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Morphology of aecia of the rust fungi
[ 223 ] Trans. Br. Mycol. Soc. 85 (2), 223-238 (1985)
Printed in Great Britain
MORPHOLOGY OF AECIA OF THE RUST FUNGI By TOYOZO SATO· AND SHOJI SATO Institute of Agriculture and Forestry, University of Tsukuba, Sakura-mura, Niihari-gun, Ibaraki 305, Japan Using light and scanning electron microscopy, comparisons of aecial states of 80 species belonging to 33 genera of rust fungi were made. Aecia were classified into 14 morphological types on the basis of spore ontogeny, shape of hymenium, position of hymenium in host tissues, presence of intercalary cells, presence of sporogenous cells, presence and number of layers of peridium, presence of peripheral paraphyses, aeciospore surface structure, and germ pores of spores. Peridermia, roestelia and aecidium could be distinguished by spore surface structure. The three traditional types, peridermium, caeoma and uraecium were divided into 3,6 and 3 types, respectively. Related genera were often included in one aecial type of the 14 aecial types recognized. Aecial morphology is important in the natural classification and phylogeny of the Uredinales. Since Brongniart recognized the rust fungi as an order' U redinees ' , a number of taxonomic systems have be~n proposed (Hiratsuka, 1955; Hennen & Buritica, 1980). Most of these have been based on the morphology of the mature telial state, with little regard for characters of other spore states. During the last two decades spermogonia (Hiratsuka & Cummins, 1963; Hiratsuka & Hiratsuka, 1980) and uredinia (Kenny, 1970) have been studied in detail throughout the Uredinales, and it has been pointed out that morphology of spermogonia and uredinia are significant for supraspecific classification as well as for discussions on intergeneric relationships in the Uredinales. However, there has been no report of morphological comparisons of the aecial states throughout the order, though numerous studies of aecial ontogeny and morphology of individual species or genera have been reported since 1896 (Sappin-Trouffy, 1896; Blackman, 1904; Christman, 1905, 1907; Blackman & Fraser, 1906; Kern, 1910, 1973; Fromme, 1912, 1914; Colley, 1918; Kursanov, 1922; Thirumalachar, Kern & PatH, 1966; Peterson, 1967, 1974; Singh, 1969; Sato & Katsuya, 1979). Laundon (1967) proposed an aecial classification based on macroscopic morphology of aecia, their host plants, host organ bearing them, and spermogonial characters. Five types of aecia, namely peridermioid, roestelioid, aecidioid, caeomoid and uredinoid, have been generally accepted (Cummins, 1959; Hiratsuka & Sato, 1982).. Precise morphological definition of these types, however, has not been
* Present address: Ogasawara Subtropical Agriculture Center, Chichi-jima Is., Ogasawara-mura, Tokyo 100-21, Japan.
possible, and some of them appear to contain several different types (Peterson, 1974). Cummins (1959) defined the aecidioid, peridermioid and roestelioid aecia by 'gentleman's agreement', because they were difficult to define and separate purely on morphological bases. Hiratsuka & Sato (1982) pointed out that the caeomoid type contained aecia with rudimentary peridial cells or with peripheral paraphyses besides naked ones. In the present study, morphological comparisons of aecial states of rust fungi mainly collected in Japan were carried out to clarify morphological differences among the aecial types and to reclassify them. The present paper follows the definition of aecial state in the 'ontogenic system' (Hiratsuka, 1973). In the present paper the words peridermium, roestelia, aecidium, caeoma and uraecium do not represent anamorphic generic names but five morphologically different spore-producing structures that may occur in the aecial position in rust life cycles. MA TBRIALS AND METHODS
Fresh material fixed with FAA or dry herbarium specimens of aecia of 80 species in 33 rust genera listed in Table 1 were sectioned with a microtome or by hand, and stained for observation by light microscopy. The FAA-fixed materials were dehydrated by ethanol and xylene series, embedded in paraffin and sectioned at 15-20 pm. Sections were stained with Flemming's triple stain orHeidenhain's iron alum haematoxylin and orange-G double stain after the paraffin had been dissolved in two changes of xylene, and mounted in Canada balsam on glass slides. Dry herbarium material of some species was
Aecial morphology
224
Table
1.
Aecial types of rust species examined
Species Aecidium foetidum Diet.
