L. V. Edgington, R. A. Martin, G. C. Bruin, and I. M. ParsonsUniversity of Guelph, Ontario, Canada

Systemic Fungicides:A Perspective After 10 Years

Since Delp and Klopping first reportedon benomyl in Plant Disease Reporter(1), dramatic acceptance of Benlate byfarmers and widespread development ofother systemic fungicides have evolved.Thiabendazole and one or two antibioticswere reported as systemics as early as1964, but the real escalation in use of sys-temic fungicides began with the discoveryof carboxin and benomyl in the late 1960s.A compilation of fungicides currentlyused in the world lists 44 systemic (Table1) and 85 nonsystemic agents.

What "Systemic" MeansWe have investigated many of the new

systemic fungicides. Before analyzing theprogress and potential of these chemicals,however, we should clarify the word "sys-temic" as used by plant pathologists. Theword implies movement throughout theplant system, but this is misleading be-cause most systemic fungicides are onlypartially systemic in plants. With the ex-ception of several unregistered experi-mental fungicides that move "system-ically" into fruit, roots, buds, and otherplant organs along with the plant photo-synthates (sugars), the so-called systemicsare carried along with the transpirationstream. Leaves are the primary transpiringorgans, and movement within plants isfrom the soil to the expanded leaves. Veryyoung leaves, flowers, and fruit do nottranspire significant quantities of waterand therefore receive onlyminuteamountsof fungicides applied to soil or to seed.Actually, this is fortuitous, as the chancesof residues in fruit are minimal. Certainly,no more residues would be expected thanwith the old conventional "protectants"applied to the surface of plants.

Why is a fungicide systemic-or par-tially systemic? Before the discovery ofsystemics, fungicides were only protec-tants, remaining on the surface of plants.The protectants are toxic to many pro-cesses common in plants and fungi but donot enter the plant and therefore are notphytotoxic. Examples of protectants aremaneb (Dithane M-22), chlorothalonil(Bravo), and captan (Captan). Systemic

00191-2917/80/000002$03.00/001980 American Phytopathological Society

fungicides, however, penetrate the plantand are selectively toxic to processesunique to fungi. This selectivity is so spe-cific that among the hundreds of differentfungi attacking plants, only certain taxo-nomic groups of fungi are sensitive toeach particular systemic fungicide (Table1).

Selectivity of SystemicsFungicides of similar chemical struc-

ture are toxic to similar types of fungalorganisms (Table 1). Obviously, as anyfarmer knows, a particular crop is notplagued by only mildew, rust, orany othersingle disease. Researchers and industryhave been busy combining fungicides tocontrol pathogens in a particular crop.For example, Ridomil, a new systemicfungicide, looks very effective against lateblight of potato caused by Phytophthora.However, a farmer must also use manco-zeb or some other fungicide for earlyblight caused by. Alternaria solani, be-cause Ridomil is selectively toxic to Phy-tophthora. The particular niche for eachnew systemic in a combination is beingdeveloped for each crop and often eachgeographical region.

A systemic fungicide appears to be se-lective because it is toxic to only a singlesite within the fungus. This can cause prob-lems, since a single change in the funguscan result in resistance to the fungicide.The threat of resistance can be reduced,however, by using different systemic fun-gicides in combination or alternately in apest management program.

Use on SeedSeed treatments have always been the

most economical use of fungicides in pre-venting plant diseases in many crops.Protective fungicides, such as captan andthiram, control surfaceborne pathogensand, to a limited extent, protect germi-nating seedlings from soilborne patho-gens. The advent of systemic fungicideshas dramatically improved this picture:1) Systemics offer control against patho-gens within the seed as well as those onthe surface; 2) the systemic is taken intothe germinating seed and moves in anupward direction, protecting the seedlingduring development as well as after emer-

gence; and 3) much less fungicide is re-quired with systemics than with protec-tants.

Loose smut of cereals is an excellentexample of an internal seedborne diseasecontrolled by systemic fungicides. Bunt,which is borne by soil and on the seedsurface, was effectively controlled by gen-eral protectants, such as hexachloroben-zene and organic mercuries. These provedineffective, however, against the loose

100

50

a

Untreated Vitavax Sisthane Sisthane+Vitavax

Fig. 1. Control of barley seedling blightcaused by Blpolarls soroklnlana Is moreeffective with combined Sisthane andVltavax treatment than when eitherfungicide Is used alone.

