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Article

Maize Inbred Leaf and Stalk Tissue Resistance to the Pathogen Fusarium graminearum Can Influence Control Efficacy of Beauveria bassiana towards European Corn Borers and Fall Armyworms

by
Patrick F. Dowd
* and
Eric T. Johnson
Crop Bioprotection Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, United States Department of Agriculture, Peoria, IL 61604, USA
*
Author to whom correspondence should be addressed.
Int. J. Plant Biol. 2024, 15(3), 673-682; https://doi.org/10.3390/ijpb15030049
Submission received: 18 June 2024 / Revised: 2 July 2024 / Accepted: 16 July 2024 / Published: 19 July 2024
(This article belongs to the Section Plant–Microorganisms Interactions)
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Abstract

:
Plant resistance mechanisms to pathogens can lead to a lowered efficacy of insect microbial biocontrol agents, but the influence of plant variety has been little-studied. Leaves and stalks from twelve maize (Zea mays L.) inbreds with different plant pathogen resistance were evaluated for their influence on the efficacy of Beauveria bassiana (Bals.-Criv.) Vuill. against European corn borers (Ostrinia nubilalis (Hübner)). For leaf assays with first instar caterpillars, mortality on day 2 ranged from an inbred-dependent high of 76.1% to a low of 10.0% for European corn borers in leaf assays. For stalk assays with third instar caterpillars, mortality on day 4 ranged from an inbred dependent high of 83.0% and 75.0% to a low of 0.0% and 8.3% for fall armyworms and European corn borers, respectively. Lesion size ratings due to Fusarium graminearum (Schwabe) applied to tissues were often significantly correlated with the mortality levels of B. bassiana-treated caterpillars that fed on leaves and stalks. This study suggests that the influence of plant varieties on the efficacy of insect microbial pathogens can vary depending on the insect species involved and the plant tissue, and this is worth considering when new plant varieties and biocontrol strains are being developed whenever practical.

1. Introduction

Insects impose a major challenge to the sustainable production of crops [1], so multiple pest management strategies need to be explored to identify the most economically effective ones for specific situations. The adoption of biological control is dependent on predictable results when implemented in the field. Understanding the factors that can influence biocontrol agents is important in developing more effective ways to deploy them. Prior studies have shown that the host plant species can influence the efficacy of Beauveria bassiana (Bals.Criv.) Vuill. [2,3]. Defensive plant secondary metabolites can inhibit the growth of B. bassiana [4]. When overexpressed in the callus, the same genes that inhibit the growth of pathogenic Fusarium fungi also inhibit the growth of B. bassiana, e.g., [5]. Studies with maize leaves have indicated that dent inbreds with different resistances to mycotoxin-producing fungi also differentially influenced the efficacy of two strains of B. bassiana applied to leaves against both corn earworms (Helicoverpa zea (Boddie)) and fall armyworms (Spodoptera frugiperda (J.E. Smith)) [6]. However, there were some instances where the relative activity of specific inbreds varied for the two insect species [6]. Both of these insect species are in the family Noctuidae and so are closely related. Another important maize pest is the European corn borer (Ostrinia nubilalis (J.E. Smith)), which commonly causes damage both by leaf feeding and stalk boring and is in the family (Crambidae). Tissue type and the associated chemistry and biochemistry may potentially influence interactions with the insect species and B. basssiana, so with European corn borers these types of interactions could also be investigated as they feed on both leaf and stalk pith tissue. Differences in the presence or associated gene expression of resistance-associated secondary metabolites and proteins have been reported for stalks in general [7] and for pith specifically [8], as well as for leaf and stalk proteins associated with fungal resistance [9]. Thus, it was of interest to examine the effects of inbreds with different disease resistance on the efficacy of B. bassiana to European corn borers using both leaf and stalk tissue. In the present study, the mortality levels over time to European corn borers varied depending on the inbred for both tissue types, and some specific inbreds had different influences depending on the strain of B. bassiana examined.

