Post-plant application of soil solarization for tree crops

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Eris C. Tjamos

Laboratory of Plant Pathology Agricultural University of Athens Votanikos 118 55, Athens, Greece

Introduction

Olive, pistachio nut, avocado and Prunus trees are among the most common Verticillium-susceptible perennials. Furthermore, root rot diseases of trees caused by Rosellinia necatrix in apples and dry roof rot of cirrus caused by Fusarium solani are of special research interest as far as their control is concerned. Trees with Verticillium wilt in young Prunus orchards, especially almond and peach, tend to overcome the disease alter an acute phase and escape new infections (22). Pistachio nut trees also suffer less, several years after establishment. Olive trees, however, possess a rather superficial root system and are almost always vulnerable to the pathogen, especially in irrigated groves of susceptible cultivars. Transient symptom development of Verticillium wilt of olive and apricot is possibly due to the inactivation of the pathogen in the annual ring (14, 22). Diseased trees are also able to recover and escape the disease after pruning, provided that future reinfestation through the roots can be avoided. Reinfestation of the root system may be a prerequisite for the development of new symptoms. Thus, the phenomenon of natural recovery of Verticillium-affected olive trees, also reported by other workers (15), could be mainly attributed to the fluctuation of populations of V. dahliae and to the possible antagonistic activity of the soil microflora. Providing that pathogen propagules are eliminated and/or fungal antagonists are selectively surviving and increasing in the rhizosphere soil, recovery or symptom remission should be expected in the treated tree (2). Therefore, any procedure able to reduce inoculum level of the pathogen in the soil could contribute to the recovery of diseased trees in established orchards. Microsclerotia of V. dahliae are vulnerable to soil solarization (13, 17, 19).

This review paper is mainly focused on the possibility of exploiting the potential of post-planting application of soil solarization for the control of serious vascular or root rot diseases and presents evidence referring to the successful or failed application of the method.

Mode of Application of Soil Solarization in Established Orchards.

Attempts to evaluate soil solarization as a post-plant treatment started in California. Ashworth and Gaona (1) demonstrated that solarization could be applied either as a continuous soil tarping by covering the whole area of the pistachio nut groves, regardless of the existence of Verticillium-affected or healthy trees, or as partial mulching of tree rows with uncovered strips of 0.50 or 1.20 m remaining between the trees. Almost contemporarily, Tjamos (17) in Greece studied the effectiveness of single application of the method around individual Verticillium- affected olive trees.

Soil Solarization and Verticillium Wilt

Verticillium Wilt of Olive Trees. - Field experiments to determine the effectiveness of soil solarization on individual trees were carried out in olive orchards in several regions of Greece between 1980-83 (17). Soil around the diseased trees was covered with transparent polyethylene sheets (6 m x 6 m) during the hot summer period. Recovery or reduction in symptom expression was demonstrated in the treated trees as compared to the untreated controls. A large-scale experiment designed to further evaluate the effectiveness of soil polarization of individual trees in controlling Verticillium wilt of olive trees over a three-year period, was conducted in Magnesia County, Greece, in a field with over 700 10-15 year old olive trees. This study involved analysis of the effect of a single treatment on the natural population of the pathogen, estimation of recovery or symptom remission of olive trees, and detection and quantification of fungi antagonists to V. dahliae in soil. Finally, the longevity of the effect was investigated and the involvement of rhizosphere heat-tolerant antagonists of V. dahliae in the effectiveness of the method was examined. Soil tarping applied in July, 1984, which followed a sufficient tree irrigation to the saturation level (300-350 I water/tree), lasted for at least two months after which sheets began to disintegrate and split apart. The maximum and minimum values of soil temperatures recorded in the unshaded parts around treated trees were usually 9-12C higher than those of the uncovered soil in the control trees. Maximum soil temperatures recorded during the first two weeks of August in covered soil, reached 58C and 48C at depths of 10 and 20 cm, respectively, as compared to 36C in the uncovered soil at 20 cm. Natural populations of V. dahliae microsclerotia were almost non-detectable following soil solarization. Numbers of viable micro-sclerotia recorded one and two years later in the same trees had increased slightly but in general remained significantly lower in treated compared with untreated trees. The actual mean figures were 1.3 + 1, 4.3 + 1.6 and 7.6 + 3 for solarized and 6.7 + 1.6, 13.3. + 1.6 and 10 + 3.6 microsclerotia for untreated soil per 15 g soil in January 1985, 1986, and 1987, respectively.