Caeoma deformans (Berk. & Br.) Tubeuf Caeoma makinoi Kusano Caeomapeltatum C.G. Shaw III & c. G. Shaw Caeoma radiatum Shirai Calyptospora goeppertiana KUhn Ceraceopsora elaeagni Kakishima et al. Cerotelium dicentrae Mains & Anderson Chrysomyxa succirrea (Sacc.) Tranz. Chrysomyxa woroninii Tranz. Coleosporium asterum (Diet.) P. & H. Sydow Coleosporium bletiae Diet. Coleosporium clematidis Barclay Coleosporium clematidis-apiifoliae Diet. Coleosporium eupatorii Hiratsuka f. Coleosporium horianum Hennings Coleosporium paederiae Diet. ex Hiratsuka f. Coleosporium phellodendri Komarov Cronartium kamtschaticum Jerstad Cronartium ribicola Fischer d. Waldh. Gymnoconia peckiana (Howe) Trotter Gymnosporangium asiaticum Miyabe ex Shirai Gymnosporangium miyabei Yamada & I. Miyake Gymnosporangium yamadae Miyabe ex Tanaka Hyalopsora aculeata Kamei Leucotelium pruni-persicae (Hori) Tranz. Melampsora abietis-populi S. Imai ex S. Ito Melampsora chelidoni-pierotii Matsumoto Melampsora larici-capraearum Kleb. Melampsora larici-populina Diet. Melampsora occidentalis Jackson Melampsora yezoensis Miyabe & Matsumoto Melampsorella caryophyllacearum Schrot. Melampsoridium hiratsukanum S. Ito ex Hiratsuka f. Mikronegeria alba Oehrens & Peterson Milesina sp. Miyagia anaphalidis Miyabe ex P. & H. Sydow Nyssopsora cedrelae (Hori) Tranz. Ochropsora kraunhiae (Diet.) Diet. Phakopsora ampelopsidis Diet. & P. Sydow Phakopsora meliosmae Kusano Phragmidium itoanum Hiratsuka f. Phragmidium montivagum Arthur Phragmidium rosae-multiflorae Diet. Phragmidium rubi-idaei (DC.) Karsten Phragmidium rubi-thunbergii Kusano Pileolaria klugkistiana Diet. Puccinia caricis-petasitidis Y. Harada Puccinia coronata Corda Puccinia crepidis-japonicae Diet. Puccinia dieteliana P. Sydow Puccinia graminis Pers.
Specimen no. TS-R 1125 TS-R 1002 TS-R 1003 TS-R 1004 TS-R 1006 TS-R 1126 TS-R 1008 TS-R 1086 TS-R 1082 TS-R 1087 TS-R 1010 TS-R 1011 TS-R 1116 TS-R 1123 TS-R 1090 TS-R 1091 TS-R 1015 TS-R 1014 TS-R 1092 TS-R 1093 TS-R 1016 TS-R 1018 TS-R 1020 TS-R 1096 TS-R 1097 TS-R 1021 TS-R 1024 TS-R 1101 TS-R 1026 TS-R 1027 TS-R 1028 TS-R 1127 TS-R 1029 TS-R 1102 TS-R 1103 TS-R 1104 TS-R 1105 TS-R 1128 TS-R 1032 TS-R 1107 TS-R 1124 TS-R 1033 TS-R 1034 TS-R 1123 TS-R 1037 TS-R 1038 TS-R 1040 TS-R 1113 TS-R 1042 TS-R 1043 TS-R 1114 TS-R 1046 TS-R 1047 TS-R 1117 TS-R 1120 TS-R 1048 TS-R 1050 TS-R 1085
Spermogonial type (group)· Aecial type 4 (V) Aecidium 4 (V) Aecidium 12 (III) Caeoma IV 12 (III) Caeoma IV 4 (V) Caeoma V 12 (III) Caeoma IV 4 (V) Caeoma V ? Peridennium I 7 (VI) Aecidium 7 (VI) Aecidium 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridermium II 2 (I) Peridermium II 2 (I) Peridermium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II Peridermium III 9 (II) Peridermium III 9 (II) 6 (IV) Caeoma II 6 (IV) Caeoma II Roestelia 4 (V) Roestelia 4 (V) Roestelia 4 (V) 2 (I) Peridennium I 7 (VI) Aecidium Caeoma II 3 (I) Caeoma II 3 (I) Caeoma I 3 (I) Caeoma I HI) Caeoma I 3 (I) Caeoma I 3 (I) Caeoma I 3 (I) Caeoma II 3 (I) Peridermium I 3 (I) Peridermium II 3 (I) Caeoma IV 12 (III) Peridermium I 1 (I) Aecidium 4 (V) Uraecium III Aecidium 7 (VI) Aecidium 7 (VI) Aecidium 7 (VI) 10 (IV) Uraecium II 11 (IV) Caeoma III Caeoma III ? ? Caeoma III 10 (IV) Uraecium II Uraecium III 7 (VI) Aecidium 4 (V) 4 (V) Aecidium Aecidium 4 (V) Aecidium 4 (V) Aecidium 4 (V)