2. Materials and Methods

2.1. Plants

Maize inbreds were selected based on prior reports of maize kernel pathogen resistance: resistant inbreds included GE440, Mp313E, NC300 [10], Tex 6 [11], and Mp717 [12], and susceptible inbreds included B73, B104, FR1064, N6 [10]; T173 [12]; CML77, and Va35 [13]. Plants were grown and utilized for leaf assays as described previously by Dowd and Johnson [6]. Briefly, these twelve maize inbreds with different resistance to Fusarium pathogens were grown in a climate-controlled facility with a day temperature of 24 ± 2 °C, a night temperature of 18 ± 2 °C, a relative humidity of 50 ± 10%, and a 14:10 light–dark photoperiod with alternating metal halide and sodium lighting fixtures The soil mixture consisted of Redi Earth and SB300 bark mix supplemented with Osmocote, iron chelate, and liquified limestone. The youngest, fully expanded maize leaf was removed for bioassays when plants reached the 10–12 leaf stage. Once leaf assays were completed, maize plants were cut down and the section of the stalk between the lowest leaf and the prop roots was used in assays.

2.2. Insects

Fall armyworms from in-house colonies were reared on an artificial diet consisting primarily of pinto beans, wheat germ, and brewer’s yeast, at 27 ± 1 °C, 40 ± 10% relative humidity, and a 14:10 light–dark photoperiod, as described previously by Dowd and Johnson [6]. First instar larvae were used for leaf assays, and third instar larvae were used for stalk assays. European corn borer eggs were obtained from Benzon Research (Carlisle, PA, USA) and reared under the same conditions, using the same diet as for fall armyworms. First instar larvae were used for leaf assays, and third instar larvae were used for stalk assays.

2.3. Fungi

Sources of fungi were the same as those described previously by Dowd and Johnson [6]. Formulated preparations of B. bassiana strains Ant03 and GHA were obtained from Anatis Bioprotections Inc., QC, Canada and BioWorks, Inc., Victor, NY, USA, respectively. The F. graminearum was obtained from an in-house stock, designated III-B, originally collected in IL, USA [14]. Formulated B. bassiana spore concentrations of 15 mg/mL were used for fall armyworms [6], and a formulated spore concentration of 3 mg/mL was used for European corn borers due to their greater sensitivity, as indicated by preliminary experiments. Formulations of spores were added to 0.01% Triton-X-100®, which assisted in leaf wetting, to obtain the desired concentrations [6].

2.4. Bioassay Setups

First instar European corn borer larvae were used in leaf assays, as described previously [6]. Briefly, leaves were cut into approximately 2 cm squares. Beauveria bassiana treatments were applied to both sides of the leaf piece using a pipetting applicator and allowed to air dry in a chemical fume hood with an air flow of approximately 40 m/min between applications, which took from 30 to 60 min, depending on the room relative humidity. Leaf pieces were trimmed to approximately 1 cm on a side, which was approximately the edge of the application area. Each leaf piece was individually placed in a Petri dish with a tight-fitting lid that contained 3% water agar, along with 10 first instar larvae. Leaf pieces from all 12 inbreds were set up at the same time in three separate batches of 3 to 4 plants for each inbred. Thus, a total of 90 to 120 larvae per inbred were typically used. For assays with F. graminearum, slits were cut into the leaf pieces, and 2 μL of spore suspension was added to each slit. Leaf pieces for F. graminearum assays were taken from the same leaves used for insect assays, but they did not receive insects. The Triton® X-100 solution was applied alone to equivalent numbers of leaf pieces or leaf slits to serve as controls. Assays were run for 6 days with caterpillars and 4 days for F. graminearum.
Because no assays with stalk tissue from different maize inbreds have been performed previously, both fall armyworms and European corn borers were examined. Stalk assays were set up similar to previously reported methods [15]. Stalk sections approximately 30 cm long starting just above the support roots were cut into pieces approximately 2 cm long, which were wrapped with aluminum foil, except at one end. A 1 cm deep hole was drilled with a 0.4 mm diameter bit in the uncovered end to facilitate feeding on pith tissue by fall armyworms. Each stalk piece was placed in a 35 mL plastic cup. Because caterpillars may bore directly into stalk tissue and thus not encounter a lethal dose of B. bassiana if it was surface applied, caterpillars were immersed in spore suspensions. Caterpillars were treated with B. bassiana by dipping in the diluted formulations of B. bassiana spores, based on a previously described procedure for another boring insect [16], and then placed individually on stalk pieces. A lid was placed on the cup, and it was sealed with Parafilm and placed under the same conditions used to rear insects. There were typically 12 stalk pieces of each inbred used with each experiment per caterpillar species and B. bassiana strain. Controls were equivalent numbers of caterpillars dipped in the 0.01% Triton® X-100 solution alone placed on equivalent numbers of stalk pieces. Percent mortality values of B. bassiana-treated caterpillars were corrected using Abbott’s formula as necessary when the mortality of insects treated with Triton® X-100 solution alone fed corresponding maize inbred stalk pieces occurred, which was rare in most cases. For maize inbred stalk assays, 2 μL of F. graminearum spore suspension was applied to the cut end of the stalk, which was placed in a plastic cup as described for insect assays. Stalk pieces for F. graminearum assays were taken from the same stalks used for insect assays, but they did not receive insects. Assays were run for 10 days with caterpillars and 7 days for F. graminearum.

