Introduction
Plant disease caused by insect-transmitted pathogens are among the most serious
production problems encountered by vegetable growers. Effective insecticidal control of
insect-borne disease is problematic because most plant disease vectors are highly mobile
insects and may colonize fields rapidly before growers are aware of their presence. In
addition, even low numbers of insects may result in high field incidence of disease, as
occurs with cucumber beetles and bacterial wilt disease (Yao et al. 1996). In
Alabama, insecticides were completely ineffective to prevent a serious epidemic of
cucumber mosaic virus (CMV) on tomato (Sikora et al. 1998). CMV is transmitted by
aphids in a nonpersistent manner, meaning that an aphid vector can acquire and transmit
virus in seconds. Thus insecticides do not act quickly enough to prevent inoculation. Our
research during the past six years has been directed towards microbe-induced resistance as
an alternative strategy for management of insect-transmitted diseases.
Plants have evolved complex and varied defense mechanisms for protection against
herbivory and disease. These mechanisms may be constitutive (e.g., active throughout the
plant’s life) or induced following attack by herbivores or pathogens. Recent studies
have suggested that inducible defenses in plants may have selective advantages over
constitutive defenses (Agrawal 1998 and references therein). While inducible defenses are
often localized at the site of attack, plant defense mechanisms may be activated
systemically throughout the plant following a localized infection or attack (Kessman et
al. 1994). One of the first published reports of systemic resistance in plants was by
Chester (1933), who used the term "acquired physiological immunity". Later, Ross
(1961) reported that tobacco plants exhibited "systemic acquired resistance"
following local infection with tobacco mosaic virus. Other terms that have been used to
describe systemic resistance in plants include "translocated resistance" (Hubert
and Helton 1967), "plant immunization" (Ku_ 1987), and "induced systemic
resistance" (Hammerschmidt et al. 1982). In this report, we will use the
latter term, or ISR, which can be defined as the process of active (systemic) protection
of a plant dependent on the host plant’s physical or chemical barriers activated by
an inducing agent when applied to a single part of the plant (Kloepper et al.
1992). Various "classical" inducers of ISR have been reported, including
pathogens, attenuated pathogens, synthetic chemicals, and metabolic products of hosts or
infectious agents (Liu et al. 1995, and references therein); however reports of induced
resistance in the field by classical inducing agents have been infrequent.
Kloepper and Schroth (1978) reported that certain root-colonizing bacteria could
promote radish growth in greenhouse and field trials and named the bacteria plant
growth-promoting rhizobacteria (PGPR). Results of early studies with PGPR also
demonstrated control of soilborne pathogens (Défago et al. 1990, Grusiddaiah et al. 1986,
Ordentlich et al. 1987). PGPR act as antagonists against soil pathogens through
competition (Elad and Chet 1987), or production of bacterial metabolites deleterious to
the pathogen (e.g., siderophores, HCN, antibiotics) (Kloepper and Schroth 1978, Thomashow
and Weller 1988, Weller 1988). More recently, three laboratories independently
demonstrated that certain PGPR strains protected plants through mechanisms associated with
ISR against pathogens that cause foliar disease symptoms (Alstrom 1991, Van Peer et al.
1991, Wei et al. 1991). Subsequent research at Auburn University has demonstrated
PGPR-ISR against various fungal and bacterial pathogens of cucumber (Liu et al. 1995a,b).
Following these studies, we were interested in testing some of the same PGPR strains for
ISR against three intractable insect-transmitted diseases; bacterial wilt of cucurbits
caused by Erwinia tracheiphila, and cucumber mosaic virus and tomato mottle
geminivirus on tomato.
Experiments with PGPR-ISR against Cucumber Beetles and Bacterial Wilt of Cucurbits
Field experiments in cucumber demonstrated that plants grown from seed treated with
PGPR sustained significantly lower populations of cucumber beetles, Diabrotica
undecimpunctata howardi and Acalymma vittatum, and lower incidence of bacterial
wilt disease (Figs. 1, 2 and 3) compared with nontreated control plants and plants sprayed
weekly with the insecticide esfenvalerate (Zehnder et al. 1997a). Free choice
greenhouse experiments with cucumber beetles were conducted in which beetles that had
acquired the wilt pathogen were released in screen cages (Fig. 4) and allowed to feed on
PGPR-treated or nontreated plants. Cucumber beetle feeding damage on cotyledons and stems
and incidence of wilt symptoms were significantly lower on PGPR-treated plants than on
nontreated plants (Zehnder et al. 1997b, Figs. 5 and 6).
