. Following transverse
sectioning, seed coat and endosperm halves were embedded in water agar and incubated
as described for drupe tissues. After 48 h, all cultures were examined microscopically
(X200) for identification of fungi. Altemaria spp. were identified as A. alternata
according to Lagopodi and Thanassoulopoulos (17) (average conidium size, 30.4 by 11.1
pm) or as A. panax according to Brammall (5) (average conidimn size, 150-160 by 12-20
pm). The percentage of Altemaria spp. isolated from both drupe and seed tissues were
subjected to ANOVA and a ‘Student-Newman-Keuls significant difference test as
previously described. Following cold storage, the remaining drupes were macerated by
hand and the seeds removed. Seeds were soaked for 5 min in a 10% bleach solution,
triple rinsed with distilled water, and allowed to air dry before weighing. Seed and drupe

weights were also statistically analyzed.

57

RESULTS

Evaluation of fungicide programs and spray schedules with TOM-CAST.
The 7-day schedule resulted in 16 sprays in 2005 and 2006 and 12 sprays in 2007. The
10-day schedule resulted in 10 (2005), 12 (2006), and 8 (2007) applications. The TOM-
CAST 10-DSV schedule prompted 10, 7, and 4 applications and the 15-DSV schedule
prompted 6, 5, and 3 fungicide applications in 2005 (89 total DSVs), 2006 (83 total
DSVs), and 2007 (57 total DSVs), respectively.

In each year of the study, Altemaria blight resulted in premature defoliation and
death of untreated plants. In 2005 and 2006, all fungicide programs were similar and
limited foliar blight compared with the untreated control (Figure 1; Table 1). Similar
results were seen for 2005 and 2006 AUDPC data (Table 1). _ In 2007, disease Pressure
was greater. The 7-day schedule, regardless of fungicide program, significantly limited
numbers of infected plants compared to the untreated control (Figure 1; Table 1). Across
all years tested, the following treatment programs were similar to the 7-day treatments in
numbers of plants infected: chlorothalonil applied every lO-days, chlorothalonil
alternated with pyraclostrobin applied every 10-days and according to TOM-CAST 10-
DSV and lS-DSV schedules, and copper hydroxide alternated with pyraclostrobin
applied according to TOM-CAST 10-DSV (Table 1). However, according to the
AUDPC data, only chlorothalonil alternated with pyraclostrobin applied every 10 days or
according to TOM-CAST 10- and lS-DSV schedules and copper hydroxide alternated
with pyraclostrobin applied according to TOM-CAST lO-DSV provided consistent
season-long protection similar to the 7-day schedules (Table 1). Phytotoxicity was not

observed with any of the treatments.

58

Regardless of the fungicide program, the fresh weights of the drupes were
significantly higher for treatments sprayed every 7 days compared with all other
treatments and the untreated control (Table 2). The seed weight was significantly greater
for the treatments applied every 7 days, regardless of fimgicide program, when compared
with the untreated control. The weight of the seed from plots treated with chlorothalonil
alternated with pyraclostrobin every 10 days or according to TOM-CAST 10- and 15-
DSV schedules was similar to that resulting from the 7-day schedule (Table 2) but was
not significantly different from the untreated control. Similarly, copper hydroxide
alternated with pyraclostrobin applied every 10 days or according to TOM-CAST 10-
DSV resulted in seed weight similar to the 7-day schedule but was not significantly
different than the untreated control.

After the drupe tissue was incubated for 48 h, A. alternata and A. panax were
isolated from all treatments (Table 3). Only copper hydroxide alternated with
pyraclostrobin applied to plants every 10 days significantly reduced the incidence of A.
panax on drupes and seed coats compared with the untreated control. A. panax was not
detected on any of the seed endosperms, regardless of treatment (data not shown). A.
alternata was commonly found on the drupe, seed coat, and endosperm tissue. Only a 7-
day treatment of chlorothalonil alternated with pyraclostrobin significantly reduced the
occurrence of A. alternata on the drupe and seed coat compared with the untreated and all

other treatments.