The effectiveness of soil solarization in symptom remission or recovery of Verticillium-affected olive trees was evaluated by assessing disease incidence of treated and untreated control trees in July 1985, January 1986, July 1986 and January 1987. Foliar symptoms were evaluated on a 04 scale based on the percentage of the affected foliage, where 0=healthy tree; I up to 25 percent (mild symptoms); 2=up to 50 percent (intermediate symptoms); 3=up to 75 percent (severe symptoms) and 4=80 percent diseased foliage (tree nearly dead to dead). After solarization, up to 87 percent of trees recovered, while with natural recovery only up to 50 percent of untreated trees recovered for trees with the same initial disease index rated as 1. The distribution of disease severity among all four categories of the disease scale was greater in untreated trees compared with the symptom development in solarized trees. Although recovery due to solarization (47.0-58.8 percent) did not exceed natural recovery (45.5-61.4 percent) of the untreated trees, disease severity was more pronounced and occurred over a greater range of disease classes in non-solarized trees compared with the solarized trees with an initial disease index of 2. Both recovery and symptom remission were significantly higher in solarized (30-70 percent) compared to the untreated trees (37.5-50.0 percent) with an initial index of 3. The beneficial effect of individual soil solarization was expressed both as an increased recovery and symptom remission in three successive growing seasons.

A beneficial effect of soil solarization on the survival and fluctuation of populations of Talaromyces flavus, an antagonist of V. dahliae (11) was demonstrated in the experimental olive grove. Population determinations carried out in rhizosphere soil of the treated or untreated control trees in spring 1985, showed a sharp difference in numbers of T. flavus in favour of the solarized trees. Further estimations conducted in October 1985, January 1986, May 1986 and May 1987 clearly demonstrated the positive effect of soil solarization on the constant occurrence of the antagonist in solarized soil. The pronounced, long-lasting effect of soil solarization on the survival, increase and maintenance of Verticillium-antagonistic population was evident in the rhizosphere soil of 10 sampled treated trees. It was also apparent that values in 10 untreated trees fell drastically in the following years. Estimations of T. flavus populations carried out in 30 randomly selected solarized, and 30 untreated control trees in January 1986, May 1986 and May 1987, indicated that solarization significantly affected survival and maintenance of populations of T. flavus for two to three years following solarization.

As for the effect of soil solarization on populations of Aspergillus terreus, colonies of this potential antagonist were frequently found in petri dishes containing the selective medium used to estimate populations of T. flavus (19). Counts of A. terreus were also made in May 1986 and 1987. A. terreus survived solarization and was detected in exceptionally high numbers both in treated and untreated trees.

Verticillium Wilt of Pistachio Nut Trees. - Ashworth and Gaona (1), studying the effectiveness of soil solarization against V. dahliae in established six-year old pistachio nut trees in California, mulched the soil surface of the groves with transparent polyethylene sheets. They also covered orchards in rows with tarped strips. They reported reduction of V. dahliae microsclerotia down to undetectable levels. They found that inoculum levels of 30, 60, 90 and 120 cm were 4.6, 0.9, 0.6, 0.4 microsclerotia (msc) per gram of air-dried soil, respectively, in control untreated trees, while they reduced numbers to undetectable amounts of soil in treated trees. They demonstrated that continuous coverage was much more effective compared with mulching in strips for reducing symptom development. Finally, they reported that high soil temperatures in mulched soil did not result in any visual detrimental effect on the root system.

