© 2011 Plant Management Network.
Field Evaluation of Trichoderma spp. for Control of Armillaria Root Rot of Peach
G. Schnabel, College of Agriculture, Forestry and Life Sciences, A. P. Rollins, and G. W. Henderson, Cooperative Extension Service, Clemson University, Clemson, SC 29634
Schnabel, G., Rollins, A. P., and Henderson, G. W. 2011. Field evaluation of Trichoderma spp. for control of Armillaria root rot of peach. Online. Plant Health Progress doi:10.1094/PHP-2011-1129-01-RS.
Management of Armillaria root rot (ARR) of perennial crops is challenging and requires an integrated approach. In this study, Trichoderma asperellum and T. gamsii formulated as Remedier WP were drenched onto peach trees 3 to 12 days after planting (2007), and biannually thereafter in spring and fall for a total of three years in two commercial replant sites of South Carolina. All trees were planted in spots where a tree had declined from ARR the previous season to maximize disease pressure. Tree survival and trunk diameter were determined each year in the control and Remedier WP treatments. Four years after planting (2011), about 50% of all control trees and Remedier WP-treated trees had died from ARR in both locations. There was no statistical significance in survival between the treatments in either location. However, three and four years after planting, surviving Remedier WP-treated trees had significantly larger tree trunks compared to control trees in the Campobello location. Not enough trees survived in the other location for meaningful analysis of tree trunk diameter data. Our results show that in soils with heavy ARR inoculum levels, biannual drenches of Trichoderma spp. formulated as Remedier WP starting at planting are ineffective for ARR control of peach.
Armillaria root rot (ARR) is a soil-borne disease affecting virtually all woody plants and even herbacious plants. The disease causes severe damage on peach in the southeastern United States, where it is primarily caused by A. tabescens (19). For example, in South Carolina between 1987 and 1992, the disease was estimated to have caused $3.86 million in annual losses (15), and in Georgia from 2000 to 2002 Armillaria root rot resulted in > $1.5 million in losses, including control costs, to the peach industry (22). Most commercial peach growers in South Carolina and Georgia encounter ARR-caused tree decline.
Currently available rootstocks are highly susceptible, but some new, as yet unavailable rootstocks hold potential for disease resistance (3). Some cultural control methods such as root collar excavation can extend the life of perennial trees on replant sites, but studies were largely conducted with citrus trees (4,6) and the system has not yet found commercial acceptance. Some chemical control options were found to reduce ARR disease incidence (1), but none provide a level of control that would sustain peach production on replant sites. Various biological control options have been investigated, including the exploration of competitive exclusion (7), but again results do not provide commercially viable control leaving producers with very few to no tools for ARR management. The lack of effective control options justifies the search for alternatives.
Trichoderma spp. are fungal antagonists that can protect plants from foliar and root pathogens. The antagonist can have direct effects on plant pathogens in the form of parasitism, competition for nutrients and space, and consumption of key exudates from seeds that stimulate the germination of propagules of plant-pathogenic fungi (8,14,21). In addition to the direct effects, Trichoderma may also contribute to protection from disease through indirect effects. For example, several studies have documented the ability of the antagonist to induce systemic and localized resistance to a variety of plant pathogens (14). The potential for Trichoderma spp. to control ARR of peach and other stone fruits under field conditions is unknown.
The objective of this study was to investigate biannual soil drenches of a commercially available Trichoderma spp. product applied in spring and fall for ARR control in peach.
Establishment of Experiments
Experiments were established at two locations: one in Monetta, Saluda Co., SC; and one in Campobello, Spartanburg Co., SC. The site in Monetta contained sandy soil (>88% sand) whereas the site in Campobello contained clay soil (>40% clay). Both sites were in peach production for more than two generations and were severely infested with ARR, such that many mature trees had died from the disease as confirmed by the presence of mycelial fans under the bark of the lower trunk. Earlier generation cultivars were grown on Lovell and Halford rootstocks, which are susceptible to ARR. Symptomatic dead trees, including the root crown, were removed with a front-end loader within one week prior to planting the experimental trees. Secondary roots and some primary roots infected with Armillaria remained in the soil and served as inoculum source for this experiment. Experimental trees were used to fill in the empty spots along the rows between asymptomatic, mature trees.