2.5. Bioassay Evaluations

Leaf assays were examined for mortality of insects, mycosis of dead insects (based on characteristic spore bearing structures), B. bassiana growth on leaf pieces, and F. graminerum lesions, as described previously [6]. Briefly, dishes or cups were examined for insect mortality by tapping; insects that did not move were considered dead. Leaf coverage by B. bassiana was rated on a 0 to 10 integer scale, with 0 being no growth present, and 10 being leaves totally covered with sporulating B. bassiana. The width of the sporulating B. bassiana on the stalk end was measured to the nearest mm. F. graminearum lesion size was measured to the nearest mm on both leaves and upward-pointing stalk ends.

2.6. Statistical Analysis

Analysis was performed as described previously by Dowd and Johnson [6]. Mortality values were examined for significant differences using Chi square analysis (Proc Freq, SAS version 9.4). Growth of B. bassiana on leaves and F. graminearum lesion size on leaf and stalk pieces were examined for significant differences by analysis of variance (Proc GLM, SAS version 9.4). Correlations (Proc Reg, SAS version 9.4) were determined for B. bassiana and F. graminerum associations, and outliers were removed as determined by plots generated by the program. These outliers could be due to the differences in resistance gene compositions of the highly diverse inbreds examined [9].

3. Results

3.1. Influence of Maize Inbred Type on Mortality Rate of Insects Fed Leaves and Stalks

On day 2 of the leaf piece assays, European corn borer mortality ranged from 46.6% to 0% when leaves were treated with the Ant03 strain of B. bassiana (Table 1). For the B. bassiana strain GHA in leaf piece assays, European corn borer mortality ranged from 10.0% to 76.1%. Overall, the ranked responses for inbred–strain combinations were similar, but there were some strain-dependent differences for a few inbred–strain comparisons, most notably for inbreds NC300 and Va35, suggesting that the tritrophic relationship is complex. Mycosis was noted for over 90% of dead insects. Inbreds causing a lower efficacy of B. bassiana had greater leaf damage over time (Figure 1).
On day 4 of the stalk piece assays, the results were similar to those seen for leaf experiments, with great differences in mortality depending on the inbred (Table 2). High control mortality ranging from 33 to 67 percent occurred for European corn borers fed stalk pieces from inbreds Mp717, NC300, and Tex6 for the B. bassiana strain GHA and over 50% for all three inbreds for the B. bassiana strain Ant03, which could not be corrected to useful values with Abbott’s formula; thus, those results were not included in the table. Mortality for the Ant03 strain of B. bassiana ranged from 83.3% to 0.0% for fall armyworms, and from 75.0% to 8.3% for European corn borers. Mortality for the GHA strain of B. bassiana ranged from 83.3% to 16.7% for fall armyworms, and from 60.0% to 9.1% for European corn borers. The overall ranked responses of both insect species for inbred–strain combinations were similar, but there were some large strain-dependent differences for a few inbred–strain comparisons, most notably for inbreds B73 and GE440 for the Ant03 strain of B. bassiana, and for inbreds FR1064 and GE440 for the GHA strain of B. bassiana. Due to the high control mortality of the European corn borers fed stalk pieces of Mp717, NC300, and Tex6, no data are supplied for those inbreds. Mycosis was noted for over 90% of the dead insects (Figure 2).

