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Reproductive Biology and Evidence for Water Dispersal of Teliospores

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Reproductive Biology and Evidence for Water Dispersal of Teliospores Mycologia, 92(4), 2000, pp. 754-763. © 2000 by The Mycological Society of America, Lawrence, KS 66044-8897 Reproductive biology and evidence for water dispersal telisporesof in Chrysomyxa weirii, a microcyclic spruce needle rust Patricia E. Crane1 second nuclear division occurs in each cell during Department of Biological Sciences, University of basidiospore formation. Both nuclei move into the Alberta, Edmonton, Alberta, T6G 2E9, and Northern basidiospore, and subsequently divide one or more Forestry Centre, Canadian Forest Service, Natural times. The two-celled basidium, the fragmenting ba- Resources Canada, 5320-122 Street,Edmonton, Alberta, T6H 3S5 Canada sidium and other unusual forms of germination, and teliospore dispersal have not been previously report- Yasuyuki Hiratsuka ed in the genus Chrysomyxa. Northern Forestry Centre, Canadian Forest Service, Key Words: basidium, cytology, microcyclic rust, Natural Resources Canada, 5320-122 Street, Picea, splash dispersal, Uredinales Edmonton, Alberta, T6H 3S5 Canada Randolph S. Currah Department of Biological Sciences, University of INTRODUCTION Alberta, Edmonton, Alberta, T6G 2E9 Canada Among the North American species of the genus Chrysomyxa,C. weiriiJacks. is unique in being autoe- Abstract: Chrysomyxaweirii (Uredinales) is the only cious and microcyclic. The rust fungus forms red- autoecious, microcyclic species of Chrysomyxaoccur- dish-orange, tonguelike telia in early spring on ring in North America. The telia form on second-year spruce needles of the previous year, and the infection needles of spruce, causing premature needle loss. spreads to young needles on newly opened buds be- The morphology of the telia was studied in herbari- fore the old infected needles drop off. The natural um specimens from diverse locations, and the telio- host range for C. weirii includes Picea engelmannii spore germination, nuclear condition, and reproduc- Parry, P glauca (Moench) Voss, P mariana (Mill.) tive biology of fresh collections were studied on mi- B.S.P., P rubens Sarg., and P sitchensis (Bong.) Carr. croscope slides and on artificially and naturally in- (Arthur 1962, Savile 1950, Ziller 1974). Although its fected host tissue using light and scanning electron occurrence is more sporadic than most other spruce microscopy. Basidiospore production was infrequent needle rusts in boreal and subalpine forests (Peter- in mature sori, but teliospores dispersed readily in son 1961), it has an extensive range that includes water and germinated to produce a two-celled basid- northern Oregon, Idaho, western Montana, Washing- ium and two basidiospores. The two cells of the ba- ton, South Dakota, British Columbia, Alberta, Sas- sidium could also separate to form two sporelike cells katchewan, Manitoba, New Brunswick, Northwest that could produce germ tubes, or the teliospore pro- Territories, Yukon Territory, as well as the southern duced a long hyphalike promycelium. The type of Appalachian Mountains (Weir 1923, Boyce 1943, Pe- germination was influenced by temperature. The terson 1961, Ziller 1974). In recent years C. weirii has ready dispersal of teliospores in water and their pres- been introduced to blue spruce (P. pungensEngelm.) ence on the surface of current-year needles confirms nurseries in the northeastern United States (Ver- that they function as diaspores. The distribution pat- mont, New Hampshire, Pennsylvania) (Pawuk 1971, tern of this rust and the elongated, smooth, thin- Bergdahl and Smeltzer 1983, Merrill et al 1993), walled spores that are held rigidly together until wet where serious outbreaks affecting up to 100% of new suggest a water-dispersal mechanism. A cytological needles on the lower branches have been recorded study showed that the vegetative hyphae are mostly (Bergdahl and Smeltzer 1983). There is also one re- monokaryotic. Dikaryotization and karyogamy occur port of C. weirii on P. schrenkiana Fischer & Meyer in the cells at the base of the telium and result in from south-central Asia (Kuprevich and Tranzschel teliospores with one large nucleus. During germina- 1957). tion, the teliospore nucleus migrates into the basidi- As in other members of the genus Chrysomyxa,the um, where it divides once before a septum forms. A teliospores of C. weirii are thin-walled and catenulate, and they germinate without a period of dormancy. Accepted for publication February 14, 2000. However, this single stage provides few systematic 1 Email: [email protected] characters for comparison with other Chrysomyxaspe- 754 CRANE ET AL: CHRYSOMYXAWEIRII REPRODUCTION 755 cies, most of which are heteroecious and macrocyclic, fluorescent illumination using a Zeiss Axiophot Photomi- with their telia on various genera of Ericaceae. There- croscope. In some cases slides of germinating teliospores fore a study of the entire life cycle of C. weirii was were dried on a slide warmer (55 C) and stained later (Im- azu et al 1989). To the results with DAPI, of undertaken in a search for characters that might elu- verify portions