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Development of Haustorium in Taphrina Maculans Butler 262 Development of Haustorium in Taphrina maculans Butler M. S. Pavgi and Rajendra Upadhyay1 College of Agriculture, Banaras Hindu University, India Received August 17, 1966 The species of Taphrina have been known to grow subcuticularly on the host surface or intercellularly within the host tissues. Taphrina maculans Butler inciting leaf spot of turmeric (Curcuma longa L.) grows both subcuticularly and intercellularly. This pathogen being a semiobligate foliicolous parasite, produces haustoria penetrating the leaf cells of this host. A haustorium is known to be the principal food absorbing organ of highly adopted parasitic fungi obligate parasites, obtaining nourishment from the host cells without killing them. Elaboration in its form is an evidence of high degree of adoptation by the haustorial parasite in establishing maximum contact with the host protoplasm. Variations in size and shape of the haustorium from the button-like type of Albugo candida (Pers.) Kuntze (de Bary 1863) to a digitately branched structure of Erysiphe graminis DC. (Smith 1900) have been reported in literature. The haustoria are too nonspecific in their developmental pattern to form a basis for classification or a distinction between allied genera (Fraymouth 1956). Development of a membraneous sheath around the haustorium has been reported earlier by several workers, but the nature of its origin and function are not yet precisely known. Fraymouth (1956) suggested that the sheath was laid down by the host cell and composed of a modified cellulose-callose. Ehrlich and Ehrlich (1963) observed presence of a sheath of naked protoplasm outside the haustorial membrane in Puccinia gvaminis tritici Erikss. and E. Henn. and believed it to have formed through contact of oozed out protoplasm of the host cell. The nature of selective or nonspecific permeability of this membrane is also not known . Appressed contact of the haustorium with host nucleus has been frequently reported in the rust fungi. Sappin-Trouffy (1892, 1896) first pointed out the association of rust haustoria with nuclei of the penetrated host cells. Colley (1918) frequently noticed the host cell nuclei dented by the haustoria of Cronartium ribicola J. C. Fisch. Allen (1928) observing as many as 82% haustorium: host nucleus contacts in Puccinia striiformis West . suggested a definite affinity between the 2 organelles, although Rice (1935) believed it a variable phenomenon . The question as to which of these members initiated such a contact has remained controversial . Allen (1928) regarded it possible only through movement of the host nucleus towards the haustorium , while Cunningham (1931) reported evidence on the growth of the haustorium progressing towards the host cell nucleus. The order Taphrinales includes parasitic species which were considered earlier as obligate in their parasitism, but success to grow them on artificial media has now established their facultative nature. Development of hasutoria in this group of fungi , mostly a character of obligate parasites, is an indication of tendencies towards high adoption . The present study was undertaken to study in detail the haustorial development in T. maculans and its parasitic relation with the host. Material and methods Young uninfected leaves of turmeric plants grown in isolated chambers were smeared with the culture suspension of T. maculans (Pavgi and Upadhyay 1964) and incubated in moisture 1 Award of a Jr . Research Fellowship by the Council of Scientific and Industrial Research, New Delhi is gratefully acknowledged. 1967 Development of Haustorium in Taphrina maculans 263 chambers. Peelings from the inoculated leaf surface taken at different intervals after 24hrs incubation were observed for spore germination, initial infection processes and progressive development of the haustorium. Leaf pieces collected from these inoculated plants as well as from the field at progressive stages of development were fixed in FAA (rect. spirit 50ml, formalin 10ml, glacial acetic acid 5ml and dist. water 35ml) and chrom-acetic (weak) sol. (10% aqueous chromic acid sol. 2.5ml, 10% aqueous acetic acid 5ml, and dist. water 35ml), washed thoroughly and preserved in 70% alcohol. Free hand sections lightly stained with aniline blue, acidic carbol fuchsin and Heidenhain's hematoxylin (Johansen 1940) and microtome sections (8-10ƒÊ) stained with Heidenhain's hematoxylin and counterstained with light green or Orange G were prepared as necessary for comparative or complementary observations. Observations Developmentof haustorium. Entry of the pathogen into a host cell is effected by an aseptate hyphal peg from a germinating blastospore or subcuticular or inter cellular hyphae. The tip of the peg or the hypha bulges a little with accumulation of dense protoplasm after entering the host cell (Fig. 1) and soon bifurcates into 2 short branches (Fig. 2), which again bifurcate in turn further (Figs. 3, 4). New branches also arise from the point of bifurcation of the stem branching dichotomously further (Figs. 5, 6, 7). The