3.2. Influence of Maize Inbred Type on B. bassiana Growth and F. graminearum Lesion Size

Visible growth of B. bassiana on treated leaves varied, with means ranging from a rating of 0.5 to 2.3 for European corn borers fed leaves with the Ant03 strain of B. bassiana (Table 3). Visible growth of B. bassiana on leaves treated with the GHA strain of B. bassiana means ranged from 2.3 to 0.0 for European corn borers. Again, the relative coverage differed between strain—inbred combinations. There were some major differences between some inbred-strain combinations, notably for inbreds B73 and Va35. Growth of B. bassiana on stalk pieces was minimal and so it is not reported.

3.3. Association between B. bassiana Efficacy and F. graminerum Resistance

There was considerable variation in mean lesion size due to F. graminearum in leaves used in assays with European corn borers with rating rankings generally similar to each other, and they ranged from 4.0 to 1.2 mm for pieces from leaves used in European corn borer assays (Table 4). A much wider range of lesion sizes due to F. graminearum were noted for stalk piece assays, with mean lesion sizes ranging from 16.8 mm to 0.7 mm (Table 4). In several instances when most inbreds were included in the analysis, the lesion size produced was correlated with the effectiveness of the insect disease. In leaf assays with European corn borers and the Ant03 strain of B. bassiana with B104 and Mp313E values removed, R = 0.77, F = 11.47, P = 0.0095; with the GHA strain of B. bassiana with B73, FR1064, Mp313E, Mp717, and Tex6 values removed, R = 0.79, F = 8.46, P = 0.0335.
Significant associations between B. bassiana efficacy and F. graminearum resistance were also noted in stalk assays. In stalk assays with fall armyworms and the Ant03 strain of B. bassiana with the NC300 values removed, R = 0.68, F = 7.70, P = 0.0216; meanwhile, with the GHA strain of B. bassiana and NC300 values removed, R = 0.73, F = 10.81, P = 0.0094. In the stalk assays with European corn borers and the Ant03 strain of B. bassiana with no inbred values removed, R = 0.68, F = 6.00, P = 0.0441; meanwhile, with the GHA strain of B. bassiana and GE440, FR 1064, and T173 values removed, R = 0.85, F = 10.57, P = 0.0313.