Verticillium Wilt of Almond Trees. - Symptom development of Verticillium wilt is rather acute in young almond trees in newly established orchards. Katan in Israel (personal communication) enumerated V. dahliae microsclerotia in continuously solarized almond orchards and found that both added or natural V. dahliae populations were almost eradicated to the soil depth of 70 cm, while eradication was complete at 50 cm. Due to the low natural inoculum level, no further evaluation of the method was attempted, since neither symptom development nor differentiation between treated and untreated trees were documented.

Verticillium Wilt of Avocado Trees. - Verticillium wilt of avocado is a rather severe disease. Experiments to evaluate soil solarization as a continuous postplant treatment were carried out in Israel. It was determined (Katan personal communication) that shade effect by the tree canopy is a limiting factor in eradicating Verticillium microsclerotia added to soil (maximum destruction 90 percent) two months after the removal of the plastic.

There was no evidence related to the longevity of a single application, because trees pruned to reduce the shade effect were drastically affected by frost injury.

Soil Solarization and Root Rot Diseases

Rosellinia Root Rot of Apple Trees. - White root rot of fruit trees caused by Rosellinia necatrix constitutes another serious disease warranting evaluation of the effectiveness of soil solarization. Recent research reported by Freeman et al. (5, 6) demonstrated a long-term effect of the method in controlling the disease in established apple orchards. The control of the disease involves destruction of natural inoculum to a depth of 30 cm, while partial or complete pathogen eradication was achieved in solarized, but shaded areas.

There are two most important points of this interesting research. One is related to the safe replanting in those sites where the disease incidence was lethal to the trees. This is because the fungus is totally destroyed. The second point refers to the effectiveness of solarization in reducing disease index to zero over a three-year period with minor symptoms during the fourth year. The mortality, however, of the untreated trees reached 100 percent four years after a single application of the technique.

The longevity of the effect could be attributed to the near-eradication of the pathogen and to the well documented phenomenon of induced suppressiveness following solarization (4, 6, 7, 8, 9, 20). Due to excessive irrigation in the mulched soil, anaerobic conditions could be created in the root system of the treated trees but plants tend to recover soon after the removal of the plastic.

Fusarium Root and Collar Rot of Citrus Trees. - Bourbos and Skoudridakis (3), in their preliminary experiments in Crete to evaluate soil solarization for controlling citrus dry root rot, mainly caused by Fusarium solani, reported the possibility of applying the method in individually diseased grapefruit trees. They also speculated on the possible role of the antagonistic mycoflora of the soil in their effort to explain the longevity of the effect.

Phytophthora cinnamoni of Avocado Trees. - Pre-planting application of soil solarization in avocado orchards infested with Phytophthora cinnamomi clearly demonstrated that the method has a detrimental effect on the survival of the pathogen in the soil (12). Application of solarization to established avocado trees (Katan, personal communication) showed that P. cinnamomi natural populations are very sensitive to soil solarization and could be reduced to zero. It must be emphasized, however, that the root system of avocado does not function properly under stress imposed by the anaerobic conditions of moist, heated and mulched soils. There is a strong tendency for the appearance of iron deficiency symptoms in solarized trees, but no heavy damage of the root system is observed, since trees recover shortly after the removal of the polyethylene. Phycomycetes, such as Phytophthora, are able to easily recontaminate the soil following application of conventional soil disinfestation methods. It is possible, however, that soil solarization could favour survival and involvement of Phytophthora antagonists and prevent or delay reinfestation of the soil by the pathogen.