haustorial base slightly thickens with branching and growth (Figs. 5, 7). Numerous short branches resulting from the profuse dichotomous branching increase the size of the haustorium imparting it a 'cystolith'-like appearance (Figs. 8, 9, 10). Continued branching at short intervals makes it a compact mass of a single unit (Figs. 11, 12), finally obliterating identity of individual branches (Fig. 13). The length of its stem is variable. In some haustoria it is short and stumpy (Figs. 4, 7, 10) and in others it is rather slender and long (Figs. 6, 8). The haustorium is hyaline in the beginning but changes to pale amber yellow with maturity. Members of Peronosporales (Fraymouth 1956), Erysiphales (Smith 1900) and Uredinales (Rice 1927) develop branched haustoria, but none is reported to possess a multiple dichotomously branched haustorium as in T. maculans. Morphologically it has attained a new form not duplicated in any other fungus species. Haustoria in epidermis. Formation of haustoria in the epidermal cells is conveni ently observed in peelings taken from inoculated/infected leaf surfaces. A thin slimy coat around the wall of the blastospores appears to help them adhere firmly to the waxy leaf surface. It has been repeatedly observed that culture spores smeared onto glass slides adhere them firmly on drying and resist washing away even by a water jet. The infection peg from the germinating blastospore penetrates directly the cuticle and subsequently the epidermal cell. On reaching inside it branches terminally forming the haustorial initial (Fig. 17). The germinating blastospore on branching into a functional haustorium in the epidermal cells grows further into a branched subcuticular mycelium (Figs. 18, 19, 20). The hyphal branches coming in contact with fresh epidermal cells penetrate through the walls similarly develop ing haustoria in them. Epidermal cells in surface view show them penetrated by a subcuticular net of hyphal branches (Figs. 21 to 25) as also in vertically 264 M. S. Pavgi and R. Upadhyay Cytologia 32 Figs. 1-16. Development of haustorium in Taphrina maculans. 1, 2, haustorial peg penetrat ing an epider mal cell and bifurcating at the tip. 3-5, further bifur cation and dichotomous branching. 6-8, young hausto ria borne on long and short stems. 9-12, progressive stages in haus torial develop ment with paired nuclei in the stem. 13-16, mature haustorium giving 'cys tolith'-like appearance. 14, young haustorium ensheathed by a membrane originating from the stem base. Note membraneous sheath in all cases. 15, epi dermal cell in surface view with hausto rium from subcuticular hypha. Note 2 nuclei in the mother cell. sectioned cells (Fig. 29). The hyphae travelling down in the leaf through the radial epidermal walls also send haustoria sideways in the neighboring epidermal cells (Figs. 30, 31). They are sent in from any one or all sides of the cell by the enveloping hyphae, often enclosing more than 1 haustorium in a cell (Fig. 26). The hyphae generally grow in the intercellular spaces sending haustoria sideways in the neighboring cells. Frequently they are observed to permeate walls of the epidermis and also penetrate the cells forming haustoria in them. 1967 Development of Haustorium in Taphrina maculans 265 Figs. 17-34. Haustorial de velopment in the host leaf in surface and transverse views. 17-20, development and dichotomous bran ching of a haus torium from the germinating blas tospore and sub cuticular hyphae in close proximity with the host nucleus. 21, two haustoria close to the nucleus borne on long and short hyphal branches. 22, haustorium enveloping the host nucleus. 23-26, stretching and swinging the host nucleus on proto plasmic strands by 2-3 haustoria from opposite sides. 27, 28, host nuclei misshapen by haustorial contact. 29, haustorium from a subcuticular hypha in transverse view. 30, 31, pene tration by peg and haustorial forma tion in epidermis through side walls. 32-34, T. S. leaf with and without hypodermic show ing haustoria in epidermis, hypo dermis and palisa de. Note intralame llar haustorial development. Haustoria in mesophyll. Further mycelial growth brings it in contact with the hypodermis, where it ramifies sending in flanking haustoria both in the epidermis and the hypodermis (Figs. 32, 34). Their growth between the radial walls of the hypodermis is restricted only to the upper side of the palisade cells (Fig. 34). Not infrequently the haustoria are formed in cells of the palisade, but never in the depth further. In the absence of a well differentiated hypodermis, they are often observed in the palisade cells of the mesophyll (Fig. 33). When the lower leaf surface is infected, only 1-2 layers of spongy parenchyma are permeated by the hyphae and haustoria. 266 M. S. Pavgi and R. Upadhyay Cytologia 32 Two types of wall penetration by the hyphae are observed. In one of them the haustorial peg produced by the intercellular hyphal branch penetrates the cell directly, while in the other type the hypha first establishes in the wall of the invaded cell before entering it to form a haustorium.
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