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«Association of Aphanomyces cladogamus with severe root rot of pansies By C h a r l e s D r e c h s l e r (Horticultural Crops Research Branch, ...»

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Association of Aphanomyces cladogamus with severe

root rot of pansies

By C h a r l e s D r e c h s l e r (Horticultural Crops Research Branch, Agricultural Research Service, United States Department of Agriculture,

Beltsville, Maryland, U.S.A.).

With plate XL—XVI.

B u i s m a n (1927), working in the Netherlands, was the first

investigator to mention having isolated an Aphanomyces from

decaying roots of pansies (Viola tricolor L.). The fungus she obtained

looked to her very similar to my A, euteiches ( J o n e s and D r e c h s l e r, 1925), but in her inoculation experiments it did not attack pea (Pisum sativum L.) roots. Prom lack of time she was unable to ascertain experimentally whether her Aphanomyces was the cause of an acute root rot affecting pansies in her experimental garden. Soon afterwards M e u r s (1928), also working in the Netherlands, carried out inoculation experiments which showed that the Aphanomyces from pansy roots was capable of attacking roots of both V. tricolor and V. cornuta L. He concluded accordingly that the fungus was the cause of an acute root rot of pansies in Holland. In supplementary inoculation experiments he determined further that A. euteiches from diseased pea roots would not infect either V. tricolor or V. cornuta.

As M e u r s, like B u i s m a n, considered the pansy fungus to be morphologically identical with A. euteiches despite some differences in growth and parasitism he designated it as A. euteiches P. P. 2. The same designation he applied likewise to cultures of Aphanomyces isolated by him from roots of spinach (Spinacia oleracea L.) and Arabis alpina L.

The association of an Aphanomyces with severe disease in Violas came to my attention more than 20 years ago ( D r e c h s l e r, 1934), when a generous collection of affected pansies was received for determination of whatever injurious fungi might be present. These diseased specimens were taken on April 29, 1933, from a garden in Mount Rainier, Maryland, in which pansies had been severely affected with root rot for several years. Their leaves, though well developed and with little discoloration, showed wilting in noticeable degree.

Their stems appeared of normal color and undiminished firmness.

Their luxuriant root systems, after being washed free of soil, were also found of normal firmness, and the root epidermis everywhere appeared free of any discoloration or external blemish. Yet when the root systems were viewed under bright illumination against a white background each showed an extensively and conspicuously darkened core. On removal of the outer cortical sheath the vascular cylinder was exposed to view as a deep red or orange-red strand. Mounts prepared from thin slices or thin fragments of affected roots showed the parenchyma tissue to be virtually undamaged and without any general invasion by bacteria. Along and within the central cylinder, however, numerous oospores were found distributed rather uniformly, though here also, bacteria, the usual escort of phycomycetous invaders, were for the most part not discernible. Many of the oospores, being wedged in the unyielding fabric of the stele, were found constrained into various elongated ellipsoidal shapes. Regardless of modifications in outward form all oospores that had reached a mature resting condition showed in the parietal protoplasmic layer surrounding the central reserve globule the geometrical arrangement of largish sphaeroidal granules familiar in the oospores of many saprolegniaceous fungi. The thorough-going distribution of the oospores, and the frequent absence of any other visible microorganism in the roots, gave very convincing reason for considering the oomycete present as the agent responsible for the wilting of the leaves. When portions of diseased root were planted on Petri plates of maize-meal agar mycelia of an Aphanomyces grew out promptly and consistently. No other organism of a likely pathogenic character appeared in the resulting cultures.

The garden from which the incipiently wilting specimens were taken still showed on inspection 20 days later (on May 19, 1933) many pansy plants of erect posture and generally healthy aspect (PI. XI, A, left, right; B, right). At distances of only 20 or 30 centimeters from some of these healthy individuals neighboring plants were found wilted down beyond recovery (PI. XI, A, middle) though the leveled foliage and stems in some instances still seemed alive at the time.

