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The role of kinetosome-associated organelles in the attachment of encysting secondary zoospores ofSaprolegnia ferax to substrates

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Summary

Electron and fluorescence microscopy were used to identify organelles involved in attachment of secondary zoospores ofSaprolegnia ferax as they were transformed into secondary cysts. When secondary zoospores were exposed to 1.0% peptone in the absence or presence of a substrate, they began to encyst. If substrates were present when encystment was induced, the groove surface of the secondary zoospores adhered to them. The first event in attachment was secretion of contents of the kinetosome-associated organelle (K-body), which was typically oriented with the tubule-filled cavity positioned toward the cell surface of the groove region in the zoospore. The tubules which contained carbohydrates became coarsely granular, the matrix became more fibrous, and the shell remained along the membrane concavity that was formed as the K-body fused with the plasma membrane.

Five minutes later, a cyst coat appeared, and cysts were not readily dislodged from a substrate. The concavity was no longer found, presumably because it had evaginated; but a layered pad of adhesion material was between the cyst coat and substrate. The layers of the adhesion pad corresponded to the structure of the matrix of K-bodies. As with the tubules of the K-body, the coarsely granular portion at the edge of the pad stained for carbohydrates. Similarly, the lectins WGA and GS-II labeled with fluorescein stained the rim of the adhesion pad on cysts, indicating the presence of glycoconjugates containing N-acetylglucosamines. Because globular areas near the kinetosomes and groove of zoospores (where K-bodies were located) also bound WGA and GS-II, K-bodies contained the same carbohydrates as the adhesion pad. We conclude that K-bodies function in the attachment of encysting zoospores to substrates as the cell differentiates. The tubular portion of the K-body matrix contains carbohydrates which might assist in the adhesion process.

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Abbreviations

D:

dictyosome

EV:

encystment vesicle

F:

flagellum

C:

cyst

CC:

cyst coat

Con A:

concanavalin A

GS-II:

Griffonia simplicifolia lectin

K:

K-body

Kt:

kinetosome

M:

mitochondria

N:

nucleus

NB:

nuclear beak

PC:

peripheral cisterna

PV:

peripheral vesicle

S:

shell region of K-body matrix

SBA:

soybean agglutinin

R 3:

anteriorly directed triplet rootlet

R 8:

posteriorly directed octet rootlet

WEV:

water expulsion vacuole

WGA:

wheat germ agglutinin

References

  • Bacic A, Williams ML, Clarke AE (1985) Studies on the cell surface of zoospores and cysts of the fungusPhytophthora cinnamomi: nature of the surface saccharides as determined by quantitative lectin binding studies. J Histochem Cytochem 33: 384–388

    Google Scholar 

  • Bartnicki Garcia SN, Hemmes DE (1976) Some aspects of the form and function of oomycete spores. In: Weber DJ, Hess WM (eds) The fungal spore. Wiley, New York, pp 593–639

    Google Scholar 

  • Beakes GW (1983) A comparative account of cyst coat ontogeny in saprophytic and fish-lesion (pathogenic) isolates of theSaprolegnia diclina-parasitica complex. Can J Bot 61: 603–625

    Google Scholar 

  • — (1987) Oomycete phylogeny: ultrastructural perspectives. In: Rayner ADM, Brasier CM, Moore D (eds) Evolutionary biology and the fungi. Cambridge University Press, Cambridge, pp 405–421

    Google Scholar 

  • Bimpong CE, Hickman CJ (1975) Ultrastructural and cytochemical studies of zoospores, cysts, and germinating cysts ofPhytophthora palmivora. Can J Bot 53: 1310–1327

    Google Scholar 

  • Cerenius L, Olson LW, Lange L, Soderhall K (1984) The secondary zoospore ofAphanomyces astaci andA. laevis (Oomycetes, Saprolegniales). Nord J Bot 4: 697–706

    Google Scholar 

  • Gilboa-Garber N, Nizkahi L (1980) Estimation of nonspecific lectinmediated staining of glutaraldehyde-fixed cells. Experientia 36: 1416–1417

    Google Scholar 

  • Grove SN, Bracker CE (1978) Protoplasmic changes during zoospore encystment and cyst germination inPythium aphanidermatum. Exp Mycol 2: 51–98

    Google Scholar 

  • Gubler F, Hardham AR (1988) Secretion of adhesive material during encystment ofPhytophthora cinnamomi zoospores, characterized by immunogold labelling with monoclonal antibodies to components of peripheral vesicles. J Cell Sci 90: 225–235

    Google Scholar 

  • Hardham AR (1985) Studies on the cell surface of zoospores and cysts of the fungusPhytophthora cinnamomi: the influence of fixation on patterns of lectin binding. J Histochem Cytochem 33: 110–118