100

0O= 50

NoSpray Zineb Bravo Ridomil

Number ofsprays 6 6 4Amount of 10.2 9.6 0.8chemical used (kg a.i./ha) per season

Fig. 2. The Incidence of downy mildew oflettuce caused by Bremla lactucae Is lowerafter biweekly applications of the systemicRidomll than after weekly sprayings withthe protectents zineb and Bravo. inaddition, the amount of Ridomil used issmaller than that of the other two chem-icals.

Plant Disease/January 1980 19

(Far left) Loose smut of barley, carried in the embryo of the seed, may be controlled bycarboxamide fungicides applied to seed (inset). (Left) Onion smut, indigenous in coolmuck soils, invades the germinating seedling but is difficult to observe in the green plant(arrow); plants on the left have been bleached with Carnoy's solution (3:1 ethanol:aceticacid) to allow accurate rating of smut infections. ProG ro seed treatment (inset) gives goodcontrol. (Middle) Barley seedling blight caused by soilborne and seedborne Bipolarissorokiniana is controlled most effectively with combined Sisthane and Vitavax (see Fig. 1).(Right) Benomyl applied in a band across the proximal end of cucumber leaves penetratesmore effectively when applied on the lower surface (BL) than when applied on the uppersurface (BU), as indicated by the mildew moving acropetally. (Far right) Downy mildew oflettuce caused by Bremia lactucae is controlled better with smaller amounts of thesystemic Ridomil than with the protectants zineb and Bravo (see Fig. 2).

smut organisms, which are carried in theembryo of the seed; furthermore, theywere environmentally undesirable andwere phased out. Von Schmeling andKulka (7) introduced the systemic car-boxin to control loose smut of barleycaused by Ustilago nuda. Carboxin isnow the most widely used seed-treatmentfungicide for small grains in Canada.

Benzimidazole systemic fungicides alsoprovide effective seed treatment. In 1978,white beans (Phaseolus vulgaris) in On-tario were threatened by a new delta raceof the anthracnose fungus Colletotrichumlindemuthianum. Maude and Kyle inEngland (4) had previously reported thatseed treatments with benomyl would con-trol seed-borne anthracnose. Research inOntario during 1977-1978 showed excel-lent control of seedborne anthracnosewith a benomyl or thiophanate-methylseed treatment in combination with cap-tan (to reduce seed decay) and diazinon(for seed corn maggot control). In 1978,experimental labels were granted in Can-ada for this combination and seed wastreated for over 40,000 hectares. A pro-tectant fungicide would never have suc-ceeded.

The control of onion smut shows howless fungicide may be required by system-ics than by protectants. The pathogenUrocystiscepulae is common in cool mucksoils and invades the first leaf (cotyledon)as it grows upward to the soil surface.In Canada, the protectant fungicidethiram may be applied as a soil granule at2.2 kg a.i. ha-' plus 0.8 kg a.i. ha - ' withseed for a total of 3 kg a.i. ha -'. ProGro(50% thiram and 30% carboxin, a sys-

20 Plant DiseaseNol. 64 No. 1

temic) may also be used to control onionsmut and is applied as a seed treatment at0.12 kg a.i. ha . Approximately 96% lessfungicide is required with ProGro, whichhas given consistently good disease con-trol since its registration in 1971.

The postemergence activity of systemicseed treatment against airborne patho-gens may have great potential. Rowell (6)first reported excellent postemergenceactivity with Indar against wheat brownrust (Puccinia recondita). In 1978, seedtreatment with triadimefon was reportedto give up to 100% control of yellow rustof winter wheat at the boot stage in Wash-ington (5); triadimefon is already regis-tered for use in Europe. Ethirimol hasshown excellent potential as a seed treat-ment for the control of powdery mildewof cereals in Europe (3).

Combining two or more fungicides canprovide broader, more complete controlof plant pathogenic fungi. Combined Sis-thane and carboxin is a very effective bar-ley seed treatment (Fig. 1). Sisthane givesexcellent control of seedling blight causedby Bipolaris sorokiniana and some con-trol of loose smut, while carboxin givesexcellent control of loose smut and slightcontrol of seedling blight. Another com-bination treatment of cereal seed, nowbeing tested in Europe, includes 1) meph-furoxam, a more fungitoxic analog of car-boxin, for smut control; 2) thiabendazolefor Fusarium control; and 3) Ridomil forPythium control. Numerous other com-binations of systemics are being tested forcontrol of several different diseases. Insome cases, broad-spectrum protectants,such as thiram, are also added.

