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CHAPTER SIX
ENDOPHYTE STEM INFECTION AS AFFECTED BY VARIOUS FUNGICIDES ONTURF-TYPE TALL FESCUE
Abstract
Endophytes are known to enhance turfgrass agronomic performance and confer
resistance to insect herbivory. Little is known regarding the effect of fungicides to
seedlings for Rhizoctonia blight or gray leaf spot will affect endophyte viability. Various
fungicides were applied to 'DaVinci' turf-type tall fescue seedlings to determine their
effects on endophyte expression. Eight fungicides, both acropetal and localized
penetrants, were applied 7 or 21 days after establishment (DAE). Ten tillers were
harvested from each plot and cross sections of each tiller were analyzed for endophyte
presence using commercial tissue print-immunoblot test kits. In 2005, fungicide
application did not significantly affect endophyte infection rates in turf-type tall fescue 7
or 21 DAE. In 2006, however, fungicide application did significantly affect endophyte
infection rates 21 DAE. In general, propiconazole applied at 2.0 kg a.i. ha"1, seven DAE
reduced endophyte infection to 43% as compared to the control (57%). However,
myclobutanil and propiconazole (applied at 1.0 and 2.0 kg a.i. ha"1) significantly reduced
endophyte infection 21 DAE as compared to the control (90%) to 40, 40 and 7%,
respectively. These results show that propiconazole applied 21 DAE had lower endophyte
infection rates than when applied seven DAE. Endophyte mortality was reduced by the
fungicides myclobutanil and propiconazole but not eliminated. Therefore to maximize
endophytic turf, turfgrass managers should minimize certain fungicides like
propiconazole or decrease application rates especially during establishment.
133
Introduction
In recent years, tall fescue (Schedonorus phoenix (Scop.) Holub; formally know
as Festuca arundinacea Schreb.) has gained popularity and become widely planted in
lawns, athletic fields, and golf course roughs throughout the cool-humid region due to the
introduction of darker green, more narrow leaved, turf-type tall fescue cultivars. More
importantly, turf-type tall fescue is tolerant of drought because of its deep root system
which may necessitate less irrigation and less fertilizer to sustain ideal turfgrass quality.
Walker et al. (2007) found that turf-type tall fescue can be fertilized at relatively low
rates of nitrogen (74-123 kg N ha"1 yr"1) and still achieve a high visual appearance with
moderate growth compared to perennial ryegrass (Lolium perenne L.) and Kentucky
bluegrass (Poapratensis L.). In addition, turf-type tall fescue, even though it's a cool-
season turfgrass species, is a popular lawn species in the Southeast (warm-humid region)
due to its' lack of winter dormancy, remaining green throughout the year (Burpee, 1995)
unlike its warm-season counterparts. Seedling turf-type tall fescue, wherever grown, is
extremely susceptible to Rhizoctonia solani Kiihn and Pyricularia grisea which causes
the turfgrass diseases Rhizoctonia blight or brown patch and gray leaf spot, respectively
(Couch 1985).
Rhizoctonia solani causes foliar necrosis of circular or irregularly shaped patches
of necrotic turf that may exceed 1 m in diameter (Burpee and Martin, 1992). Pyricularia
grisea also causes foliar necrosis (blue-gray cast) which readily infects and kills leaf
blades which can progress down to the crown resulting in plant death. Both diseases,
brown patch and gray leaf spot, can be devastating on seedling tall fescue (< 1 yr.) killing
the entire turfgrass stand within weeks of infection. Weather conditions (hot, humid and
raining) favoring pathogen activity for both brown patch and gray leaf spot extend into
the early fall. This presents a major problem because the best time to seed cool-season
turfgrass species such as tall fescue is in the early fall so the plant can become established
before winter. Integrated methods for control against these diseases include avoiding
cultural practices that would extend the dew period to reduce of leaf wetness such as
watering or irrigating in the late afternoon and early evening and excessive nitrogen
134
applications. However, the best control against brown patch and gray leaf spot especially
on seedling tall fescue requires the use of fungicide applications (Smith et al., 1989).