4. Discussion

Prior studies have indicated that plant species can influence the efficacy of B. bassiana. One study investigated the effects of different Solanum species and Colorado potato beetles, with susceptibility to B. bassiana related to host plant suitability [17]. Chinch bugs (Blissus leccopterus) that fed on corn and sorghum were less susceptible to B. bassiana compared to those that fed on wheat and barley [3]. Prior studies also indicate that plant variety can influence the composition of microorganisms on plant leaves [18], including small grains [19], as well as in soil and the rhizosphere of maize [20,21]. A recent study also indicates that maize variety can also affect the efficacy of B. bassiana towards noctuid maize caterpillar pests when fed on treated leaves [9]. The present study demonstrates that maize variety can also influence the efficacy of B. bassiana towards a different plant tissue (stalk pith) as well as a major maize insect pest in a different family (Crambidae). The different maize inbreds may contain different levels of antifungal compounds that affect the pathogenic ability of B. bassiana. Interestingly, the variability in inbred influence on insect mortality did not always follow the same trend as noted for the ability of B. bassiana to grow on inbred leaf tissue, suggesting that different mechanisms are involved for the two different parameters. Additional experiments would need to be performed to determine the ability of different B. bassiana strains to colonize the tissue of different maize inbreds in the absence of insect damage.
In addition, the present study indicates that the influence of a plant variety on B. bassiana efficacy is dependent on the tissue and insect species involved. Variations in B. bassiana efficacy against different insect species have been reported previously [22]. Some, but not all, of the most effective strains against European corn borers versus fall armyworms were the same [22]. Relative rankings of B. bassiana efficacy were similar for fall armyworms feeding on treated leaves in a prior study [9] compared to European corn borers in the present study, but there were some exceptions. Ranking differences in B. bassiana efficacy from 8 to 10 were noted between fall armyworms and European corn borers for inbreds CML77 and Mp313E for B. bassiana strain Ant03 in leaf assays; large differences were also noted for inbred Mp313E when the GHA strain was assayed. Some large ranking differences between results of B. bassiana efficacy for fall armyworm vs. European corn borer assays were also noted in stalk tissue assays, for B73 and GE440 with the B. bassiana strain Ant03 and for GE440, FR1064, and N6 for the B. bassiana strain GHA. This information suggests that some specific plant factors interact with the caterpillar species in different manners.
The relative effect of different maize inbreds can also vary according to the strain of B. bassiana used, in combination with plant tissue and insect species, as was noted in a prior study [6]. Although, for the most part, differences in efficacy were similar for the two strains tested, there were some exceptions. In leaf assays with European corn borers, B. bassiana efficacy rankings for NC300 and Va35 differed by an interval of 5 to 6. In stalk piece assays, a difference of 7 rankings was noted for inbred NC300 with fall armyworms and with inbred B73 with European corn borers. This information suggests that some inbred-specific plant factors interact with the B. bassiana strains in different manners. It is likely that the two strains of B. bassiana have different gene combinations that can code for proteins that degrade plant defensive proteins and/or detoxify plant secondary metabolites that interfere with B. bassiana efficacy towards insects.
Plant variety or cultivar is thought to influence the ability of B. bassiana to colonize plants endophytically and thus influence insect control efficacy [23]. As reported previously for maize leaf tissue and Noctuid caterpillar species [6], the resistance of maize tissue to plant pathogens can negatively impact the efficacy of foliar applied B. bassiana. The same effect was noted in the present study, both for caterpillars in two different families for stalk tissue, and for both leaf and stalk tissue of maize fed European corn borers. In other words, the more resistant the tissues are to the representative plant disease organism F. graminearum, the less effective the B. bassiana was when the insect fed on that tissue treated with B. bassiana, suggesting that plant disease resistance interferes with insect pathogen effectiveness in controlling insects that feed on maize tissue. However, there were some examples where plant pathogen resistance did not interfere with the efficacy of B. bassiana. Although many different plant pathogen resistance genes are known, and in several cases resistance genes can vary for pathogens that have biotrophic versus necrotrophic strategies, there are reports of a few plant varieties that have resistance to plant pathogens in multiple tissues and diseases [24], suggesting that compatible plant variety, plant pathogen resistance, and B. bassiana efficacy is achievable.

5. Conclusions

As discussed previously, tritrophic interactions of fungal entomopathogens can be complex [25], which is further exemplified in the present study. In the present study, the results indicate that both maize inbred leaf and stalk tissue can influence the efficacy of different strains of B. bassiana towards maize caterpillar pests. The relative efficacy of the two commercial strains of B. bassiana to both insect species for both stalk and leaf tissue was often similar and associated with the degree of resistance to the maize pathogen F. graminearum, although variations did exist depending on the strain, tissue, and insect species combination. This information suggests that the plant varietal effect can vary according to the tissue, insect species, and strain of B. bassiana combination, and potentially be influenced by resistance mechanisms to plant pathogens, a phenomenon to consider for other insect pests and plant species. This situation helps explain the variability in efficacy that has been noted in the past for B. bassiana and other insect pathogens when applied in the field [26]. The development and tailoring of different plant variety and insect pathogen strain combinations may be necessary for the desired quality of insect pest management, and it will likely need to be conducted on a case-by-case basis that includes consideration of plant pathogen resistance. Effective deployment of insect pathogens can lead to more sustainable production of crops, conferring economic and quality benefits to growers, users, and consumers.

Author Contributions

Conceptualization, P.F.D.; methodology, both authors; data analysis P.F.D.; writing—original draft preparation, P.F.D.; writing—review and editing, both authors; project administration, P.F.D. All authors have read and agreed to the published version of the manuscript.

Funding

Funding for this work was provided to E.T.J. using USDA, Agricultural Research Service in-house project 5010-22410-024-00-D, and to P.F.D. using USDA, Agricultural Research Service in house project 5010-22410-0230-00D and USDA National Institute of Food and Agriculture grant 2019-33522-30037.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

