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植物研究雑誌 J. J. Jpn. Bo t. 73:279-286(1998) 73:279-286(1998) Ultrastructure Ultrastructure of the Pyrenoid in the Family Cladophoraceae (Cladophorales ，Chlorophyta) Kazuyo MATSUYAMA a， Takanori MATSUOKA b，Kazuyuki MIYAJI c， Jiro Jiro TANAKA a and Yusho ARUGA a aLaboratory aLaboratory of Phycology ，Tokyo University of Fisheries ， Konan 4-5-7 ，Minato-ku ，Tokyo ， 108-8477 JAPAN; bDepartment bDepartment of Histology ，The Nippon Dental University ， F吋imi 1-9-20 ，Chiyoda-ku ，Tokyo ， 102-8159 JAPAN; CDepartment CDepartment ofBiology ， Faculty of Science ，Toho University ， Miyama 2-2-1 ，Funabashi ，Chiba ， 274-8150 JAPAN (Received on November 27 ， 1997) The pyrenoid structure was examined with TEM in 14 J apanese species belonging to four four genera of the family Cladophoraceae. Four types of pyrenoids were recognized; i.e. bilenticular ，zonal ，simple polypyramidal andcomplex polypyramidal types. The pyrenoid matrix matrix of the bilenticular pyrenoid is traversed by a single thy lakoid band ，the matrix being composed of a pair of hemispheres and surrounded by two starch sheaths. The pyrenoid matrix matrix of the zonal type is divided by parallel thylakoid bands ， and is surrounded by more than than three sheaths. starch The pyrenoid matrix of the simple polypyramidal type is traversed traversed by three or more thylakoid bands ，four or more pieces of starch sheaths or grains covering covering the surface of the pyrenoid matrix. The pyrenoid matrix of the complex polypyramidal polypyramidal type is divided by intrusions of many sinuous thylakoid bands ， and is surrounded surrounded by many small starch sheaths or grains. Three or four types of pyrenoid were observed observed in the genera Chaetomorpha ， Cladophora and Rhizoclonium. Until Until recently cladophoracean algae were Materials and Methods considered to possess hemispherical Fourteen J apanese species belonging to four bilenticular bilenticular pyrenoids in which the pyrenoid genera of Cladophoraceae were examined. matrix matrix was traversed by a single thylakoid The species ，localities and dates of collection band and surrounded by a pair of starch sheaths are given in Table 1. Most materials were fixed (Gibbs (Gibbs 1962 ，Hori and Ueda 1967 ，Phillips one or two days after collection ， while others 1990). 1990). Wang (1 989) and Miyaji (1 995) ，how- were fixed a few weeks after collection. All of ever ， reported that some species of the marine species were fixed with 2% glutar- Cladophoraceae have polypyramidal aldehyde in 0.1 M sodium phosphate buffer pyrenoids ， the matrix of which is traversed by (pH 7.1) with 0.25 M sodium saccharose for 1 many thylakoid bands and surrounded by many hr. For fresh water species ， the fixation was pieces pieces of starch sheaths or grains. The present made with a solution of2% glutaraladehyde in study study was carried out to examine ultrastruc- 0.1 M sodium phosphate buffer (pH 7.1) for 1 ture ture of the pyrenoid of Cladophoraceae. hr. Postfixation was made with 2% osmium tetroxide tetroxide in 0.1 M sodium phosphate buffer for -279 ー 280 280 植物研究雑誌第73 巻第5号 平成10 年 10 月 Table Table 1. Species examined in the present study Species Species Locality Date of collection Ch α etomorpha antennina Shirahama ，Shimoda City ， Shizuoka Pref. May 16 ，1996 Ch. Ch. basiretrorsa Shirahama ，Shimoda City ， Shizuoka Pre f. May 16 ，1996 Ch. Ch. brachygona Uranohama ，Yamada-cho ， Iwate Pref. Aug. 12 ，1996 Ch. Ch. crassa Toji ，Shimoda City ， Shizuoka Pre f. May 17 ，1996 Ch. Ch. gracilis Banda ，Tateyama City ，Chiba Pre f. June 1，1996 Ch. Ch. moniligera Uranohama ，Yamada-cho ， Iwate Pref. Aug. 12 ，1996 Ch. Ch. spir α， lis Shirahama ，Shimoda City ， Shizuoka Pref. May 16 ，1996 Cladophora Cladophora aegagropila * Lake Saiko ，Ashiwada-mura ，Yamanashi Pref. Oc t. 9，1994 CI. CI. catenata Hachijojima Is 1.， Tokyo Metropolitan Ap r. 27 ，1996 l. C l. conchopheria Okinoshima ，Tateyama City ，Chiba Pref. June 4，1996 l. C l. ohkuboana Shirahama ，Simoda City ， Shizuoka Pre f. May 16 ，1996 l. C l. stimpsonii Uranohama ，Yamada-cho ， Iwate Pref. Aug. 12 ，1996 Rhizoclonium Rhizoclonium riparium* Oiso ，Naka-gun ，Kanagawa Pre f. June 12 ，1996 Pithophora Pithophora mooreana* Nankoku City ，Kochi Pre f. Oc t. 18 ， 1996 *freshwater *freshwater species 1h r. After the postfixation ， the material was TypeA Type B transferred transferred into 0.5% uranyl acetate solution and and kept for 1 hr. The specimens were dehy- drated drated in a graded acetone series up to 100% acetone acetone and were then transferred into 100% propylene propylene oxide. The materials were then embedded with Spurr's low-viscosity embed- ding ding medium (Spurr 1969). P01ymerization Type C Type D was carried out at 60 0 C for 24 hr. The polym- erized erized material was sectioned with a diamond knife knife on a Sorvall MT2-B or a LKB 2088 ultramicrotome. ultramicrotome. The section was stained with uranyl uranyl acetate and lead citrate ， and examined with with a Hitachi H-7000 or a Jeol 2000EXII Fig. 1. Schematic drawings of the four types of electron electron microscope. pyrenoids. Observations Observations From observations of the structure of matrix traversed by a single thylakoid band pyrenoid pyrenoid matrix ， the shape of the associated which is continuous with the chloroplast starch starch sheaths or grains and the number of thy lakoid. The pyrenoid matrix is surrounded intrapyrenoidal intrapyrenoidal thy lakoid bands ， the four types by two cup-shaped starch sheaths. This is the of of pyrenoids (Types A ，B ，C and D) were most typical pyrenoid in Cladophoraceae and recognized recognized in the present materials. These corresponds to the bilenticular pyrenoid de- types types are schematically shown in Figure 1. fined by Chadefaud (1941). Hori and U eda 1) 1) Type A (Figs. 2-11) (1967) referred to this type of pyrenoid as the In In this type ， the pyrenoid is composed of a “Cladophora-type". This typeofpyrenoid was October October 1998 Journal of Japanese Botany Vo l. 73 No. 5 281 Figs.2-9. Figs.2-9. Type A pyrenoids. Fig. 2. Chaetomorpha antennina. Fig. 3. Ch. basiretrorsa. Fig. 4. Ch. br α， chygon α. Fig. 5. 