Tall fescue is frequently infected with the endophytic fungus Neotyphodium
coenophialum [Morgan-Jones and Gams] Glenn, Bacon, and Hanlin) formally known as
Acremonium coenophialum. Endophytes and grasses have a mutualistic, symbiotic
association in which the plant provides the fungi with water, nutrients, and structural
refuge from the host in return the endophyte provides several benefits to the plant. These
benefits include: increased tillering and root growth, resistance to drought stress
(Arachavaleta et al., 1989), protection against insect herbivory (Rowman, 1993),
nematodes (Kimmons et al., 1990), mammalian herbivores (Bacon et al., 1977), and
fungal pathogens (Gwinn and Gavin, 1992). These benefits have made the use of
endophytes in turf an attractive alternative to chemical inputs used to enhance overall
turfgrass performance (Funk et al., 1985, 1992; Sun et al., 1990; Clarke et al., 2006).
Previous research by both White and Cole (1986) and Siegel et al. (1991) showed
that Acremonium coenophialum and other endophytes of grasses were able to inhibit the
growth of several fungal pathogens in vitro. However, disease resistance in endophyte-
infected grasses is still somewhat limited. Vincelli and Powell (1991) found that when
endophyte infection levels where high 'Manhattan IF perennial ryegrass (Lolium
perenne) had less red thread {Laetisaria fuciformis (McAlp) Burdsall) than endophyte
infection levels were low. In 1992, Gwinn and Gavin found that the survival of
endophyte-infected tall fescue seedlings was greater than that of non-endophyte-infected
seedlings in soil infested with two isolates of Rhizoctonia zeae Voorhees. Burpee and
Bouton (1993), however, reported that the progress of Rhizoctonia blight was not altered
by N. coenophialum in field grown tall fescue. Bonos et al. (2005) observed that
differences in red thread severity between endophyte-infected and non-endophyte-
infected fine fescue (Festuca spp.) occurred within the same host genotype. In 2006,
Clarke et al. reported endophyte-infected Chewings, hard, blue, and strong creeping red
fescue cultivars, selection, and crosses taken from fine fescue germplasm from the United
States and Europe, exhibited endophyte-mediated suppression of dollar spot (Sclerotinia
homoeocarpa) when compared to closely related non-endophyte-infected entries.
135
Latch and Christensen (1982) reported that seed treatments of propiconazole and
prochloraz and drenches of benomyl to potted plants eliminated an unidentified
endophyte from perennial ryegrass. Several studies have shown that triadimenol,
triadimefon, bitertanol, and propiconazole were the most effective fungicides for
eradicating Neotyphodium in tall fescue seed (Williams et al., 1984; Bilotti et al., 1989;
Maddaloni et al., 1989). Leyronas et al. (2006) found that prochloraz eliminated
Neotyphodium endophytes in perennial ryegrass and tall fescue seed. Few studies,
however, have investigated the effects on endophyte infection in plant stems as a result of
fungicide applications used to control turfgrass diseases (Dernoeden et al., 1990; Hill and
Brown, 2000). Dernoeden et al. (1990) found none of the fungicides used in the field
study (benomyl, triadimefon, iprodione, chlorothalonil, and thiram) reduced the percent
of the Acremonium endophyte in 'Regal' and 'Fiesta' perennial ryegrass infected with
endophytes. Hill and Brown's (2000) greenhouse study found that weekly applications of
the systemic fungicide, propiconazole (5%), virtually eliminated the endophyte in
seedling 'Jesup' tall fescue whereas, weekly applications of contact fungicides (terrazole
and chloroneb) had no apparent adverse effects on endophyte viability.
Rhizoctonia blight and gray leaf spot are severe diseases of seedling tall fescue
and therefore, management is limited to mainly fungicide applications. Previous research
conducted on the effects of fungicides on endophyte infection, have been limited to seed
testing and mostly greenhouse studies conducted with older fungicide formulations and
older cultivars of tall fescue. Currently, there are a wider range of commercially
available/modern fungicides for brown patch and gray leaf spot control which need to be
assessed for their effect on endophyte viability in newer turf-type tall fescue cultivars.
Therefore, the objective of this multi-year, field study was to determine the effects of
various fungicides on endophyte stem infection rates in turf-type tall fescue when applied
7 and 21 days after seedling emergence (DAE).