Often, again, the wilting in closely neighboring plants was found more advanced, with the prostrated stems, leaves, and flowers drying out and shrivelling (PI. XI, B, middle). In some borders a row of 3 or 4 badly withered plants (PI. XII, A, center) were found flanked by plants that showed only incipient wilting (PL XII, A, lower left, upper right). The final stage of destruction came to light in instances where denuded.'stenig and peduncles lay extended on the ground intermingled with shrivelled remains of leaves and flowers (PI. XII, B, lower middle).

In the more severely affected pansy plants the basal portion of the stem always showed pronounced injury from softening, discoloration or decay of its cortex. At the ground line little frequently would be left of the stem except the denuded core. Above the denuded portion the cortical layer of the stem was often softened for a distance of 5 to 25 mm. The cortical layer of the roots below the denuded portion of the stem likewise showed more or less extensive softening and discoloration. Owing to the conspicuous injury they displayed externally, plants in the later stages of attack had little the appearance of succumbing to internal infection along the woody stele. When portions of softened stem or root were now bathed in sterile water for 5 to 15 hours, and after being pressed between sheets of filter paper were transferred to Petri plates of maize-meal agar, mycelia soon grew out that yielded pure cultures not only of an Aphanomyces but also of several species of Pythium.

Since 1933 pansy plants with severe root rot have been received repeatedlyfrom home gardens in and near Washington, D. C. As the specimens would seem usually to have been gathered in late stages of decline it was not possible, as a rule, to determine whether attack had been initiated with invasion by an Aphanomyces along the central stele. Most often the plants were broken off near the ground level, having apparently been pulled up without much care. Nevertheless, by cutting pieces of affected stem tissue from these ineptly collected specimens, and bathing them in sterile water for several hours before placing them on maize-meal agar plates, it was usually possible to obtain pure cultures of the familiar Aphanomyces as well as of several species of Pythium.

Despite the habitual recurrence of severe root rot in some gardens, especially in years of liberal spring rainfall, this disease would yet seem wholly absent in many pansy beds in and near Washington, D. C. The rather extensive borders on the grounds of the Plant Industry Station, near Beltsville, Maryland, that have been planted with pansies for more than 15 years in succession, have so far shown only a few examples of severe root rot. The seedlings set out in these borders were always grown in unsterilized soil except in one year when sterilized soil was employed incidentally. In some wet years when the pansies in these borders were dug up after the middle of May to be replaced by other ornamentals better adapted to the hot summers of the region, examination of their well-developed root systems revealed only very meager injury in that the epidermis here and there was darkened or discolored in rather vaguely delimited areas. Such discoloration is not uncommon on pansy roots in and near Washington, D. C., often appearing to some extent even when only moderate rainfall has come early in spring. It has no evident association with wilting or discoloration of leaves and stem, and is not known to usher in the severe type of root decay. Prom the superficially discolored portions of root numerous isolations of Pythium ultimum Trow, P. debaryanum Hesse, P. mamillatum Meurs, P. vexans De Bary, P. oliyandrum Drechsl., and P. acanthicum Drechsl. have been obtained, but no isolations referable to any species of Aphanomyces. Nor were any Aphanomyces cultures obtained from the softened stems and roots of the pansy specimens originating from Washington, D. C., in 1938 (D r e c h s 1 e r, 1949) that yielded isolations of the distinctive P. violae Chesters and Hickman (1944).

Although the gardens from which came the diseased pansies that yielded Aphanomyces cultures varied moderately with respect to texture and fertility of the soil, all the Aphanomyces cultures obtained from pansies in the Washington area during 20 years resembled one another closely in growth habit and morphology. The figures (Pi.

XIII, A—H; PI. XIV, A—H) showing 16 units of sexual reproductive apparatus formed in a culture isolated from a diseased pansy taken from a home garden in Arlington, Virginia, late in May, 1939, illustrate tolerably the more usual variations in make-up characteristic also of many other isolations. Thus a generally satisfactory agreement in make-up is evident when the 16 reproductive units are compared with homologous units (PL XV, A—G) formed in a culture isolated from a pansy plant found succumbing to root rot in a garden near Bethesda, Maryland, on May 23, 1953. The assortment of sexual apparatus produced by the isolation obtained from Virginia and the assortment produced by the isolation originating 14 years later from a locality 10 kilometers away both reveal obvious parallelism with the 13 sexual reproductive units earlier presented in figures (D r e c h sl e r 1929, p. 330, 331) illustrating the tomato-root fungus on which was based the original description of A. cladogamus.