T. Sato and S. Sato Table Species Puccinia linosyridi-caricis Ed. Fischer Puccinia m;scanthi Miura Puccinia nolitangeris Corda Puccinia osmorrhizae Cooke & Peck Puccinia podophylli Schw. Puccinia polygoni-amphibii Pers. Puccinia pulchella Ono & Kakishima Puccinia punctata Link Puccinia recondita Roberge ex Desm. Puccinia zoysiae Diet. Pucciniastrum fag; Yamada Pucciniastrum kusanoi Diet. Pucciniastrum tiliae Miyabe ex Hiratsuka Pucciniostele clarkiana (Barel.) Diet. Pucciniostek mandschurica Diet. Thekopsora areolata (Fr.) Magnus Thekopsora sp. Tranzschelia pruni-spinosae (Pers.) Diet. Triphragmium ulmariae Link Uredinopsis jilicina Magnus Uredinopsis komagatakensis Hiratsuka f. Uromyces amurensis Komarov Uromyces erythronii Passerini Uromyces heimelianus Magnus Uromyces truncicola Hennings & Shirai Uromyces f)iciae-fabae (Pers.) Swot. Xenodochus carbonarius Schlecht. Zaghouania phillyreae Pat.
1
225
(Cont.)
Specimen no. TS-R 216 TS-R 1051 TS-R 1084 TS-R 1052 TS-R 1053 TS-R 1118 TS-R 1055 TS-R 1056 TS-R 1083 TS-R 1057 TS-R 1121 TS-R 1058 TS-R 1059 TS-R 1115 TS-R 1060 TS-R 1062 TS-R 1063 TS-R 1109 TS-R 1069 TS-R 1110 TS-R 1111 TS-R 1070 TS-R 1112 TS-R 1072 TS-R 1073 TS-R 1074 TS-R 1076 TS-R 1077 TS-R 1122 TS-R 1078 TS-R 1080
Aecial type Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Peridermium I Peridermium I Peridermium I Peridermium I Caeoma II Caeoma II Peridermium I Uraecium I Aecidium Aecidium Uraecium II Peridermium I Peridermium I Aecidium Aecidium Aecidium Uraecium III Aecidium Caeoma III Caeoma VI
Spermogonial type (group)"* 4 4 4 4 4
(V) (V) (V) (V) (V)
? 4 (V)
4 (V) 4 (V) 4 (V) 3 (I) 3 (I) 3 (I) 3 (I) 7 (VI) 7 (VI) 3 (I) 3 (I) 7 (VI) 7 (VI) 11 (IV) 3 (I) 2 (I) 4 (V)
4 (V) 4 (V) 4 (V) 4 (V) 10 (IV) 4 (V)
"* Mter Hiratsuka & Hiratsuka (1980).
also examined under a scanning electron microscope (SEM). Small pieces of the leaves bearing aecia or aeciospores only were placed on double adhesive tape on specimen holders, and coated with gold under a high vacuum with an Eiko IB-3 ion coater. The preparations were examined under a Hitachi S-430 SEM operating at 20 kV. RESULTS
The following characters of the aedal state were examined in detail: (1) spore ontogeny, (2) shape of hymenium, (3) position of hymenium in host tissues, (4) lateral growth of hymenium, (5) presence of intercalary cells, (6) presence of sporogenous cells, (7) presence of number of layer(s) of peridium, (8) presence and peripheral paraphyses, (9) germ pores ofspores, and (10) spore surface structure. These seemed to be stable characters of aeda. The lateral growth of hymenia 8
appeared to depend on the position of hymenia formed in host tissues. Aecia were classified into 14 morphological types (Fig. 31) on the basis of the nine characters listed above except for the lateral growth ofhymenia. The morphological types of aecia of species examined are listed in Table 1, and genera included in each type are listed in Table 2. Descriptions ofthe types follow. Peridermium Aecia recognized previously as of the peridermioid type could be divided into three morphological types mainly on the basis of hymenial positions in host tissues: intramesophyllic, peridermium I; subepidermal, peridermium II; intracortical, peridermium III. Peridermium I (Figs 1-3). Spores catenulate, spore surface structure of the annulate type (Sato & Sato, 1982), germ pores obscure, intercalary cells present MYC
85
Aecial morphology
226 Table
2.