Application to Soil

The fate of systemic fungicides in soil isnot different from that of protective fun-gicides; both are subject to inactivationby adsorption and degradation. Untilnow, therefore, application of systemicfungicides to soil has been limited primar-ily to use in greenhouses, where soildrenches are successfully used with beno-myl and thiabendazole to control Verti-cillium and Fusarium wilts of tomatoesand black root rot of cucumbers causedby Phomopsis sclerotioides (2). Soildrenches with dimethirimol, benomyl, orcarbendazim show potential for controlof such airborne diseases as powderymildew of cucumber caused by Sphaero-theca fuliginea.

In-furrow sprays and granular formu-lations are applied at planting to be in theproximity of the developing roots. Thisform of application is outstanding forrecently developed systemic compounds,such as Aliette, Ridomil, and prothiocarb,that are active against Pythium, Phyto-phthora, and fungi causing downy mil-dew. Ridomil as a 5% granular applied at0.5 kg a.i. ha gives excellent control ofPhytophthora root rot of soybean (R.Pitblado, personal communication).

Soil injection of systemic fungicidescan be used against numerous diseases ofperennials but is still an uncommon prac-tice. Incorporation into seedbeds and intoseed blocks for transplants also lookspromising for some Oomycete fungicidesagainst Pythium damping-off in vege-tables and downy mildew of lettuce causedby Bremia lactucae.

Root dips of transplants in solutions ofAliette controls red stele of strawberrycaused by Phytophthora fragariae (8).

The addition of systemic fungicides toirrigation systems can save time andequipment, especially via trickle irrigationdistribution, which allows accurate regu-lation of time and space. In Japan, the fun-gicide IBP is applied as granules to irri-gation water to control rice blast causedby Pyricularia oryzae (9); because theactive ingredient is only moderately sol-uble in water (500 yg/ml), the granulespersist for up to 3 wk.

Much has yet to be done to find theright formulations and application meth-ods to avoid phytotoxicity and adsorptionto soil and to give long enough action forthe desired control while not being overlypersistent in the environment. The newOomycete fungicides are a step in theright direction; they are very soluble inwater, readily taken up by the roots, andeffective in low concentrations.

Application by Follar SprayUptake of systemic fungicides applied

as foliar sprays by the cuticle of plants isseriously limited. The outer surface waxesprotect plants from excessive desiccationand, conversely, make it difficult for fun-gicides dissolved in water to enter leaves.In addition, the high surface tension ofaqueous sprays prevents systemics fromentering stomata. The cuticle on the un-derside of leaves is easier to penetrate,but sprays are usually applied to theupper surface. Most systemics are rel-atively insoluble in water, and if appliedas wettable powders (WP), as protectants

Plant Disease/January 1980 21

are, they remain as a suspension on theleaf surface, unable to traverse the cuti-cular barrier. The fungicide must dissolvein the spray droplet and diffuse into thecuticle, all before the droplet dries on theleaf surface. Once the droplet has dried,very little further uptake occurs.

To improve cuticular uptake, the pes-ticide industry has switched to formula-tions that are either emulsifiable concen-trates (ECs) or oil emulsions. In 1967,before systemics, 6.5% of the fungicidesreported in the APS Fungicide-Nemati-cide Report were formulated as ECs. In1977, with many systemics in use, thenumber of EC formulations reported hadincreased to 28.7%. Systemics formulatedas ECs give better disease control, prob-ably because the fungicides are soluble inthe organic phase of the EC and can rap-idly partition into the water of a spraydroplet and then into the waxy cuticle.Even with this improved uptake, however,only about 5% of a systemic applied toleaves enters the plant, with most remain-ing on the leaf surface and acting as a pro-tectant.

Addition of 1% spray oil has also beenused to enhance uptake. The oil possibly"solubilizes" the cuticle by being misciblewith the waxes or cutin. Because uptake isincreased, less fungicide is required. InCanada, for example, benomyl as a WP isapplied to apples for scab control at 0.28kg a.i. ha- ' with oil and at 0.63 kg a.i. ha- 1

without oil.Usually, most of a chemical sprayed on

a crop is deposited on the upper surface ofthe leaves, and pathogenic fungi growingon the lower surface, such as downy mil-dew, are poorly controlled. Systemicfungicides, however, can move trans-laminarily, being taken up on one side ofthe leaf and translocated to the other.Another advantage of systemic over pro-tective fungicides is a curative postinfec-tion action. By entering the plant tissue, asystemic fungicide can eradicate patho-gens shortly after infection. Because theneed for constantly protecting the foliageis avoided, less fungicide is used, mini-mizing stress on the environment. An-other advantage of systemic fungicides iscompensation for poor coverage becauseof redistribution within the plant.