We thank D.G. White, University of Illinois, Champaign, IL (retired); W.P. Williams, U.S.D.A., Agricultural Research Service, Mississippi State, MS; U.S.D.A., Agricultural Research Service, North Central Regional Plant Introduction Center for supplying initial maize inbred seed; M. Doehring and D. Lee for technical assistance; and J. L. Ramirez, F. E. Vega, and T. J. Ward for their comments on earlier drafts.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Leaf piece damage caused by European corn borer larvae fed different inbreds treated with the GHA strain of Beauveria. bassiana. (Left) leaf piece from inbred N6; (right) leaf piece from inbred Mp717.
Figure 1. Leaf piece damage caused by European corn borer larvae fed different inbreds treated with the GHA strain of Beauveria. bassiana. (Left) leaf piece from inbred N6; (right) leaf piece from inbred Mp717.
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Figure 2. European corn borer showing mycosis from Beauveria bassiana after feeding on a stalk piece of inbred FR1064 treated with the Ant03 strain of B. bassiana.
Figure 2. European corn borer showing mycosis from Beauveria bassiana after feeding on a stalk piece of inbred FR1064 treated with the Ant03 strain of B. bassiana.
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Table 1. Mortality on day 2 of first instar European corn borer larvae fed maize leaves treated with strains Ant03 and GHA of B. bassiana.
Table 1. Mortality on day 2 of first instar European corn borer larvae fed maize leaves treated with strains Ant03 and GHA of B. bassiana.
% Mortality
InbredAnt03GHA
B7315.6 * (6)19.3 * (10)
B10436.5 (2)63.2 (5)
CML7746.6 (1)76.1 (1)
FR106411.8 * (8)46.8 * (8)
GE4403.0 * (10)61.5 * (7)
Mp313E0.0 * (12)10.8 * (11/12)
Mp7171.9 * (11)10.0 * (11/12)
N623.5 (3)66.3 (4)
NC30013.6 * (7)71.9 (2)
Tex616.5 * (5)36.1 * (9)
T17322.4 * (4)62.0 (6)
Va3511.5 * (9)68.0 (3)
Percent mortality values followed by a “*” are significantly lower from the highest mortality value in a column (indicated in bold) at p < 0.05 by Chi square analysis. Ranks are indicated in parentheses.
Table 2. Mortality on day 4 of third instar larvae fed maize stalk pieces when larvae were treated with strains Ant03 and GHA of B. bassiana.
Table 2. Mortality on day 4 of third instar larvae fed maize stalk pieces when larvae were treated with strains Ant03 and GHA of B. bassiana.
% Mortality(Rank)
InbredFAW Ant03ECB Ant03FAW GHAECB GHA
B7318.2 * (7/8)45.4 (3)54.5 (6/7)33.3 (4/5)
B10416.7 * (9)16.7 * (8)50.0 (8/9) 18.2 * (7)
CML7718.2 * (7/8)18.2 * (7)54.5 (6/7)28.6 (6)
FR106433.3 * (4/5)50.0 * (2)50.0 (8/9)50.0 (2/3)
GE4408.3 * (11)41.7 * (4/5)25.0 * (10)50.0 (2/3)
Mp313E50.0 (3)75.0 (1)75.0 (3/4)60.0 (1)
Mp71733.3 * (4/5) 16.7 * (11/12)
N625.0 (6)41.7 (4/5)16.7 (11/12)33.3 (4/5)
NC30075.0 (2) 83.3 (1/2)
Tex683.0 (1) 83.3 (1/2)
T17312.5 * (10)25.0 * (6)62.5 (5)14.3 * (8)
Va350.0 * (12)8.3 * (9)16.7 * (11/12)9.1 * (9)
FAW = fall armyworm, ECB = European corn borer. Percent mortality values followed by a “*” are significantly lower from the highest mortality value in a column (indicated in bold) at p < 0.05 by Chi square analysis. Ranks are indicated in parentheses. Missing values for some ECB inbreds are due to the high mortality of controls.
Table 3. Visible growth coverage of strains Ant03 and GHA of B. bassiana on maize inbred leaves used in assays on day four.
Table 3. Visible growth coverage of strains Ant03 and GHA of B. bassiana on maize inbred leaves used in assays on day four.
0–10 Scale0–10 Scale
InbredAnt03GHA
B732.3 ± 0.3 (1)0.4 ± 0.2 * (8/9)
B1040.7 ± 0.3 * (10)0.0 ± 0.0 * (11/12)
CML770.5 ± 0.2 * (12)0.2 ± 0.1 * (10)
FR10640.9 ± 0.2 * (8)0.5 ± 0.2 * (6/7)
GE4400.8 ± 0.2 * (9)0.0 ± 0.0 * (11/12)
Mp313E1.7 ± 0.3 (2)2.3 ± 0.4 (1)
Mp7171.4 ± 0.2 (6)0.7 ± 0.2 * (3/4)
N60.6 ± 0.2 * (11)0.5 ± 0.3 * (6/7)
NC3001.5 ± 0.2 (4/5)0.8 ± 0.2 * (2)
Tex61.6 ± 0.2 (3)0.7 ± 0.2 * (3/4)
T1731.0 ± 0.4 * (7)0.6 ± 0.3 * (5)
Va351.5 ± 0.3 (4/5)0.4 ± 0.2 * (8/9)
Values are means ± standard errors of a 0 to 10 integer scale, with 0 = no growth seen, and 10 = leaf totally covered. Values followed by a “*” are significantly lower from the highest value in a column (indicated in bold) at p < 0.05 by analysis of variance. Ranks are indicated in parentheses.
Table 4. Size of necrotic zones due to Fusarium graminearum on maize inbred leaves and stalks used in assays with fall armyworms and European corn borers.
Table 4. Size of necrotic zones due to Fusarium graminearum on maize inbred leaves and stalks used in assays with fall armyworms and European corn borers.
InbredWidth (mm) LeavesWidth (mm) Stalks
B731.2 ± 0.1 * (12)3.9 ± 0.7 * (7)
B1041.9 ± 0.2 * (7)6.5 ± 1.2 * (4)
CML774.0 ± 0.4 * (1)1.6 ± 0.9 * (9)
FR10641.8 ± 0.2 * (8/9/10)4.4 ± 2.0 * (6)
GE4401.4 ± 0.1 (11)1.5 ± 0.6 * (10)
Mp313E2.6 ± 0.3 * (4)16.8 ± 2.5 (1)
Mp7171.8 ± 0.2 * (8/9/10)1.2 ± 0.5 * (11)
N62.3 ± 0.2 * (5)6.0 ± 1.3 * (5)
NC3003.3 ± 0.3 (2)1.9 ± 1.2 * (8)
Tex62.2 ± 0.2 * (6)11.5 ± 1.3 (2)
T1732.8 ± 0.3 * (3)7.5 ± 2.5 * (3)
Va351.8 ± 0.2 * (8/9/10)0.7 ± 0.5 * (12)
Values are means ± standard errors. Values followed by a “*” are significantly lower from the highest value in a column for leaves (indicated in bold) at p < 0.05 by analysis of variance. Ranks are indicated in parentheses. Stalks from the same plants were used in assays with both insect species.
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MDPI and ACS Style