Aeciospore surface-structure types, groups of spermogonial types and rust genera corresponding to the aecial types
Aecial type Peridermium I
Aeciospore surfacestructure type Annulate
Peridermium II
Annulate
I
Peridermium III Roestelia
Annulate Coronate Coronate and verrucose Verrucose
II V V
Verrucose
VI
Nail-headed Verrucose Verrucose Verrucose Tubulate Echinulate
VI I I IV VI IV
Verrucoset Verrucose and aciculate Nail-headed:j: Verrucose Aciculate Reticulate Echinulate Echinulate Echinulate§ Echinulate§ Echinulate§
III III
Aecidium
Caeoma I Caeoma II Caeoma III Caeoma IV
Caeoma V Caeoma VI Uraecium I Uraecium II Uraecium III
(Ridgy) II
Group of spermogonial type*
V
III V V V I IV V IV VI
Rust genus (no. of species examined) Calyptospora (1), Hyalopsora (1), Melampsorella (1), Milesina (1), Pucciniastrum (3), Thekopsora (1), Uredinopsis (2) Chrysomyxa (2), Coleosporium (8), Melampsoridium (1) Cronartium (2) Gymnosporangium (2) Gymnosporangium (1) Aecidium (1), Miyagia (1), Uromyces (4), Puccinia (14) Cerotelium (1), Leucotelium (1), Ochropsora (1), Phakopsora (1), Tranzschelia (1), Ceraceopsora (1) Phakopsora (1) Melampsora (3) Melampsora (3) Gymnoconia (1) Pucciniostele (2) Phragmidium (3), Xenodochus (1) Mikronegeria (1) Caeoma (1) Caeoma (1) Caeoma (1) Caeoma (1) Zaghouania (1) Thekopsora (1) Phragmidium (2) Uromyces (1) Triphragmium (1) Nyssopsora (1) Pileolaria (1)
* After Hiratsuka & Hiratsuka (1980). t After Peterson & Oehrens (1978). :j: After Shaw (1976). § Determined by light microscopy only. II Not contained in the aeciospore surface-structure types (Sato & Sato, 1982) because of lack of SEM observations.
Figs 1--6. Venical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IS, immature spore; M, host mesophyll; P, peridium; PC, peridial cell; PP, pseudoparenchyma; SC, sporogenous cell. Stainings: 1,2,3,4,6, Heidenhain's haematoxylin and orange G; 5, Flemming's triple stain. Scales: 1,4, 10llm; 2, 3, 1llm; 5, 6, 21lm. Fig. 1. Peridermium I type of an aecium of Pucciniastrum fagi showing an intramesophyllic hymenium' (H). Fig. 2. Basal periphery of peridermium I type of an aecium of Milesina sp. Fig. 3. Peridial cells (PC) of Milesina sp.
T. Sata and S. Sata
227
Fig. 4. Peridermium II type of an aecium of Chrysomyxa succinea showing a subepidermal hymenium (H). Fig. 5. Basal periphery of peridermium II type of aecium of Coleosporium eupalorii. Fig. 6. A basal part of peridermium II type of an aecium of Ch. succinea, 8-2
228
Aecial morphology
PO
8
....... . ~
.... ;.
Figs 7-13. For caption see opposite.
T. Sato and S. Sato (Fig. 2), hymenium intramesophyIlic, sori peridiate with single-layered peridia (Fig. 3), inner walls of peridial cells usually thicker than outer walls (Fig. 3). This type of aecium is formed in two rows on the lower surface of needles of coniferous plants, and lateral growth of their hymenia is so detertninate that aecial shapes are slenderly cylindrical except for aecia of Thekopsora areolata. Peridermium I is similar to the roestelia and aecidium types, but these three types are clearly distinguished by spore surface structures. Aeciospores of peridermium I, roestelia and aecidium types correspond toannulate, coronate and verrucose or nail-headed surface structure types, respectively (Sato & Sato, 1982).