In Monetta, 66 experimental trees on Guardian rootstock were planted within 3 rows of trees on 10 March 2007. Treatment (33) and control (33) trees were alternated within a row. Remedier WP (Isagro USA, Morrisville, NC), a biorational fungicide containing 2% Trichoderma asperellum strain ICC 012 and 2% T. gamsii strain ICC 080 (9) was applied as a soil drench on 13 March and 20 September 2007; 18 April and 2 October 2008; and 3 April and 9 September 2009 at 8 g formulated product in 2 gal of water. The same strains are also available in other formulations, including Tenet WP, BiotenWP, and Tenet T&O. Remedier WP and water were mixed thoroughly in a 5-gal bucket for about 2 min before drenching the trees (Fig. 1). Control trees received 2 gal of water. In Campobello, 82 experimental trees (43 control trees and 39 treatment trees) grafted on Halford rootstock were planted within 12 rows of trees on 10 March 2007. The Remedier WP drench was applied as described above on 22 March and 7 October 2007; 15 April and 7 October 2008; and 2 April and 18 September 2009. To avoid runoff, a rim (5 cm in height and 75 cm in diameter) was formed around the trees prior to drench application (Fig. 1A).
Trunk diameters for each treatment were calculated as the mean of at least 20 observations for each location. The evaluation dates were analyzed separately. The data for each evaluation date was subjected to analysis of variance (ANOVA) using Sigma Stat software (version 3.00; SPSS Inc., Chicago, IL). Separation of means was conducted using the Holm-Sidak method with α = 0.05. The objective of the statistical analysis for disease mortality data collected each year was to compare mean percentages among the treatments each year. An analysis of covariance (ANCOVA) statistical model was developed that included treatment effect, linear effect of year, and differences in the linear effects among the treatments. This model was used to estimate the mean percentage in each year, and then compare the mean percentages among the treatments. All calculations were performed using SAS (SAS Institute Inc., Cary, NC) procedure GLM with α = 0.05.
Effect of Trichoderma spp. Drenches on Tree Mortality Due to ARR
To our knowledge this is the first study examining the interaction of Trichoderma spp. and naturally occurring Armillaria involving living, woody host plants. Three consecutive years of spring and fall drenches of Remedier WP to peach tree roots did not protect the trees from ARR disease (Fig. 1B). Trees started to decline in both treatments of both locations in 2009 and by the end of the experiment in 2011, 56% of all control trees and 66% of Remedier WP-drenched trees at the Monetta location had died from ARR. At the Campobello location, 41% of all control trees and 56% of all Remedier WP-drenched trees had declined (Figs. 1 and 2). The presence of mycelial fans under the bark of the lower crown was confirmed in every dead tree. There was no statistical difference between the control and Remedier WP treatment in either location (Fig. 2). While decline of peach trees in a first-generation peach orchard is typically a slow process, losses of 50% and more in the first four to five years of establishment is not exceptional in replant sites. The use of a replant site with high inoculum levels in the soil may have imposed so much disease pressure that potential beneficial effects by Trichoderma in soil with little inoculum may have been overshadowed.
While Trichoderma spp. have been successfully used to combat root diseases of annual crops (13) and postharvest diseases of fruit and vegetable crops (20), few studies are available investigating their impact against root rots of perennial crops. Most studies focused on controlled in vitro experiments demonstrating antagonistic action of Trichoderma on root disease pathogens (2,10,17). Some established a beneficial interation of soil fumigation and suppressive action of Trichoderma (5,16), whereas others failed to demonstrate suppressive activity of Trichoderma and other biological control agents for ARR control in apple seedlings in the field (17). However, in the latter study the inoculum was artificially delivered in form of inoculum billets to roots near the soil surface representing an inoculum source much different from root pieces.
Depending on location we applied Remedier WP 3 and 12 days after the trees were planted within 5 min of making the solution. That is in contrast to recommendations for other formulations such as Tenet WP, which recommends to apply the product prior to planting and to prepare the solution 24 to 36 h prior to application. Whether this modification had a significant impact on the performance of Remedier WP is not known. However, it is unlikely that root infection occurred within weeks of planting considering that roots must first be established to find ARR inoculum sources. After all, infections on replant sites typically start 3 years after planting as is documented in both the control and Remedier WP treatments. Also, the documented growth promotion of treated trees suggests that the fungus likely colonized the root system.
Remedier WP Provided a Benefit for Tree Growth
Interestingly, biannual Remedier WP drenches provided a tree growth benefit in one location. Tree trunk diameter was higher in the Remedier WP treatment compared to the control treatment in the Campobello location starting with the fourth year after planting (P ≤ 0.05 for years 2010 and 2011). Not enough trees lived long enough in the Monetta location to validate this effect over the course of the entire experiment (Fig. 3). A similar promotion of plant growth was demonstrated in Pinus radiata seedlings following Trichoderma treatment (18). This effect may be due to an enhancement of root biomass as well as increased nutrient mobilization and uptake (13). The beneficial growth effects of Trichoderma spp. have been documented and were summarized recently (11,12). It would certainly be interesting to determine the potential impact of Trichoderma on peach tree yield, fruit quality, or general tree health.