spruce needles bearing telia were also stained with hema- cidate its relationship with other members of the ge- toxylin (Sass 1958). Tissue was first fixed in formalin-acetic nus. In this study we describe the cytology and the acid-ethanol for 3 d, then rinsed in 50% ethanol, dehy- form of in C. weirii, unique teliospore germination drated in a n-butanol series, and embedded in paraffin and discuss the of these possible implications features (Sass 1958). Sections (10 p.m thick) were made using a ro- for its dispersal. tary microtome and mounted on glass slides with Haupt's adhesive (Gurr 1965). Slides were dewaxed in xylene, re- in an ethanol series, in 4% iron alum mor- MATERIALSAND METHODS hydrated placed dant for 4 h, rinsed in distilled water, and stained in Hei- Specimens of C. weirii were examined from the Mycological denhain's hematoxylin for 4 h, then destained in diluted Herbarium of the Northern Forestry Centre (CFB), Ed- iron alum as necessary (Sass 1958). Slides were dehydrated monton, Alberta, and the Pacific Forestry Centre (DAVFP), in an ethanol series then placed in xylene before coverslips Victoria, British Columbia, Canadian Forest Service; and were permanently mounted with Permount (Fisher Scien- the Arthur Herbarium (PUR), Purdue University, Lafayette, tific Co.). Indiana. The following collections were examined (host, lo- Microscopy of inoculated spruce.-To study spore germina- cation, collection number): P engelmannii, Alberta, CFB tion on host tissue, newly opened vegetative buds of 3-yr- 7967, British Columbia, CFB 458, CFB 7960, CFB 22109 (ex old greenhouse-grown P glauca were inoculated in two DAVFP), CFB 22111 (ex DAVFP 69-9-0775-01), Idaho, PUR ways. Needles bearing mature sori were attached to the lids 4906, Oregon, PUR 4907 (Type); P glauca, Alberta, CFB of petri dishes above excised shoots in a moist chamber, as 4903, CFB 5742, CFB 8089, CFB 20015, CFB 22077, CFB above. In other cases, sori were wetted with droplets of dis- 22195, CFB 22196, CFB 22198, British Columbia, CFB 8498, tilled water, then telia were rubbed along the young nee- Saskatchewan, CFB 20816, Yukon Territory, CFB 7495, CFB dles, and the shoots were kept in a moist chamber either 8904; P mariana, Manitoba, CFB 22175; P pungens, New at room temperature or in a refrigerator. At regular inter- York, PUR 49269; P rubens, West Virginia, PUR 44396; P vals from 5 to 30 h after inoculation, thin segments of the sitchensis, Oregon, CFB 8818. Three fresh collections, one upper surface (epidermis and part of underlying meso- from Kananaskis (CFB 22198) and two from Jasper (CFB phyll) of individual needles were removed with a razor 22195, CFB 22196), Alberta, were used to study the cytology blade, mounted in lactophenol-cotton blue, and examined and spore germination. Morphology was studied by light by light microscopy for spore germination on the host sur- microscopy using squash mounts of telia and cross sections face. In fresh collections of infected spruce, young current- of spruce needles bearing sori mounted in lactophenol or year needles adjacent to sporulating needles were exam- lactophenol-cotton blue. ined for evidence of natural spore deposition and germi- Teliosporegermination.-Spruce needles bearing mature te- nation. Host epidermis was removed and examined micro- lia were attached with petroleum jelly to the lids of petri scopically in the same manner as for artificially inoculated dishes containing moist filter paper. Glass slides were placed needles. For scanning electron microscopy (SEM), young below the needles to capture basidiospores, and the dishes current-year spruce shoots, both artificially and naturally in- were sealed and kept in a refrigerator (4 C) or at room oculated as above, were vapor-fixed in OSO04:shoots were temperature (20 C) for up to 1 wk. Teliospores were also enclosed in sealed petri dishes containing 3 or 4 drops of dispersed in droplets of water on glass slides and kept in a 2% OS04 in phosphate buffer, pH 7, for 24 h. They were moist chamber. They were examined by light microscopy at then either air-dried or frozen in liquid nitrogen and regular intervals from 2 h to 3 d after dispersal. Because freeze-dried, coated with gold using a sputter coater, and initial studies showed some variation in type of germination, examined with an Hitachi S-510 scanning electron micro- slides were kept in a refrigerator in darkness or at room scope operated at 15 kV. temperature either under fluorescent light or in darkness, Light microscope images were made by digitizing black and the results were compared. and white photographic negatives made from Kodak TMAX 100 or 400 film. SEM images were captured using Quartz Cytological studies.-The fluorescent dye 4',6-diamidino-2- PCI software, version 4.0. Image contrast was adjusted and phenylindole (DAPI) was used to study the nuclear condi- all halftone plates were composed using Adobe Photoshop tion of the various stages in the life of C. weirii: cycle hyphae 5.0. in cross sections of infected needles, squash mounts of the base of telia, ungerminated teliospores, germinating telio- spores (at 2, 3, 4.5, and 22 h after dispersal of teliospores RESULTS in water), and basidiospores.
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