59

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60

Table 2. Effects of fungicide programs and application schedule in management of
Altemaria panax on drupe and seed weight in 2007

 

 

 

Fresh weight (g)2
Treatmentsy Drupe 4 — Seed
Untreated 25.7 b 11.1 b
7-day schedule
Chlorothalonil 515.4 118.7 a
Chlorothalonil alt. pyraclostrobin 618.6 143.7 a
Copper hydrox1de alt. 602.9 142.9 a
pyraclostrobin
10-day schedule
Chlorothalonil 67.1 b 21.1 b
Chlorothalonil alt. pyraclostrobin 177.1 b 53.9 ab
Copper hydroxrde alt. 176.7 b 53.8 ab
pyraclostrobln
TOM-CAST 10 DSV schedule
Chlorothalonil 47.9 b 20.4 b
Chlorothalonil alt. pyraclostrobin 243.1 b 62.3 ab
Copper hydrox1de alt. 188.6 b 54.9 ab
pyraclostrobin
TOM-CAST 15 DSV schedule
Chlorothalonil 44.2 b 16.4 b
Chlorothalonil alt. pyraclostrobin 272.2 b 75.6 ab
Copper hydroxrde/ alt. 33.1 b 13.9 b
pyraclostrobin

 

yNumber of fungicide applications scheduled according to 7-day: 16 (2005 and 2006)

and 12 (2007), lO-day: 10 (2005), 12 (2006) and 8 (2007), 10 DSV: 10 (2005), 7 (2006)
and 4 (2007) and 15 DSV: 6 (2005), 5 (2006) and 3 (2007) timing intervals.
Chlorothalonil was applied at 0.68 kg a.i.fha, pyraclostrobin at 0.07 kg a.i./ha, and copper

hydroxide at 0.73 kg a.i.lha.

2 Column means followed by the same letter are not significantly different (Student-

Newman-Keuls, P=0.05).

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Figure. 1. Disease progress curves for Altemaria panax infection of 4-year-
old ginseng plants not treated or treated with the fungicide chlorothalonil (0.68
kg a.i.lha), chlorothalonil (0.68 kg a.i.lha) alternated with pyraclostrobin (0.07
kg a.i.lha), or copper hydroxide (0.73 kg a.i.lha) alternated with pyraclostrobin
(0.07 kg a.i./ha). Fungicide programs were scheduled during the 2006 growing
season every, A, 7 days, B, 10 days, or according to the TOM-CAST disease
forecaster using, C, 10 DSV or D, 15 DSV. Fungicide programs were
scheduled during the 2007 growing season every, E, 7 days, F, 10 days, or
according to the TOM-CAST disease forecaster using, G, 10 DSV or H, 15
DSV.

63

 

200 I I

150*A

100 -
50 -

 

4r

 

200 -

1505C

100 ‘1
50 -
o _
7/20 8I3 8/16 8I24 7/20 8I3 8l16 8I24
Month/day
+ Copper hydroxidelpyraclostrobin
—O— Chlorothalonillpy raclostrobin

+ Chlorothalonil
—/—\— Untreated

Number of infected plants

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

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2
D.
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.2
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0
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0
n
E
3
Z
0 ‘ I I I I I I I I I
7I3 7’18 8/2 8/14 8122 9I4 7I3 7/18 8/2 8114 8’22 9“-
Month/day

64

DISCUSSION

Altemaria leaf blight on ginseng is especially destructive, causing rapid
defoliation and plant death when left untreated. Without effective control measures,
growers risk reduced root yields or losing entire plantings (5).. Wisconsin and Michigan
Ginseng growers currently rely on fungicides to manage Altemaria blight during the
relatively long growing season of May through September. Ginseng growers must apply
fungicide sprays judiciously to protect the crop while complying with the labeled
seasonal application limits.