Improvements in Post-Plant Application of Soil Solarization

Data clearly demonstrated that soil solarization of individual trees could be a practical and economical measure for the control of Verticillium wilt in irrigated orchards. Soil solarization effect could be further exploited by:

- earlier applications of the technique (e.g. in May);

- combining solarization with the addition of biological preparations of fungal antagonists to V. dahliae (21);

- application of antagonists (e.g. T. flavus) particularly in the shaded areas of the treated trees;

- benzimidazole derivatives that could be added during or after solarization, since V. dahliae is very sensitive to benomyl;

- carefully selected herbicides that could be added at low doses in order to eradicate weeds and increase effectiveness of the method in shaded areas;

- antagonistic bacteria such as fluorescent Pseudomonas or Bacillus spp. that could be added to the soil through the drip irrigation system.

Discussion and Conclusion

A practical and effective approach to Verticillium wilt in established orchards of susceptible trees remains a remote hope. This is particularly true for perennial crops which harbour the pathogen in the xylem, such as in the case with V. dahliae. Destruction of microsclerotia of V. dahliae occurred in fully solarized soils of pistachio nut groves in California (1). Preliminary evidence suggested satisfactory recovery of olive trees from Verticillium wilt after soil solarization of individual trees in Greece (17).

Results from a large-scale experiment (20) demonstrated that natural populations of microsclerotia of V. dahliae could be drastically reduced or eliminated in individually solarized olive trees. In contrast to the solarized soil, the untreated soil showed rather constant populations of V. dahliae throughout the three-year trial. Comparison of olive data with findings in globe artichoke, another perennial host susceptible to V. dahliae, showed that soil solarization prior to the establishment of the artichoke plantation had a pronounced and durable effect on the elimination of fungal propagules, and on the prevention of soil reinfestation (19). A long-term effect of soil solarization has been reported for Fusarium wilt of cotton (8). In olive orchards, it is plausible to anticipate that microsclerotia of V. dahliae hidden in soil pockets in the shaded part of the tree, could escape the effects of solarization, be revitalized and contribute to the increase of the populations and to reinfect the trees. It may also be envisaged that olive leaves from diseased olive twigs might eventually contribute to the reinfestation of the groves, since leaf petioles and laminae are colonized by V. dahliae (18). The inability of soil solarization to fully destroy the fungus in shaded areas of the soil could account for the gradual increase of microsclerotia populations during the third year following soil solarization. Involvement of weed hosts susceptible to V. dahliae (16) could be prevented from contributing to the population increase by using herbicides.

Application of soil solarization to individual trees resulted in a more pronounced recovery of those trees with initially mild wilt symptoms. A less strong tendency for symptom remission was evident in trees with initially intermediate or severe symptoms. Both recovery and symptom remission exceed natural recovery, which still occurred but in a significantly lower amount than with the solarized trees.

Recovery or symptom remission in diseased olive trees reflects a definite beneficial and long-term effect of the treatment. Soil solarization had also a potential for long-term control of Verticillium wilt of pistachios for 1218 months following soil mulching (1).

The involvement of heat-resistant antagonists of V. dahliae in the longterm effect of soil solarization on globe artichokes has already been postulated (19). T. flavus (10, 11) and A. terreus (19) survive solarization and increase in the soil of trees treated with solarization, compared with untreated control trees. Numerical differences in populations of V. dahliae could mean that fungal antagonists are partially involved in delaying increase of V. dahliae and prolonging the effectiveness of the method. The biological action of solarization could be effective in individual tree sites because the application of the method is restricted to a small soil area.

References

1. Ashworth, L. J., Jr. and S. A. Gaona. 1982. Evaluation of clear polyethylene mulch for controlling Verticillium wilt in established pistachio nut groves. Phytopathology 72:234-246.

2. Ashworth, L. J. Jr., O. E. Huisman, R. G. Grogan and D. M. Harper. 1976. Copper induced fungistasis of microsclerotia of Verticillium albo-atrum and its influence on infection of cotton in the field. Phytopathology 66:970-971.

3. Bourbos, V. A. and M. T. Skoudridakis. 1989. Study of the control possibilities of the citrus dry rot. p. 104-109. In: Proceedings of the 2nd International Meeting on Mediterranean Tree Crops.