Fig. 1. Control of cucumber beetles in field cucumber with PGPR and Asana.
Fig. 2. Incidence of bacterial wilt in field cucumber treated with PGPR and
Asana.
 
Fig. 3 (left). PGPR-treated cucumber on right showing protection against bacterial
wilt of cucurbits.
Fig. 4 (right). Screen cage used in experiments to evaluate PGPR protection against
cucumber beetle transmission of bacterial wilt disease of cucurbits.
 
Fig. 5 (left). Reduced cucumber beetle feeding on stems of PGPR-treated cucumber
compared with nontreated cucumber.
Fig 6. (right). PGPR-treated plant on left showing less feeding damage and wilt
symptoms compared with nontreated plant. Note PGPR-induced growth promotion in plant on
left.
Role of Cucurbitacin in Induced Resistance in Cucumber
Because cucumber beetle feeding behavior is strongly influenced by cucurbitacins, a
group of triterpenoid plant metabolites that occur in the plant family Cucurbitaceae
(Chambliss and Jones 1966), and previous studies demonstrated a positive correlation
between cucurbitacin content and cucumber beetle feeding (Ferguson et al., 1983),
we hypothesized that plants induced by PGPR treatment contain a reduced concentration of
cucurbitacins. To test this, we subjected cotyledon leaves of PGPR-treated and nontreated
cucumber plants to HPLC analysis for cucurbitacin. We tested two cucumber cultivars; one
with high and one with low levels of cucurbitacin. Results indicated that PGPR-treated
plants of both cultivars contained significantly lower levels of cucurbitacin than
nontreated plants (Zehnder et al. 1997b; Fig. 7). This suggested that a mechanism
for PGPR-induced resistance against cucumber beetle feeding may involve a change in the
metabolic pathway for cucurbitacin synthesis. Support for this hypothesis comes from
previous studies demonstrating that metabolic pathways for cucurbitacin and other plant
defense compounds share similar precursors (Balliano et al. 1982).
Fig. 7. Effect of PGPR treatment on cucurbitacin levels in straight 8 cucumber.
Experiments with PGPR-ISR against CMV on Tomato
Our success with PGPR-ISR in cucumber led us to expand our research to address cucumber
mosaic virus (CMV) infection of tomato. A severe epidemic of CMV in fresh market tomato in
North Alabama resulted in an estimated 25% yield loss in that region (Sikora et al. 1998).
CMV is a particularly difficult virus to manage, due in part to its extensive host range
and ability to be transmitted by more than 65 aphid species. Moreover, there is a lack of
genetically resistant fresh-market tomato varieties to CMV infection, so management
options are limited. Thus, tomato growers are in need of alternative management
strategies, particularly those that are environmentally sound and easily implemented.
A series of greenhouse experiments was conducted at Auburn to evaluate 26 PGPR strains
for ISR against CMV in tomato. These strains were selected based on their ability to
induce resistance against other pathogens of cucumber and tomato. In these experiments,
PGPR cultures were centrifuged and the tomato seeds mixed with the bacterial pellet before
planting into plastic pots with planting mix. After two weeks of growth, tomato plants
were transplanted into new plastic pots containing planting mix, and PGPR suspension
treatments (100 ml containing approximately 5 x 108 cfu/ml) were poured into
each pot immediately after transplanting. CMV inoculum was prepared from fresh tobacco
leaves infected with CMV. The CMV extract was rub-inoculated onto the first two tomato
leaves/plant one week after transplanting. Plants were examined daily for CMV symptoms
(Fig. 8); these typically include leaf distortion, chlorosis and mosaic symptoms on
leaves, and a general stunting of the plant. The number of symptomatic leaves per plant
and the number of plants with severe symptoms (e.g., >2/3 of symptomatic leaves) were
recorded. After the initial screening experiment, 14 of the best PGPR strains were
selected for further evaluation. The range in the percentage of plants exhibiting CMV
symptoms 10 days after inoculation in the 14 PGPR treatments was 40-70%, compared to 100%
of plants with symptoms in the treatment where plants were inoculated with CMV but not
treated with PGPR. In a second series of greenhouse experiments to evaluate the 14 PGPR
strains, treatment with 8 PGPR strains resulted in 30-40% plants with symptoms, compared
to 90% of nontreated plants with symptoms. Finally, in a third series of greenhouse
experiments, 4 of the 8 PGPR strains were chosen for further evaluation in field
experiments. The percentage of plants with CMV symptoms in the 4 PGPR treatments ranged
from 14.7 to 22.1%, compared with 75.8% of plants with symptoms in the plants without PGPR
treatment.