Materials and Methods
A field experiment was conducted from August 2005 through November 2006 at
the Purdue University, W. H. Daniel Turfgrass Research and Diagnostic Center, West
136
Lafayette, Indiana on a Stark silt-loam (fine-silty mixed mesic Aerie Ochraqualfs) with a
pH of 7.4, 67 kg P ha"1, 147 kg K ha"1, and 47 g kg"1 organic matter. Prior to planting, the
entire study area (17 x 9 m) was treated with glyphosate, N-(phosphonomethyl) glycine
to eradicate the existing turf. On the day of seeding, the entire study area was verticut to
facilitate seed to soil contact. Endophytic turf-type tall fescue ('Da Vinci') was seeded
(28 Aug. 2005 & 18 Aug., 2006) using the same seed lot both years (cold storage) at 391
kg ha"1 (Lebanon Seed Co., Lebanon, IN) using a drop spreader. This cultivar was
selected based on it's previously reported high, 84%, endophyte seed infection level
(Mohr et al., 2002). After seeding the entire study area received an application of 73 kg P
ha"1 from 6-24-24 (N-P-K) and was covered with Agrofabric Pro 17 germination blanket
(American Agrifabrics, Alpharetta, GA) to conserve moisture and promote germination.
The study area was frequently irrigated approximately three times daily via an overhead
sprinkler system to promote germination and seedling establishment.
Eight fungicides, at their label rates (Table 6-1), commonly used to control
seedling diseases were applied either 7 (12 Sept., 2005 & 1 Sept., 2006) or 21 (26 Sept.,
2005 & 14 Sept., 2006) days after emergence (DAE) to determine their effects on
endophyte infection at a spray volume of 215 gal ha"1. Emergence as defined as a uniform
stand of one-leaf seedlings which occurred on 5 Sept., 2005 and 25 Aug., 2006.
Localized penetrants included: iprodione [3-(3,5-dichlorophenyl)-N-(l-methylethyl)-2,4-
di-oxo-1-imidazolidinecarboxamide], triadimefon, and pyraclostrobin [carbamic acid, (2-
[[[ 1 -(4-chlorophenyl)-1 H-pyrazol-3-yl]oxy]methyl]phenyl]methoxy-, methyl ester].
Acropetal penetrants included: myclobutanil [a-butyl-a-(chlorophenyl)-lH-1,2,4, triazole-
1-propanenitrile], thiophanate-methyl [dimethyl 4,4'-o-phenylenebis(3-thioallophanate)],
flutolanil [N-(3-[l-methylethoxy] phenyl)-2-(trifluoromethyl) benzamide],
propiconazole, and azoxystrobin [methyl (E)-2-{2-[6-(2-cyanophenoxy) pyrimidin-4-
yloxy]phenyl}-3-methoxyacrylate]. Additionally, the plots sprayed in autumn 2005,
were sprayed again one year later (365 DAE) to determine what effect these fungicide
applications would have on endophyte infection when applied to a mature turfgrass stand.
When the study was repeated in 2006, the same eight fungicides were applied but two
additional treatments (Table 6-2) were added to include twice the label rates of
137
propiconazole (2.0 kg a.i. ha"1) and azoxystrobin (0.6 kg a.i. ha"1) because they are widely
used to control both brown patch and gray leaf spot and to assess a potential spray over-
lap situation.
Endophyte Infection
Approximately six weeks after emergence, ten tillers were randomly selected and
cut at the soil surface from each plot (1.5 x 1.5 m) to determine stem endophyte infection.
Tillers were wrapped in a damp towel and placed into a cooler of ice for transport to the
lab where they were stored overnight at 4°C. the following day, two, 2 mm cross sections
of each stem, 0.3 cm above the base, were analyzed for endophyte infection using
commercial tissue print-immunoblot test kits (TPIB) (Agrinostics Ltd. Co., Watkinsville,
GA) (Gwinn et al., 1991). For additional information on these procedures refer to
Appendix A.