    Google Scholar 

  • —, Suzaki E (1986) Encystment of zoospores of the fungus,Phytophthora cinnamomi, is induced by specific lectin and monoclonal antibody binding to the cell surface. Protoplasma 133: 165–173

    Google Scholar 

  • Hausmann K (1978) Extrusive organelles in protists. Int Rev Cytol 52: 197–276

    Google Scholar 

  • Heath IB, Greenwood AD (1970) Wall formation in the Saprolegniales II. Formation of cysts by the zoospores ofSaprolegnia andDictyuchus. Arch Mikrobiol 75: 67–79

    Google Scholar 

  • Hibberd DJ (1970) Observation on the cytology and ultrastructure ofOchromonas tuberculatus sp. nov. (Chrysophyceae), with special reference to the discobolocysts. Br Phycol J 5: 119–143

    Google Scholar 

  • Holloway SA, Heath IB (1974) Observations on the mechanism of flagellar retraction inSaprolegnia terrestris. Can J Bot 52: 939–942

    Google Scholar 

  • — — (1977) An ultrastructural analysis of the changes in organelle arrangment and structure between the various spore types ofSaprolegnia. Can J Bot 55: 1328–1339

    Google Scholar 

  • Hoch HC, Mitchell JE (1972) The ultrastructure of zoospores ofAphanomyces euteiches and of their encystment and subsequent germination. Protoplasma 75: 133–138

    Google Scholar 

  • Lehnen LP (1988) Development and cytochemistry of kinetosome associated organelles inSaprolegnia fernax. Ph.D, Dissertation, Miami University, Oxford, OH, USA, 171 p

    Google Scholar 

  • —, Powell MJ (1988) Cytochemical localization of carbohydrates in zoospores ofSaprolegnia ferax. Mycologia 80: 423–432

    Google Scholar 

  • Lunney CZ, Bland CE (1976) Ultrastructural observations of mature and encysting zoospores ofPythium proliferum de Bary. Protoplasma 90: 119–137

    Google Scholar 

  • Manton I, Clarke B, Greenwood AD (1951) Observations with the electron microscope on a species ofSaprolegnia. J Exp Bot 2: 321–331

    Google Scholar 

  • Meier H, Webster J (1954) An electron microscope study of cysts in theSaprolegniaceae. J Exp Bot 5: 401–409

    Google Scholar 

  • Nyhlen L, Unestam T (1975) Ultrastructure of the penetration of the crayfish integument by the fungal parasite,Aphanomyces astaci, Oomycetes. J Invertebr Pathol 26: 353–366

    Google Scholar 

  • Paktitis S, Grant B, Lawrie A (1986) Surface changes inPhytophthora palmivora zoospores following induced differentiation. Protoplasma 135: 119–129

    Google Scholar 

  • Pickett-Heaps JD (1967) Preliminary attempts at ultrastructural polysaccharide localization in root tip cells. J Histochem Cytochem 15: 442–455

    Google Scholar 

  • Powell MJ, Lehnen LP, Bortnick RN (1985) Microbody-like organelles as taxonomic markers amongOomycetes. Biosystems 18: 321–333

    Google Scholar 

  • Sing VO, Bartnicki-Garcia S (1975 a) Adhesion ofPhytophthora palmivora zoospores: electron microscopy of cell attachment and cyst wall fibril formation. J Cell Sci 18: 123–132

    Google Scholar 

  • — — (1975 b) Adhesion ofPhytophthora palmivora zoospores: detection and ultrastructural visualization of concanavalin A receptor sites appearing during encystment. J Cell Sci 19: 11–20

    Google Scholar 

  • Svensson E (1978) Interactions between a parasitic fungus,Aphanomyces astaci, Oomycetes, and its crayfish host. I. Motility, encystment, attachment and germination of the zoospore. Acta Univ Ups Abstr Uppsala Diss Sci 457: 1–18

    Google Scholar 

  • Swift JA, Saxton CA (1967) The ultrastructural location of the periodate-Schiff reactive basement membrane of the dermoepidermal junctions of human scalp and monkey gingiva. J Ultrastruct Res 17: 23–33

    Google Scholar 

  • Toth R (1976) The release, settlement and germination of zoospores inChorda tomentosa (Laminariales). J Phycol 12: 222–233

    Google Scholar 

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Lehnen, L.P., Powell, M.J. The role of kinetosome-associated organelles in the attachment of encysting secondary zoospores ofSaprolegnia ferax to substrates. Protoplasma 149, 163–174 (1989). https://doi.org/10.1007/BF01322988

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