Fig. 8. CMV symptoms on tomato.
Field experiments were done in 1996 and 1997 to evaluate the 4 PGPR strains, a disease
control (mechanical inoculation with CMV; no PGPR) and a healthy control (no CMV
inoculation; no PGPR). There were 6 replications per treatment arranged in a randomized
block design, each consisting of 15 tomato plants (single row plots). For PGPR treatments
in the field experiments, `Mountain Pride’ tomato seeds were mixed with the PGPR
pellet (as described above). In addition to seed treatment, a PGPR soil drench was poured
around the base of each plant immediately after transplanting (when plants were in the two
leaf stage). All plants except those in the healthy control treatment were inoculated with
CMV, as described above, one week before transplanting in the field. All plants in each
treatment were examined weekly for virus symptoms using the following rating scale: 0, no
symptoms; 2, leaf puckering or curling just beginning; 4, 50% of leaves on plant appear
puckered or curled; 6, mosaic symptoms just beginning; 8, 50% of leaves showing mosaic
symptoms; 10, 100% of leaves showing mosaic symptoms. Disease severity values were
calculated using the formula:
Disease severity (Y) = [S(rating no.) (no. plants in
rating category)(100)]
(Total no. plants)(highest rating value)
Disease progression over time was measured using a formula for calculating the area
under the disease progress curve (AUDPC):
AUDPC = S [(0.5)(Yi + 1 + Yi)(Ti
+ 1 + Ti)]
where Y = disease severity at time T, and I = the time of the assessment (in days
numbered sequentially beginning with the initial assessment).
In addition to virus symptom rating, leaves from the upper plant canopy were collected
from each plant 32 days after transplanting in the field (90 leaf samples per treatment).
Leaf samples were subjected to indirect enzyme-linked immunosorbent assay (ELISA). Height
of plants was measured 30 days after transplanting in the field. Marketable (non-damaged
and mature) tomato fruit were weighed on 6 harvest dates during the season.
In the 1996 field experiment, AUDPC values, indicating disease symptom progression over
time, were significantly lower in all PGPR treatments compared with the disease control
(Fig. 9). Similarly, ELISA values in all PGPR treatments, and the percentage of infected
plants (Fig. 10) (based on ELISA) in 3 PGPR treatments, were significantly lower than in
the disease control. The percentage of infected plants in the disease control treatment
was over 3-fold greater than in the IN937a and IN937b treatments. Plant height
measurements taken 30 days after transplanting indicated that plant growth in the PGPR
treatments was greater than in the disease control. The increased growth may have resulted
from PGPR-induced resistance against CMV, PGPR-induced growth promotion, or both factors
combined. Importantly, yields in the SE34, IN937a and IN937b treatments were significantly
greater than in the disease control (Fig. 11).
Fig. 9. PGPR-ISR against CMV on field tomato, 1996: AUDPC values.
Fig. 10. Powerpoint bar graph: PGPR-ISR against CMV on field tomato, 1996: % infected
plants.
Fig. 11. PGPR-ISR against CMV in field tomato, 1996: Yields.
As in 1996, results of the 1997 field experiment indicated that AUDPC values (Fig. 12)
and ELISA absorbance values were significantly lower in the PGPR treatments than in the
disease control. Overall, the percentage of plants infected with CMV was higher in 1997
than in 1996 (Fig. 13). In 1997, 62.2% of the nonchallenged, healthy control plants were
infected, suggesting that naturally-occurring aphids acquired the virus by feeding on the
mechanically-inoculated plants, and subsequently inoculated other plants, including those
in the healthy control treatment. This could have resulted in the higher incidence of CMV
in 1997. Although the percentages of infected plants in the PGPR treatments were lower
than in the disease control, differences were not significant. Plant growth was
significantly greater in the PGPR treatments compared with the disease control, but
average tomato yields were not significantly different among treatments.