Optimizing fungicide applications by using a disease forecaster with reduced-risk
fungicides may offer an integrated pest management (IPM) strategy suitable for ginseng
production. A conservative threshold (IO-DSV) of TOM-CAST used with an alternating
program of chlorothalonil and pyraclostrobin provided control equivalent to 7-day
applications. Under moderate disease pressure, fungicides applied according to TOM-
CAST 10- or lS-DSVs adequately protected the crop foliage. In 2007, DSVs did not
accumulate quickly and fewer fungicide treatments were prompted. Some of the TOM-
CAST programs that included pyraclostrobin provided control similar to the 7-day
programs. Initial inoculum levels in 2007 may have been higher than in 2005 and 2006,
increasing disease pressure.

Although TOM-CAST lS-DSV is a practical and economical alternative to
calendar-based applications in asparagus (18), carrot (3), and tomato (6), high-value
crops such as celery and ginseng pose unique challenges. Carrot plants can tolerate some
Altemaria leaf blight and Cercospora leaf spot (caused by A. dauci and Cercospora

carotae, respectively) as long as they can withstand the mechanical harvesting which

65

pulls the roots from the ground (3). Also, these foliar pathogens do not typically
defoliate the crop as rapidly as observed with A. panax on ginseng. Similarly, purple spot
of asparagus (incited by Stemphylium vesicarium) causes premature browning and
defoliation of the photosynthetic tissue but consecutive years of premature defoliation is
required before yield is reduced (18). Carrot and asparagus are valued at $3,424 and
$2,420/ha, respectively (2), whereas celery and ginseng root average $20,431/ha (2) and
$13,930/ha (11), respectively. There is no tolerance for late blight on celery incited by S.
apiicola because the marketable portion of the celery is affected and consumers demand
unblemished product (2). Similarly, A. panax cannot be tolerated in a ginseng crop
because of its ability to rapidly blight and defoliate the crop, negatively affecting root and
seed yield.

Ginseng seed yield and quality is an important consideration when assessing
fungicide programs. Current market prices for stratified seed are SSS/kg. With an
average seed yield of 336.3 kg/ha, each hectare represents a value of $18,537. Even
when fimgicide programs were adequate, seed yield and quality was not always
acceptable. Sprays according to TOM-CAST 10-or 15-DSV or every 10 days resulted in
reduced seed weights compared with spraying every 7 days. Future research will test a
hybrid program whereby TOMCAST 10 DSV with chlorothalonil and pyraclostrobin is
used from plant emergence to flowering (mid- to late June), after which fungicides are
applied every 7 days to protect developing seed from becoming infected by A. panax
inoculum. As ginseng growers harvest their own seed for planting and to sell to other
growers, therefore, the potential seed dissemination of Altemaria is an important

component of overall disease management and must be addressed for an IPM program to

66

be successful. In our studies, A. panax was prevalent on the ginseng drupe and seed coat.
Although A. panax was not isolated from the endosperm in this study, previous seed
samples from ginseng growers submitted for diagnosis have often yielded this pathogen
from the endosperm tissue (13). In addition to A. panax, A. alternata was recovered from
ginseng seed. A. alternata is often encountered on other ginseng tissue, including stem
and leaves submitted for diagnostic evaluation. The impact of A. alternata associated
with seed tissues on viability and crop health is unknown.

Considering the chemical control measures needed to maintain commercial
ginseng gardens, continued efforts to explore methods to reduce sprays without risking
crop health are desirable. Alternating applications of fungicides with different modes of
action is critical due to restrictions on numbers of applications or amounts of fungicides
per season and to delay development of resistance in the pathogen. In our study,
alternating chlorothalonil with pyraclostrobin provided protection of the foliage and seed.
Because all fungicide programs tested in our project exceeded seasonal label allowances,
growers must incorporate additional labeled fungicides (i.e., mancozeb or boscalid) into
their management programs. Although these products were not included in this study,
field studies have been conducted that tested these fungicides against Altemaria and

indicated that mancozeb and boscalid would be helpful (12).

67

10.

ll.

12.