PerUkrmium II (Figs 4~). Spores catenulate (Figs 4, 5), intercalary cells present (Figs 5, 6), hymenium subepidermal (Fig. 4), and sori peridiate with single-layered peridium (Fig. 5). In this type, lateral growth of hymenia is so indeterminate longitudinally on ne~es of coniferous plants that aecia like tongues or pillows develop (Fig. 4). Conspicuous palisade-like pleetenchymata under the epidermis surround the aecial margin of Coleosporium spp. examined. Peridermium III (Figs 7-9). Spores catenulate (Fig. 9), intercalary cells present (Fig. 9), hymenia intracortical (Fig. 7), and sori peridiate with multi-layered peridia (Fig. 8). This type of aecium was produced on trunks or branches of Pinus, and shape of hymenia depends on that of the host tissue bearing them because of the indeterminate nature of their lateral growth. Peridia of Cronartium ribieola were composed of 2-3 layers of cells, while those of C. kamtschaticum were 2- to 4-layered (Fig. 8). Pseudoparenchymata were well-developed beneath and around the sori of both species (Fig. 7).
229
Roestelia Spores catenulate (Fig. 11), spore surface structure of the coronate type, germ pores conspicuous (Fig. 13), intercalary cells present (Fig. 11), hymenium intramesophyllic (Fig. 10), sori peridiate with single-layered peridia (Fig. 12), inner walls of peridial cells usually thicker than outer ones (Fig. 12). Comute to cylindrical aecia of this type elongate from the lower surface of host leaves, and their determinate hymenia are seated in a deep portion of hypertrophied mesophyll (Fig. 10). Chains composed of immature spores and cylindrical to string-like intercalary cells are characteristically long (Fig. 11). Aecidium Spores catenulate, spore surface structure verrucose or of the nail-headed type, germ pores obscure or conspicuous, intercalary cells present, hymenium intramesophyIlic, sori peridiate with single-layered peridium (Fig. 14), inner walls of peridial cells usually thinner than outer one (Fig. 15). Hymenia·ofthis type are detertninate in general though some of the aecidioid aecia, e.g. Puccinia osmorrhizae and Uromyces erythronii, show considerable variation of hymenial size. In Puccinia crepidis-japonicae, Phakopsora meliosmae and Miyagia anaphalidis, inner walls of peridial cells are thicker than outer ones, and coherence of peridial cells of P. osmorrhizae and Ph. meliosmae is weak. Intercalary cells of the aecidium type are flat to wedge-shaped. Spore surface structure of all species of this type corresponds to the verrucose type except for those of Ph. meliosmae, as reported previously (Sato & Sato, 1982).
Figs 7-13. Vertical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IN, inner wall; IS, immature spore; M, host mesophyll; 0, outer wall; P, peridium; PO, host periderm; PP, pseudoparenchyma; T, host tissue. Stainings: 7, 8, 9,10,11,13, Flemming's triple stain; 12, Heidenhain's haematoxylin and orange G. Scales: 7, 10, :zo pm; 8, :1 pm; 9, 11, 12, 13, 10 pm. Fig. 7. Peridermium III type of an aecium of Cronartium kamtschaticum showing an intracortical hymenium (H). Fig. 8. A two- to three-layered peridium of C. kamtschaticum. Fig. 9. A basal part of an aecium of C. kamrschaticum. Fig. 10. Roestelia type of an aecium of Gymnosporangium asiaticum. Fig. 11. A basal part of an aecium of G. asiaticum showing elongated intercalary cells (I). Fig. 12. A peridial cell (PC) of G. asiaticum showing inner wall (IN) thicker than outer one (0). Fig. 13. Aeciospores of G. asiaticum with conspicuous germ pores.
2~O
Aecial morphology
-AM
Figs 14-18. Vertical sections and a scanning electron micrograph (16) of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; M, host mesophyll; P, peridium; PC, peridial cell; PP, pseudoparenchyma; RP, rudimentary peridial cell. Stainings: 14, lS, Heidenhain's haematoxylin and orange G; 17, no staining; 18, Flemming's triple stain. Scales: 14, 17, 18, 10,um; 16, 20,urn; lS, l,urn. Fig. 14. Aecidium type of an aecium of PUCciM pulchella. Fig. lS. A peripheral part of an aecium of P. pulchella. Fig. 16. A scanning electron micrograph of caeorna I type of an aecium of Melampsora occidentalis showing peripheral rudimentary peridial cells (RP). Fig. 17. Caeoma I type of an aecium of M. occidentalis. Fig. 18. Caeoma II type of an aecium of Pucciniosrele mandschurica.