Conclusions and Management Recommendations
In this study, T. asperellum and T. gamsii (Remedier WP formulated product) applied as a biannual drench did not reduce tree mortality due to ARR disease in two commercial peach replant sites and thus cannot be recommended to be used in soil with high ARR inoculum levels as part of an integrated or organic pest management strategy for ARR control.
This material is based upon work supported by NIFA/United States Department of Agriculture under project number SC-1000642. Technical contribution number 5960 of the Clemson University Experiment Station. We thank W. Bridges, Clemson University, for assistance in regard to the ANCOVA analysis; A. Amiri for helping plant the trees; and our grower collaborators for letting us use their orchards. We also thank Isagro USA for financial support.
1. Adaskaveg, J. E., Forster, H., Wade, L., Thompson, D. F., and Connell, J. H. 1999. Efficacy of sodium tetrathiocarbonate and propiconazole in managing Armillaria root rot of almond on peach rootstock. Plant Dis. 83:240-246.
2. Aytoun, R. S. C. 1953. The genus Trichoderma: its relationship with Armillaria mellea (Vahl ex Fries) Quel. and Polyporus schweinitzii Fr., together with preliminary observations on its ecology in woodland soils. Trans. Proc. Bot. Soc. Edinb. 36:99-114.
3. Beckman, T. G., Chaparro, J. X., and Sherman, W. B. 2008. 'Sharpe', a clonal plum rootstock for peach. HortScience 43:2236-2237.
4. Birmingham, W. H. 1931. Armillaria root rot of fruit trees. N. S. W. Dep. Agric. Plant Dis. Leaflet 18:1-4.
5. Bliss, D. E. 1951. Destruction of Armillaria mellea in citrus soil. Phytopathology 41:665-683.
6. Bliss, D. E. 1944. Controlling Armillaria root rot in citrus. Lithoprint#50. Univ. of California Agric. Exp. Stn., Berkeley, CA.
7. Cox, K. D., and Scherm, H. 2006. Interaction dynamics between saprobic lignicolous fungi and Armillaria in controlled enivronments: Exploring the potential for competitive exclusion of Armillaria on peach. Biol Control 37:291-300.
8. Elad, Y. 1996. Mechanisms involved in the biological control of Botrytis cinerea incited diseases. Eur. J. Plant Pathol. 102:719-732.
10. Guillaumin, J. J., and Dubos, B. 1984. Antagonism between Armillaria and Trichoderma. Etudes sur l'antagonisme entre Armillaire et Trichoderma. Association de coordination technique agricole.
11. Harman, G. E. 2011. Multifunctional fungal plant symbionts: new tools to enhance plant growth and productivity. New Phytol 189:647-649.
12. Harman, G. E. 2011. Trichoderma - not just for biocontrol anymore. Phytoparasitica 39:103-108.
13. Harman, G. E. 2006. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96:190-194.
14. Harman, G. E., Howell, C. R., Vieterbo, A., Chet, I., and Lorito, M. 2004. Trichoderma species: Opportunistic, avirulent plant symbionts. Nature Rev. Microbiol. 2:43-56.
15. Miller, R. W. 1994. Estimated peach tree losses from 1980 to 1992 in South Carolina: Causes and economic impact. Pages 121-127 in: Proc. 6th Stone Fruit Decline Workshop. A. P. Nyczepir, P. F. Bertrand, and T. G. Beckman, eds. Ft. Valley, GA.
16. Ohr, H. D., Munnecke, D. E., and Bricker, J. L. 1973. Interaction of Armillaria mellea and Trichoderma spp. as modified by methyl bromide. Phytopathology 63:965-973.
17. Raziq, F., and Fox, R. T. V. 2006. The integrated control of Armillaria mellea 2. Field experiments. Biol. Agric. Hortic. 23:235-249.
18. Reglinski, T., Rodenburg, N., Abad, P., Northcott, G. L., Ah Chee, A., Spiers, T. M., and Hill, R. A. 2011. Trichoderma atroviride promotes growth and enhances systemic resistance to Diplodia pinea in radiata pine (Pinus radiata) seedlings. Forest Pathol. doi: 10.1111/j.1439-0329.201000710.x.
19. Schnabel, G., Ash, J. S., and Bryson, K. P. 2005. Identification and characterization of Armillaria tabescens from the southeastern United States. Mycol. Res. 109:1208-1222.
20. Sharma, R. R., Singh, D., and Singh, R. 2009. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biol. Contr. 50:205-221.
21. Sivasithamparam, K., and Ghisalberti, E. L. 1998. Secondary metabolism in Trichoderma and Gliocladium. Pages 139-191 in: Trichoderma and Gliocladium. C. P. Kubicek and G. E. Harman, eds. Taylor and Francis, London, UK.
22. Williams-Woodward, J. L. 2004. 2003 Georgia Plant Disease Loss Estimates. Coop. Ext. Bull. 41., Univ. of Georgia, Athens, GA.