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70

PROPOSAL

FOR FUTURE WORK

71

Altemaria blight is a significant threat to ginseng (2, 3). If not controlled,
Altemaria blight can reach epidemic proportions within a month. The destructiveness of
A. panax is exacerbated by the cultivation practices for ginseng. To utilize limited land
resources and maximize profits, gardens are often densely planted. Dense crop planting,
coupled with the use of artificial shade creates a unique microclimate within the plant
canopy which can be beneficial to A. panax and other foliar pathogens. The primary
objectives of this research were to determine (i) A. panax inoculum availability and what
weather factors influence conidial concentrations, and (ii) if TOM-CAST could be
helpful in timing fungicide applications. While summarizing these objectives, other
research foci were identified to address garden monitoring, mulch contamination, and
additional forecasting systems.

As A. panax can overwinter in crop debris and mulch, there is a potential for
epidemics in subsequent seasons. Overwintering conidia can also serve as the first
inoculum source as plants emerge through infested mulch. In this research, ACCs were
detected throughout the monitoring periods. However, conidia may have been present in
the atmosphere earlier than May. In the future, spore trapping should include an
extended monitoring period to assess inoculum levels prior to crop emergence. It would
also be helpful to determine ACCs afier natural crop defoliation.

Ginseng cultivation is a no-till system. Currently, there are no practical methods
to reduce overwintering inoculum levels on the mulch. A common recommendation is to
remove straw mulch in infected areas yearly (1) however, most growers do not find it
practical when entire gardens are infected. A modification to this recommendation would

be to consider the complete mulch removal in the fall following the second or third

72

growing season. By moving the straw just once during the cultivation process, growers
may benefit from the reduction in overwintered inoculum and the financial costs of
replacing straw once as opposed to three or more times would be reduced.

The correlation between weather variables and ACCs is critical to the
development of disease models and disease management. Temperatures considered in
TOM-CAST range from 13 to 29°C and are based on conidiophore and conidium
formation of A. solani (4). With the use of a black polypropylene canopy, temperatures
within the ginseng gardens occasionally exceeded 29°C. TOM-CAST may require
modification to include higher temperatures as observed in commercial ginseng gardens.
In addition, placement of the leaf wetness sensor should be evaluated to adequately assess
moisture within the ginseng gardens. Prior to modification of TOM-CAST, temperature
and moisture requirements for A. panax germination and infection of ginseng should be
assessed. The infection process and potential treatments for A. panax on ginseng seed
would also be helpful.

As an alterative to TOM-CAST, the forecasting system Alter-Rater could be
tested. Alter-Rater uses a daily point value ranging from O to 11 depending on rainfall
+/- 2.5 mm, leaf wetness +/- 10 h, and average temperatures <20, 20-28, and >28°C (5).

F ungicide applications are then made once a threshold value has been reached. Alter-
Rater may be effective in ginseng gardens as it allows for a daily point accumulation with
an average day temperature between 20 and 28°C, rain < 2.5 mm and leaf wetness < 10 h,

whereas with TOM-CAST, leaf wetness must be present for a DSV calculation.

73

Literature Review

. Davis, J. and Shoemaker, P. B. 1999. Ginseng disease control Phytophthora and
Altemaria. Extension bulletin. North Carolina State University and A&T State
University. Hort. Inform. Leaflet No. 132.

. Hausbeck, M. K. 2007. Pest management in the future. A strategic plan for the
Michigan and Wisconsin ginseng industry. USDA Regional IPM Centers, Center
Products, PMSPs, Ginseng, archived, April 12, 2007. Online publication. Last
accessed 3/12/2009. http://www.ipmcenters.org/pmsp.

. Parke J. L. and Shotwell, K. M. 1989. Diseases of cultivated ginseng. University
of Wisconsin-Madison. Agricultural Experiment Station. Publication no. 3465,16

PP-

. Madden, L., Pennypacker, S. P., and McNab, A. A. 197 8. FAST, a forecast
system for Altemaria solani on tomato. Phytopathology 68:1354-1358.

. Timmer, L. W., Darhower, H. M., Zitko, S. E., Peever, T. L., Ibafiez, A. M., and
Bushong, P. M. 2000. Environmental factors affecting the severity of Altemaria

brown spot of citrus and their potential use in timing fungicide applications. Plant
Dis. 84:638-643.

74

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