General Plot Maintenance
The study site was located in full-sun with no obstructions, which was conducive
to rapid drying of the canopy in the early morning hours. Plots were mowed weekly (6.35
cm) throughout the growing season and clippings were not removed. In the absence of
significant rainfall (12 mm per week), overhead irrigation was supplementally applied
every two days (approximately 5 mm) to promote growth.
Experimental Design and Statistical Analysis
Each treatment was replicated three times and plots (1.5 x 1.5 m) were arranged in
a randomized complete-block design. All data was subjected to analysis of variance
(ANOVA) using the general linear model procedure in SAS (SAS Institute, Cary, NC).
Means were separated using protected least significant differences at the 0.05 level of
probability. Additionally, each fungicide treatment was compared to the untreated control
using pair-wise comparisons according to Dunnett's test.
138
Environmental Conditions
Weather data was collected from the Purdue University Airport, West Lafayette,
IN from Aug. 2005 through Nov. 2006. Environmental conditions, precipitation
measured as rainfall and high and low air temperature, varied between the two study
periods (Figure 6-1). Rainfall totaled 246 mm and 275 mm for Aug.-Nov. period in 2005
and 2006, respectively. Average air temperatures were slightly higher during the Aug.-
Nov. period in 2005 than in 2006 averaging 16°C and 14°C, respectively.
Results and Discussion
In 2005, fungicide application did not significantly affect endophyte infection
rates in turf-type tall fescue 7, 21, or 365 DAE (Table 6-1). In general, myclobutanil,
thiophanate-methyl, and pyraclostrobin reduced endophyte infection as compared to the
control (53%) to 33, 37, and 37%, respectively when applied seven DAE. Myclobutanil,
trifloxystrobin+triadimefon, and propiconazole reduced endophyte infection as compared
to the control (47%) to 37, 33, and 37%, respectively when applied 21 DAE. One year
later (365 DAE), propiconazole reduced endophyte infection to 27% as compared to the
control (37%). Even though there was a slight reduction in endophyte infection by the
application of these fungicides (Table 6-1), the decrease was not significant for the 7,21,
or 365 DAE applications. Dernoeden et al. (1990) reported similar results in which foliar
applications of fungicides (benomyl, triadimefon, iprodione, chlorothalonil, and thiram)
did not significantly reduce Acremonium endophyte infection in either 'Regal' or 'Fiesta'
perennial ryegrass. Hill and Brown (2000) found similar results in which weekly
applications of terrazole and chloroneb did not affect endophyte infection in seedling
"Jesup" tall fescue.
In 2006, fungicide application significantly affected endophyte infection rates 21
DAE (Table 6-2). In general, endophyte infection rates were lower than the untreated
control regardless of when propiconazole was applied which is consistent with previous
research in which the fungicide was applied to plant tissue (Harvey et al., 1982; Hill et
al., 1990; Hill and Brown, 2000) or as a seed treatment (Harvey, 1982). Propiconazole
applied at 2.0 kg a.i. ha"1 seven DAE, reduced endophyte infection to 43% as compared
139
to the control (57%). However, myclobutanil and propiconazole (applied at 1.0 and 2.0
kg a.i. ha1) significantly reduced endophyte infection 21 DAE as compared to the control
(90%) to 40, 40 and 7%, respectively. Hill and Brown (2000) reported similar results in
which propiconazole (4.0 g a.i. L"1) applied seven DAE reduced endophyte infection
(9%) compared to the untreated control (83%) for 'Jesup' tall fescue. Hill and Brown
(2000) also reported that propiconazole applied 21 DAE reduced endophyte infection
(55%). This study shows that increasing the rate of propiconazole from 1.0 to 2.0 kg a.i.
ha"1 decreased endophyte viability from 40 to 7%.
This study as well as other studies (Dernoeden et a l , 1990; Hill and Brown, 2000)
found that the use of some fungicides in seedling tall fescue adversely affected endophyte
viability however, effects are somewhat variable. The greatest risk in decreasing
endophyte viability occurs when more than the recommended label rate of these
fungicides are applied or when overlapping of fungicide occurs resulting in higher
application rates then typically suggested. It is important to note that endophyte mortality
was reduced but not eliminated by these fungicides used for brown patch and gray leaf
spot control. Due to beneficial attributes of endophytic fungi in tall fescue and the
extensive use of these fungicides to control Rhizoctonia blight or gray leaf spot on
managed turfgrass areas, these findings are important to turfgrass managers enabling
them to properly care for endophyte-infected tall fescue. Therefore to maximize
endophytic turf, turfgrass managers should minimize certain fungicides like
propiconazole or decrease application rates especially during establishment.