Fig. 12. PGPR-ISR against CMV in field tomato, 1997: AUDPC values.
Fig. 13. PGPR-ISR against CMV in field tomato, 1997: % infected plants.
Field Experiment with PGPR-ISR against Tomato Mottle Geminivirus on Tomato
Tomato mottle, caused by the tomato mottle virus (ToMoV), poses a major threat for both
transplant and field production of tomato in west-central and south-west Florida (Abouzid
et al. 1992, Polston et al. 1993). ToMoV is in the geminiviridae family and is transmitted
by adult sweet potato whiteflies, Bemisia tabaci, biotype B (also known as the
silverleaf whitefly, Bemisia argentifolii). Symptoms of ToMoV in field grown
tomatoes include chlorotic mottling and upward curling of leaflets, and an overall
reduction in plant height and in the number and size of fruit (Polston et al. 1993).
Similar to the CMV pathosystem, management of ToMoV is very difficult. Tomato varieties
resistant to ToMoV are not yet commercially available, and insecticides have not provided
effective management; in part because of the development of insecticide-resistant whitefly
biotypes. Prompted by our findings that PGPR-ISR successfully protected tomato from
infection by CMV, trials were planned to evaluate PGPR for ISR in tomato against ToMoV.
Field experiments were conducted during the fall tomato growing season at the
University of Florida Gulf Coast Research and Extension Center in Bradenton, Florida.
Tomatoes grown at the Center were exposed to high levels of natural whitefly infestation
and ToMoV infection. Spores of PGPR strains IN937b and SE34 (two of the strains used in
experiments with CMV described above) were produced in culture and formulated as both a
seed treatment and a powder by Gustafson Corp., Plano, TX. The PGPR powder was diluted
with water according to manufacturer recommendations and incorporated into the planting
mix before seeding. Seed treatment and powder formulations of each PGPR strain were
evaluated in single row plots; treatments were replicated four times. At 40 days after
planting, each plant in each treatment plot was rated for disease severity using a scale
of 0 to 2.5, and all samples were analyzed for ToMoV DNA by dot blot analysis (Polston et
al. 1993). Leaf samples for analysis of ToMoV DNA were also collected 80 days after
planting. The disease rating scale was as follows: 0 = no symptoms; 0.5 = early stages of
chlorosis of young leaf bases; 1.0 = obvious chlorosis/mottle of leaves on any of the
tomato plant stems; 1.5 = obvious chlorosis/mottle of leaves over most of the plant; 2.0 =
serious chlorosis/mottle of leaves and deformation and leathery appearance of leaves; 2.5
= severe chlorosis/mottle of leaves and deformation and leathery appearance of leaves and
plants severely stunted. Tomatoes were harvested from all plots 80, 94 and 108 days after
transplanting.
The IN937b and SE34 PGPR strains both provided protection against ToMoV in the Florida
tomato field experiment. Visual symptom ratings and dot blot analysis of leaves at 40 days
after transplanting indicated that the PGPR powder and powder + seed formulations were
more effective for ISR against ToMoV than the PGPR seed formulations (Fig. 14). The
severity of virus symptoms was significantly lower in all PGPR powder and powder + seed
treatments than in the nontreated control, but symptoms were
not significantly different between the seed-only treatments and the control (contrast
analysis; a = 0.05). There were no significant differences in symptom ratings between the
PGPR powder only and the PGPR seed + powder formulations. Contrast analysis of the
percentage of plants testing positive for ToMoV DNA from leaf samples collected 40 days
after planting generated similar results (Fig. 15). By 80 days after planting, most plants
in all treatments were infected with ToMoV, and differences in the percentages of infected
plants among treatments were not significant.
Fig. 14. PGPR-ISR against ToMoV in field tomato, 1997: symptom ratings.