5. C h. crassa. Fig. 6. Ch. gracilis. Fig. 7. Ch. moniligera. Fig. 8. Ch. spiralis. Fig. 9. Cladophor α， ohkuboana. Scale bars bars = 1μm. 282 282 植物研究雑誌第73 巻第5号 平成10 年10 月 Figs. Figs. 10-1 1. Type A pyrenoids. Fig. 10. Cladophora stimpsonii. Fig. 11. Rhizoclonium riparium. Figs. 12-16. Type B pyrenoids. Fig. 12. C h. antennina. Fig. 13. Ch. brachygona. Fig. 14. C h. moniligera. Fig. 15. Ch. spiralis. Fig. Fig. 16. C l. ohkuboana. Fig. 17. Type C pyrenoid.C l. αegagropila. Scale bar = 1μill. October October 1998 Journal of Japanese Botany Vo l. 73 No. 5 283 observed observed in Chaetomorpha antennina (Bory) in the present study this species was found to Kutz. Kutz. (Fig. 2) ， Ch. basiretrorsa Setch. (Fig. 3) ， have two types ofpyrenoids (Types A and B). Ch. Ch. brachygona Harv. (Fig. 4) ，C h. crassa 3) Type C (Figs. 17-19) (C.Agardh) (C.Agardh) Kutz. (Fig. 5) ， Ch. gracilis Kutz. In this type ， the pyrenoid matrix is traversed (Fig. (Fig. 6) ，C h. moniligera Kjellm. (Fig. 7) ，C h. by three or more thylakoid bands and four or spiralis spiralis Okamura (Fig. 8) ，Cladophora more pieces of starch sheaths or grains cover ohkuboana Holmes (Fig. 9) ， Cl. stimpsonii the surface of the pyrenoid matrix. This type of Harv. Harv. (Fig. 10) and Rhizoclonium riparium (Roth) (Roth) Kutz. ex Harv. (Fig. 11) in the present study. study. With an exception of R. riparium ，all of them are marine species. This This type of pyrenoid has already been reported reported for Chaetomorpha brachygona (Chan et et al. 1978); C h. crassa ， C l. wrightian αHarv. Rhizoclonium Rhizoclonium tortuosum (Dillwyn) (Hori Kutz. andUeda 1967); C h. linum(Mull.)Kutz. (Gibbs 1962); 1962); C h. spiralis(HirayamaandHori 1984); Cladophora albida (Nees) Kutz. ， Cl. fascicularis fascicularis (Mertens ex C.Agardh) Kutz. ，C l. opaca Sakai ， Cl. rudolphiana (C.Agardh) Kutz. ， Cl. sakaii Abbott (Wang 1989); Cl. flexuosa flexuosa (Muller) Kutz. (Scott and Bullock 1976); 1976); Cl. fracta (Mull. ex Vahl) Kutz. (StruggerandPeveling (StruggerandPeveling 1961)andC l. glomerata (L.) (L.) Kutz. (McDonald and Pickett -Heaps 1976) (Table (Table 2). 2) 2) Type B (Figs. 12-16) In In this type ， the pyrenoid matrix is divided by parallel thylakoid bands ，and is surrounded by more than three starch sheaths. This type of pyrenoid pyrenoid was always observed together with Type A pyrenoids but was only rarely ob- served served in cells of the present materials ， as Chaetomorpha antennina (Fig. 12) ， Ch. brachygona brachygona (Fig. 13) ，C h. moniligera (Fig. 14) ，C h. spiralis (Fig. 15) and Cladophora ohkuboana (Fig. 16) ，all of which are marine specles. specles. This This type of pyrenoid was also reported for Ch. Ch. linum (Gibbs 1962) and Rhizoclonium tortuosum tortuosum (Hori and Ueda 1967) (Table 2). Even though Chan et al. (1978) described that Figs. 18-19. Type C pyrenoids. Fig. 18. Cladophora catenata. catenata. Fig. 19. Pithophora mooreana. Fig. 20. Ch. Ch. brachygona has only one type of pyrenoid Type D pyrenoid. CI. conchopheria. Scale bar = 1 in in which the matrix is divided into two pieces ， μm. 284 植物研究雑誌 第73 巻 第5号 平成10 年10 月 pyrenoid was observed in Cladophora Thus ， the pyrenoid structure of this type has a aegagropila aegagropila (L.) Rabenh. (Fig. 17) ， Cl. more complex appearance as compared with catenata catenata (L.) Kutz. (Fig. 18) and Pithophora that of Type C. This pyrenoid type was ob- mooreana Collins (Fig. 19) in the present served in Cladophora conchopheria Sakai (Fig. study. study. 20) in the present study. This This type of pyrenoid has already been The same type of pyrenoid has already been reported reported for Cl.

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