140
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144
Table 6-1. Percent endophyte stem infection of 'Da Vinci' turf-type tall fescue after eightfungicides were applied 7 and 21 days after emergence (DAE) in 2005.
Fungicide
IprodionePyraclostrobinTrifloxystrobin+TriadimefonAzoxystrobinFlutolanilMyclobutanilPropiconazoleThiophanate-methylNone
ANOVARepFungicide
TopicalActivity!
LPLPLPAPAPAPAPAP—
ApplicationRate
kg a.i. ha'1
3.10.60.90.36.41.51.06.1—
Endophyte Infection!
7 DAE
503750606033503753
NSNS
21 DAEo/o
474330435037375047
NSNS
365DAE
333737373053274037
NSNS
f AP=Acropetal Penetrant, LP=Localized PenetrantJTen tillers from each 2.3 m2 plot were tested for endophyte stem infection on 5 Nov.,2005 using a tissue print-immunoblot assay for Neotyphodium spp.NS refers to non-significantTurf-type tall fescue ('Da Vinci') was provided by Lebanon Seed Co., Lebanon, EN andseeded at rate of 391 kg ha'on 28 Aug., 2005. Emergence as defined as a uniform standof one-leaf seedlings occurred on 5 Sept., 2005.Seven DAE was applied on 12 Sept., 2005 and 21 DAE was applied on 26 Sept., 2005 ata spray volume of 215 gal ha"1.Randomized complete block design with three replications.
145
Table 6-2. Percent endophyte stem infection of 'Da Vinci' turf-type tall fescue after eightfungicides were applied 7 and 21 days after emergence (DAE) in 2006.
Fungicides
IprodionePyraclostrobinTrifloxystrobin+TriadimefonAzoxystrobinAzoxystrobinFlutolanilMyclobutanilPropiconazolePropiconazoleThiophanate-methylNone
ANOVARepFungicide
TopicalActivityt
LPLPLPAPAPAPAPAPAPAP—
ApplicationRate
kg a.i. ha"3.10.60.90.30.66.41.51.02.06.1—
Endophyte Infection^
7 DAE
7383709087806773436757
NSNS
21 DAE__o/o
83808767838340*40*7 ***
8090
NS***
t AP=Acropetal Penetrant, LP=Localized Penetrant{Ten tillers from each 2.3 m2 plot were tested for endophyte stem infection on 26 Oct.,2006 using a tissue print-immunoblot assay for Neotyphodium spp.*, *** and NS refer to significant at the 0.05 and 0.001 level and non-significant relative to theuntreated control using pair-wise comparisons with the untreated control according to Dunnett'stest, respectively.Turf-type tall fescue ('Da Vinci') was provided by Lebanon Seed Co., Lebanon, IN andseeded at rate of 391 kg ha^on 18 Aug., 2006. Emergence as defined as a uniform standof one-leaf seedlings occurred on 25 Aug., 2006.Seven DAE was applied on 1 Sept., and 21 DAE was applied on 14 Sept., 2006 at a sprayvolume of 215 gal ha1.Randomized complete block design with three replications.
146
Table 6-3. Analysis of variance (ANOVA) for both 2005 and 2006 study periods.ANOVARepDAEFungicideDAE*Fungicide
2005NSNSNSNS
2006NSNS***
*e, *** and NS refer to significant at the 0.05 and 0.001 level and non-significant, respectively.
147
200
150
1ca:
50
RainfallHighLow
Total = 246 mm
Jk
Total = 275 mm
Aug. Sept. Oct. Nov.
2005
Aug. Sept. Oct. Nov.
2006
40
30
20 Q
10
-10
-20
(D
2CDQ.
Figure 6-1. Daily temperature (high and low) and rainfall during Aug. through Nov. of2005 and 2006 in West Lafayette, IN.