15. PGPR-ISR against ToMoV in field tomato, 1997: % infected plants.
At the first harvest date at Bradenton (80 days after transplanting), tomato yields
were higher in PGPR powder or seed + powder treatments than in the control or seed-only
treatments; however yield differences were statistically significant only between the 937b
powder treatment and the control. Analysis of tomato yield data from harvests at 94 and
108 days after transplanting did not indicate a significant effect of PGPR treatment on
tomato yield. We suspect that PGPR-ISR against ToMoV occurred in the early stages of
infection, but that continual whitefly infestation of plants and inoculation of the virus
eventually overcame the induced resistance response.
Discussion
The results with CMV provide a preliminary indication that PGPR-induced ISR against CMV
on tomato, previously reported from greenhouse experiments (Raupach et al. 1996),
can be obtained under field conditions. It is known that virus symptoms and effects on
yields are most severe when plants are infected with virus in early growth stages.
Therefore, we were encouraged by the 1996 field results showing that virus symptoms were
reduced and tomato yields were not affected on PGPR-treated plants that were mechanically
challenged with virus even before transplanting in the field. In 1997, when natural CMV
infection by aphids apparently supplemented infection by mechanical infection, PGPR
treatment reduced the severity of virus symptoms, but the effects of PGPR treatment on the
percentage of infected plants and on tomato yields was not as great as in 1996. This may
indicate that the impact of PGPR-ISR may be most apparent when the levels of virus
inoculum are low or moderate, and that PGPR-induced plant defense mechanisms are not as
effective in the presence of high viral inoculum. This hypothesis is corroborated by the
fact that we have not observed PGPR-ISR against naturally-transmitted CMV in trials
conducted on a north Alabama tomato farm where the incidence of CMV infection was
extremely high.
The results with ToMoV in Florida following the CMV experiments in Alabama demonstrate
that specific PGPR strains can provide broad spectrum protection in field tomato against
viruses in different groups with different insect vectors; i.e., CMV with aphids and ToMoV
with whiteflies. The observed level of PGPR-ISR against ToMoV was encouraging given that
the PGPR strains used in the Florida trial were selected based on screening for activity
against CMV and not ToMoV. This illustrates the potential of PGPR to provide broad
spectrum protection against several pathogens. The levels of whitefly infestation and
ToMoV inoculum at the Bradenton field experiment site were greater than what typically
occurs in commercial tomato fields. Thus it is possible that the level of PGPR-induced
protection against ToMoV in commercial tomato fields may be greater than might be expected
based on our experimental results. In addition, vegetative cell treatments of PGPR were
used in our previous experiments in tomato. The PGPR spore seed and powder formulations
used in the Florida trial had not previously been tested.
Results of the Florida experiment also indicate that the PGPR powder formulations were
more effective for ISR against ToMoV than the treatments where PGPR was applied only to
the seed. Although we have not compared the speed of PGPR germination and root
colonization in the two formulations, it is possible that these events occurred earlier in
the powder formulation treatments than in the seed treatments resulting in an earlier ISR
response. Formulations of PGPR powder provide a practical delivery system for ISR in crops
because powder can be easily added to planting mix, or mixed with water and applied as a
transplant drench application.
Our results with PGPR-ISR over the past six years have shown that PGPR can be an
effective tool for crop protection against a variety of plant pathogens and, in specific
cases (i.e., cucumber beetles and bacterial wilt), can protect plants from insect feeding
and transmission of disease. Cooperative work with Gustafson, Inc., is underway to
evaluate commercially-prepared PGPR seed treatments for cucumber, and it is possible that
a PGPR seed treatment for cucurbit crops will be commercially available within the next
few years. We will continue to evaluate the stability and durability of PGPR protection
against plant viruses under diverse field conditions where natural infection by insect
vectors occurs. Increased efforts to screen PGPR strains for ISR against other viruses,
like ToMoV, will likely result in the identification of PGPR strains, or a combination of
strains, that may be used effectively to reduce the impact of virus infection on plant
health and yields.
Because specific PGPR strains have demonstrated ISR against multiple pathogens, it is
possible that several PGPR strains could be identified for each vegetable crop to provide
some level of protection against multiple pathogens of economic importance. We do not view
PGPR as a universal solution for all crop protection needs. Rather, we believe that PGPR
represent a potentially useful tool for environmentally sound pest management programs and
a means to reduce our reliance on pesticides by exploiting the plant’s existing
defense mechanisms.
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