In the pansy fungus, as in the tomato-root fungus, the hypha (PI.

XIII, A—C: a; PL XIV, A—D: a; PL XV, A, a) bearing the oogonial stalk often has no close or visible connection with the hypha (PL XIII, A—C: b; PL XIV, A—D: b; PL XV, A, b) bearing the antheridial branches. Yet very often, again, the oogonial stalk (PL XIII, D—H: a;

PI. XIV, E-—F: a; PL XV, B—G: a) originates from the same hypha as the antheridial branch (PL XIII, D—H: b; PL XIV, E—F: b; PL XV, B—G: b) the resulting monoclinous relationship being, indeed, a feature especially characteristic of the species. Sometimes the hypha that gives off the oogonial stalk (PI. XIV, G, a; H, a) gives off two antheridial branches each of which may supply one (PL XIV, H, b, c) or more (PL XIV, G, b, c) male cells. In rather compact monoclinous reproductive units the total length of the hyphal elements connecting oogonium and antheridium may scarcely exceed 100 or 125 \L (PL XIII, G; PL XIV, F; PL XV, F) while in rangier monoclinous units the oogonial stalk, antheridial branch, and connecting portion of parent hypha may have an aggregate length of approximately 250 (j, (PL XIV, G, a, c; H, a, c; PL XV, C, a, b). Short diverticulations and spurs are often borne here and there on the sexual branches so that even 22 Sydowia, Vol. VIII. 1954. Nr. 1/6. 337 reproductive units with only one or two antheridia sometimes will present a fairly intricate appearance. The generally bulbous shape of the antheridium is often modified, much as in the tomato-root fungus, by the presence of a lateral hyphal appendage or of a distal prolongation. The oogonial stalk in diclinous (PI. XIII, A, C; PL XIV, D; PL XV, A) as also in monoclinous (PL XIII, D; PI. XIV, E; PL XV, D;

units sometimes winds spirally around an antheridial branch, or, again, an antheridial branch may wind noticeably around the oogonial stalk (PL XIII, G; PI. XIV, F), but in comparison with the extensive enwrapment of oogonia by antheridial branches the entwinement of one sexual branch by the other is not usually a conspicuous feature in the development of reproductive apparatus under the surface of agar substratum.

Two hundred oogonia selected at random in maize-meal agar plate cultures of the Bethesda isolation gave measurements for diameter, expressed in the nearest integral number of microns, with a distribution as follow: 21 p., 2; 22 p., 9; 23 p, 13; 24 ^, 27; 25 ^, 46;

26 p, 32; 27 «. 29; 28 p., 19; 29 ^ 11; 30 p., 8; 31 p., 3; 35 p., 1; and the mature oospores contained in them — all of correct internal organization — gave measurements for diameter distributed thus: 17 ^ 2;

18 p, 6; 19 ^ 19; 20 ^ 41; 21 ^ 61; 22 p, 43; 23 ^ 18;35 ^ 1; and the From the two sets of measurements averages of 25.8 p. and 21.0 ^ were computed for oogonial diameter and oospore diameter, respectively.

Varying from 0.5 to 1.2 p., the supplementary measurements for thickness of oogonial envelope averaged 0.8 ^ while the measurements for thickness of oospore diameter, with a range from 1.2 to 2.1 jx, gave an average of 1.6 p. Measurements for diameter of the reserve globule here ranged from 8.2 to 13.5 ^ and averaged 10 \i. The main dimensions of oogonium and oospore in the pansy fungus thus would appear to agree satisfactorily with the corresponding dimensions in isolations of Aphanomyces cladogamus from roots of tomatoes and of spinach and flax ( D r e c h s l e r, 1954).

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