4. Elad, E., J. Katan and I. Chet. 1980. Physical, biological and chemical control integrated for soilborne diseases in potatoes. Phytopathology 70:418-422.

5. Freeman, S. and J. Katan. 1988. Weakening effect on propagules of Fusarium by sublethal heating. Phytopathology 78:1656-1661.

6. Freeman, S., A. Sztejnberg, A. Shabi and J. Katan. 1990. Long-term effect of soil solarization for the control of Rosellinia necatrix in apple. Plant Disease (In Press).

7. Greenberger, A., A. Yogev and J. Katan. 1987. Induced suppressiveness in solarized soils. Phytopathology 77:1663-1667.

8. Katan, J., G. Fisher and A. Grinstein. 1983. Short and long-term effects of soil solarization and crop sequence on Fusarium wilt of cotton in Israel. Phytopathology 73:1215-1219.

9. Katan, J., J. E. DeVay and A. Greenberger. 1989. The biological control induced by soil solarization. p. 493-499. In: Vascular wilt diseases of plants. E.C. Tjamos and C.H. Beckman (eds.) Springer-Verlag.

10. Marois, J. J., D. R. Fravel and G. C. Papavizas. 1984. Ability of Talaromyces flavus to occupy the rhizosphere and its interaction with Verticillium dahliae. Soil Biology and Biochemistry 16:381-390.

11. Marois, J. J., S. A. Johnston, M. T. Dunn and G. C. Papavizas. 1982. Biological control of Verticillium wilt of eggplant in the field. Plant Disease 66:1166-1168.

12. Pinkas, Y., A. Kariv and J. Katan. 1984. Soil solarization for the control of Phytophthora cinnamomi: thermal and biological effects. Phytopathology 74:796 (Abstr.).

13. Pullman, G. S., J. E. DeVay and R. H. Garber. 1981. Soil solarization effects on Verticillium wilt of cotton and soil-borne populations of Verticillium dahliae, Pythium spp., Rhizoctonia solani and Thielaviopsis basicola. Phytopathology 71 :954-959.

14. Taylor, J. B. and N. T. Flentje. 1968. Infection, recovery from infection and resistance of apricot trees to Verticillium albo-atrum. New Zealand Journal of Botany 61 :417-426.

15. Thanassoulopoulos, C. C., D. A. Biris and E. C. Tjamos. 1979. Survey of Verticillium wilt of olive trees in Greece. Plant Dis. Reptr. 63:936-940.

16. Thanassoulopoulos, C. C., D. A. Biris and E. C. Tjamos. 1981. Weed hosts as inoculum source of Verticillium in olive orchards. Phytopath. Medit. 20:164- 168.

17. Tjamos, E. C. 1983. Prospects for controlling Verticillium wilt of olive trees by soil solarization. P. 15. In: Hellenic Congress on Plant Diseases and Pests, Athens, Greece, p.15 (Abst.).

18. Tjamos, E. C. and D. Botseas. 1987. Occurrence of Verticillium dahliae in leaves of Verticillium wilted olive trees. Canadian J. of Pl. Path 9:86 (Abstract).

19. Tjamos, E. C. and E. J. Paplomatas. 1988. Long-term effect of soil solarization in controlling Verticillium wilt of globe artichokes in Greece. Pl. Pathol. 37: 507-515.

20. Tjamos, E. C., D. A. Biris and E. J. Paplomatos. 1990. Recovery of olive trees with Verticillium wilt following individual application of soil polarization in established olive orchards. Plant Disease (In Press).

21. Tjamos, E. C., L. Skretis and H. Loumakou. 1990. Establishment of applied or increase of natural Verticillium dahliae antagonists in solarized soils. In: 5th International Verticillium Symposium, Leningrad, USSR, June 1990 (Abstr.).

22. Wilhelm, S. and J. B. Taylor. 1965. Control of Verticillium wilt of olive through natural recovery and resistance. Phytopathology 55:310-316.


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