Dowd, P.F.; Johnson, E.T. Maize Inbred Leaf and Stalk Tissue Resistance to the Pathogen Fusarium graminearum Can Influence Control Efficacy of Beauveria bassiana towards European Corn Borers and Fall Armyworms. Int. J. Plant Biol. 2024, 15, 673-682. https://doi.org/10.3390/ijpb15030049

AMA Style

Dowd PF, Johnson ET. Maize Inbred Leaf and Stalk Tissue Resistance to the Pathogen Fusarium graminearum Can Influence Control Efficacy of Beauveria bassiana towards European Corn Borers and Fall Armyworms. International Journal of Plant Biology. 2024; 15(3):673-682. https://doi.org/10.3390/ijpb15030049

Chicago/Turabian Style

Dowd, Patrick F., and Eric T. Johnson. 2024. "Maize Inbred Leaf and Stalk Tissue Resistance to the Pathogen Fusarium graminearum Can Influence Control Efficacy of Beauveria bassiana towards European Corn Borers and Fall Armyworms" International Journal of Plant Biology 15, no. 3: 673-682. https://doi.org/10.3390/ijpb15030049

APA Style

Dowd, P. F., & Johnson, E. T. (2024). Maize Inbred Leaf and Stalk Tissue Resistance to the Pathogen Fusarium graminearum Can Influence Control Efficacy of Beauveria bassiana towards European Corn Borers and Fall Armyworms. International Journal of Plant Biology, 15(3), 673-682. https://doi.org/10.3390/ijpb15030049

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