FINE STRUCTURE OF MYCOTA

XI. OCCURRENCE OF THE GOLGI DICTYOSOME IN THE HETEROBASIDIOMYCETEPUCCINIA PODOPHYLLI

ROYALL T. MOOREElectron Microscope Laboratory, University of California, Berkeley, California

Received for publication 24 June 1963

ABSTRACT

MOORE, ROYALL T. (University of California,Berkeley). Fine structure of mycota. XI. Oc-currence of the Golgi dictyosome in the hetero-basidiomycete Puccinia podophylli. J. Bacteriol.86:866-871. 1963.-The Golgi dictyosome isreported for the first time in the subclass Hetero-basidiomycetidae in the rust Puccinia podophylliSchw. It is observed that the dictyosome appearsto be limited to primordial cells, particularlythose nearest the host, and does not occur in theaeciospores. In comparison with the Golgi sys-tems of plant and animal cells, the Golgi complexof P. podophylli is found to be more similar tothose of the latter. Also discussed is the distribu-tion of the Golgi complex in fungi described inpublished reports and the need for more suchreports so that the range of its variation anddistribution may be established.

The Golgi dictyosome has only recently beendemonstrated in the fungi. First described in theAscomycete Neobulgaria pura (Moore and Mc-Alear, 1962, 1963), it has most recently beendescribed in Peronospora rmnshurica (Peytonand Bowen, in press) and Pythium debaryanum(Hawker, 1963), both biflagellate Phycomycetes,and in the Homobasidiomycete Armillaria mellea(Roskin, Snyder, and McAlear, in preparation).The following communication relates the occur-rence of what is believed to be an example of theGolgi system in the Heterobasidiomycete Pucciniapodophylli, a representative of the other Basidio-mycete subclass.

MATERIALS AND METHODS

Young aecia of P. podophylli Schw. wereexcised from the lower stem of Podophyllumpeltatum L. (Berberidaceae) collected from thefield. (Reference material from the same specimen

has been deposited in the Cornell UniversityPlant Pathology Herbarium, CUP 45416.) Thesewere prefixed for about 10 min in 2% aqueousunbuffered KMnO4, then fixed in buffered OS04for 3 to 5 hr, dehydrated in an ethanol series, andembedded in a methacrylate mixture (Moore,1962). Sections cut with a diamond knife wereexamined in a Siemens Elmiskop I electron mi-croscope.

RESULTS

Figure 1 shows a cell of the aecial primordiumcontiguous with a thick-walled epidermal cell(E, E) of the host. A Golgi dictyosome (G) withnumerous marginal vesicles (X) is prominentnear the fungal nucleus (N). Above this are whatappear to be two smaller complexes.

Figure 2 is a similar plane of section at a highermagnification. The dictyosome membranes dis-play frequent swellings at their margins (arrows),and adjacent vesicle aggregations (X) are con-spicuous.

Figure 3 presents a somewhat tangential sec-tion of a Golgi complex proximate to a nucleus(N). The fungal wall (W) is identified.

Figure 4 is interpreted as a section cut approxi-mately perpendicular to the vertical stack ofsaucer-shaped sacs that form the dictyosome.The three dictyosome membrane aggregates (G)are believed all to belong to one complex. Thegreat accumulation of Golgi vesicles (X) spaciallyis probably at the inner region of the complex(similar to those in Fig. 1 and 3).

DISCUSSIONThe Golgi system, thought classically to occur

only in animal cells, owes its present delimitationsto the early studies of zoological fine structure.These established the following criteria: (i) stacksof flattened sacs-the "fingerprint" of the dictyo-some; (ii) propinquity of the dictyosome to the

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FIG. 1. Contiguity of fungal and host epidermal (E, E) cells. A Golgi dicytosome (G) and vesicles (X)are prominent near the nucleus (N). Scale line = 1 ,; X 20,000.

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FIG. 2. Dictyosome lamellae showing blebbing (arrows) and adjacent vesicle clusters (X). Scale line = 1

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FIG. 3. Tangential section through a Golgi complex near a nucleus (N). W', the fungal cell wall. Scaleline = 1 IA; X 60,000.

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FIG. 4. Section through the Golgi apparatus approximately perpendicular to the plane of stacking; G,dictyosome; X, vesicles. Scale line = 1 p; X 30,000.