The incidence of downy mildew oflettuce caused by B. lactucae in Ontario,Canada, at harvest time after a spray pro-gram with protective and systemic fungi-cides is shown in Fig. 2. The protectantszineb and chlorothalonil were sprayedweekly and gave poor control. The sys-temic Ridomil was applied biweekly andgave much better control, with about 92%less fungicide being used. The need forless systemics than protectants can beobserved in numerous spray programs.For instance, in Ontario, the recommen-

ded spray for apple scab caused by Ven-turia inaequalis is 5.4 kg a.i. ha- ' for theprotectant maneb and 0.28 kg a.i. ha-' forthe systemic benomyl. The systemic fen-arimol is even more active, requiring only

22 Plant DiseaseNol. 64 No. 1

0.065 kg a.i. ha -1.In the near future, we expect some sys-

temic fungicides will become availablethat are also translocated downward inthe plant. The results of Zentmyer (9),who was able to control root rot of avo-cado caused by Phytophthora cinnamomiwith foliar applications of Aliette andRidomil, are a hopeful indication that weare entering a new era in disease controlwith downward-moving systemic fungi-cides.

SummaryThe number of systemics has increased

during the last decade to compriseapprox-imately one-third of the total fungicides inuse. The systemics are much more selectivethan the protectants in the spectrum ofdiseases controlled. Because of selectivetoxicity to distinct fungal groups and de-velopment of resistant fungal strains, a se-rious look at fungicide combinations andmanagement programs is required. Boththe amount of fungicide needed and thefrequency of application are markedlyreduced with systemics compared withprotectants. Formulations have alsochanged from WPs to ECs to improvecuticular uptake of systemic fungicides.Current systemics are transported up-ward in plants. The development of fun-gicides that move downward from a foliarapplication to control root pathogens isjust beginning and requires further inves-tigation.

Literature Cited

L. DELP, C. A., and H. L. KLOPPING.1968. Performance attributes of a newfungicide and mite ovicide candidate.Plant Dis. Rep. 52:95-99.

2. FUCHS, A., A. L. HOMANS, and F. W.de VRIES. 1970. Systemic activity ofbenomyl against Fusarium wilt of pea andtomato plants. Phytopathol. Z. 69:330.

3. MARSH, R. W. (ed.). 1977. Page 401 inSystemic Fungicides, 2 ed. LongmanGroup Ltd.: Edinburgh.

4. MAUDE, R. B., and A. M. KYLE. 1971.Seed dressings with systemic fungicidesfor the control of seed-borne fungal patho-gens. Rep. Natl. Veg. Res. Stn. (LongAshton, U.K.), 1970, p. 106.

5. RAKOTONDRADONDA, R., and R. F.LINE. 1978. Control of Puccinia strii-formis and Puccinia recondita by treatingwheat seed with systemic fungicides.Phytopathol. News 12:144. (Abstr.).

6. ROWELL, J. B. 1976. Control of leaf ruston spring wheat by seed treatment with4-N-butyl-1,2,4-triazole. Phytopathology66:1129-1134.

7. SCHMELING, B. von, and M. KULKA.1966. Systemic fungicidal activity of 1,4-oxathiin derivatives. Science 152:659.

8. WILLIAMS, D. J., B. G. W. BEACH,D. HORRIERE, and G. MARECHAL.1977. LS 74-783, a new systemic fungicidewith activity against Phycomycete dis-eases. Pages 565-573 in Proc. 1977 Br.Crop Prot. Conf.-Pests and Diseases.

9. ZENTMYER, G. A. 1978. New organicfungicides for control of Phytophthoraroot rots. Page 362 in Proc. 3rd Int. Congr.Plant Pathol., Minchen.

L. V. Edgington

After obtaining his Ph.D. at the Uni-versity of Wisconsin in 1956, Dr.Edgington worked at the Connecti-cut Agricultural Experiment Stationi nvestigati ngfu ng icides. Since 1966,he has been at the University ofGuelph, Ontario, Canada, where heis doing research on fungicides andteaching a course on the bioactivityof fungicides, herbicides, and in-secticides. The coauthors of thisarticle are students of his.

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