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GOLGI DICTYOSOME IN P. PODOPHYLLI

nucleus; (iii) the apparent blebbing off of smallvesicles from the margin of the dictyosome; (iv)membranes that are smooth, i.e., ribosome-free.

Criteria i and iv appear to be invariable:the dictyosome is, ipso facto, the defining attributeof the Golgi complex, and in no examples ofosmium-fixed material have ribosomes beenreported on Golgi membranes. An exception tocriterion iii was reported by iMoore and McAlear(1963) in the fungus Neobulgaria in which mar-ginal vesicles were not observed. Plant cells tendto be exceptions to criterion ii. In these cells, thedictyosomes generally appear to be rather scat-tered in the cytoplasm. Also, the dictyosomes asmost frequently observed are more compact andmore numerous, and the quantity of marginalvesicles is sparser than is generally characteristicof the dictyosomes of animal cells. From thenumerous electron microscopic studies of planttissues during the past several years, it now isquite evident that the Golgi system is as widelyoccurring in plant cells as in animal cells.The same is not yet true for the fungi. The

Golgi dictyosome for these organisms was firstreported from the monotypic discomycete N.pura (MIoore and MIcAlear, 1963). This stillremains our only example from the Ascomycetes.However, as mentioned above, there are nowseveral reports of the Golgi apparatus from thePhycomycetes. All of these, curiously enough,are from the biflagellate series, a series uniquelycharacterized by cellulose in the hyphal walls(J. M. Aronson, personal communication) and aseries which Bessey (1942) believed to be phylo-genetically linked with the Vaucheriaceae of theyellow-green algae. The first report of the Golgidictyosome in the Basidiomycetes was made byRoskin et al. (in preparation) from A. mellea.The present report is believed to be the secondfor this class.The thallus of P. podophylli is composed of

disarticulated cells (Moore, in press), and theGolgi formation is observed most frequently inthe several layers of cells nearest the host. Atthe outer face of the aecium, aesciospores areproduced. These are dikaryotic, filled withstorage vesicles, and bounded by a thick, wartywall. No Golgi-like membranes have been ob-served in them, and their appearance is quitesimilar to the aeciospores of Uromyces caladii(Moore and McAlear 1961).

The observed membrane complex in P. podo-phylli complies with the first three criteria. (In-formation on the fourth criterion is precluded bythe permanganate fixation.) Its micromorphologyappears most similar, broadly speaking, to thedictyosomes observed in animal cells; that is,the lamellae forming the dictyosome are quitebroad, the number of marginal vesicles is large,and the complex occupies the perinuclear region.Further, there is seldom more than one fullydeveloped complex per cell.From this r6sum6 of all the reports of the

occurrence of the Golgi dictyosome in the fungi,it is quite evident that it is still rather a noveltyin the Eumycota. It is, therefore, important thatas examples of the Golgi system are encounteredin these organisms they be reported so that therange of the micromorphology and the distribu-tion of the organelle may be established. Froman accumulation of such information, there mayperhaps be derived in the future a clearer under-standing of the phylogenetic position of the fungi.

ACKNOWLEDGMENTS

The technical assistance of Lloyd Thibodeauand Philip Spencer of our Laboratory is grate-fully acknowledged.

This investigation was supported by Post-doctoral Fellowships 9197-02 and 2 F2 AI-9197-04from the National Institute of Allergy and Infec-tious Diseases, U.S. Public Health Service; JamesH. McAlear, sponsor.

LITERATURE CITED

BESSEY, E. A. 1942. Some problems in fungusphylogeny. Mycologia 34:355-379.

HAWKER, L. E. 1963. Fine structure of Pythium debar yanum Hesse and its probable significance.Nature 197:619.

MIOORE, R. T. 1962. Fine structure of mycota. 1.Electron microscopy of the discomyceteAscodesmis. Nova Hedwigia 5:262-278.

MOORE, R. T., AND J. H. MCALEAR. 1961. Finestructure of mycota. 8. On the aecidial stageof Uromyces caladii. Phytopathol. Z. 42:297-304.

MOORE, R. T., ANI) J. H. McALEAR. 1962. Charac-terization of the Golgi dictyosome of thefungus Neobulgaria pura. Intern. Conf. Elec-tron Microscopy, 5th 2:UU-7.

MOORE, R. T., AND J. H. McALEAR. 1963. Finestructure of mycota. 4. The occurrence of theGolgi dictyosome in the fungus Neobulgariapura (Fr.) Petrak. J. Cell Biol. 16:131-141.

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