T. Sato and S. Sato Caeoma Non-peridiate aecia with catenulate spores, currently lumped together under the anamorphic genus Caeoma, could be divided into six morphological types on the basis of shape of hymenia, Intercalary cells present Hymenia hemispherical. Hymenia flat Rudimentary peridial cells present Rudimentary peridial cells absent Peripheral paraphyses present Peripheral paraphyses absent . Intercalary cells absent Sporogenous cells conspicuous Sporogenous cells obscure
Caeoma I (Figs 16, 17). Spores catenulate, intercalary cells present, hymenia subepidermal, and rudimentary peridial cells present around sori (Fig. 16). This type of aecium is formed on the lower surface of needles of coniferous plants, where the hymenia are longitudinally indeterminate. Coherence of the rudimentary peridial cells was different among the species. Three- to four-celled pieces of peridium were observed in aecia of Melampsora larici-capraearum, while the peridial cells loosely lined aecia of M. larici-populina and M. occidentalis. Such variation may suggest that caeoma I is a transitional type between peridermium II and caeoma II described below. Caeoma II (Fig. 18). Spores catenulate, intercalary cells present, hymenium flat and subepidermal, and both peridia and paraphyses absent (Fig. 18). Hymenia ofthis type are indeterminate. Though this type lacks peridia, in the three species of Melampsora and Pucciniostele clarkiana subepidermal pseudoparenchyma was well-developed around the sori (Fig. 18). Caeoma III (Figs 19, 20). Spores catenulate, intercalary cells present, hymenium subepidermal, and peripheral paraphyses present (Fig. 19). This type of aecium is produced on rosaceous plants, and the hymenium develops indeterminately. Large, incurved peripheral paraphyses surround aecia of Phragmidium rubi-idaei (Fig. 19), whereas paraphyses of Xenodochus carbonarius are relatively small and cylindrical, as reported by Sato & Sato (1980). Caeoma IV (Figs 21, 22). Spores catenulate, intercalary cells absent, sporogenous cells conspicuous, hymenium subepidermal (Fig. 21).
231
presence of rudimentary peridial cells, peripheral paraphyses, intercalary cells and sporogenous cells as follows.
.caeoma VI · caeoma I .caeoma III · caeoma II .caeoma IV · caeoma V
This type of aecium is produced on needles of coniferous plants distributed in the southern hemisphere or on witches' brooms of Asian conifers. Hymenia of Caeoma peltatum and C. deformans are indeterminate, whereas those of Mikronegeria alba are determinate. Spore chains of C. peltatum and M. alba are surrounded with thick pseudoparenchyma (Fig. 21). In M. alba, they are surrounded with another inner pseudoparenchyma lined with many small paraphyses (Fig. 22). Aecia of C. deformans, which causes witches' brooms of Thuja and Thujopsis, have neither pseudoparenchymata nor peripheral paraphyses.
Caeoma V (Figs 23, 24). Spores irregularly chained (Fig. 24), intercalary cells absent, sporogenous cells obscure, sori subepidermal, and both peridia and peripheral paraphyses absent (Fig. 23). Aecia of two species of Caeoma corresponding to this type (Table 1) rupture on witches' brooms, and their hymenia are indeterminate. In aecia of Caeoma radiatum, peripheral pseudo-parenchymata are well-developed, while another species, C. makinoi, has poor ones. Because only spores and pseudoparenchymata are present, the aecium of this type has been concluded to have the most simple structure. Caeoma VI (Figs 25, 26). Spores catenulate, intercalary cells present, hymenia intra-mesophyllie, hemispherical (Fig. 25), and both peridia and peripheral paraphyses absent. Zaghouania phillyreae is the only species of this type, and its hemispherical hymenia are essentially determinate. In the present studies, light and scanning electron microscopy of many specimens did not show any peridia in aecia of the species, although Dumee & Marie (1902) and Sydow & Sydow (1915) have described its ephemeral peridia.
232
Aecial morphology
Figs 19-24. For caption see opposite.
T. Sato and S. Sato Intercalary cells are between newly differentiated spores only (Fig. 26). Peripheral pseudo-parenchymata are poorly developed. Chrysocelis lupini Lagerh. & Dietel seems to have aecia corresponding to caeoma VI type (Dr Y. Ono, Ibaraki Univ., pers. comm.).
Uraecia U raecia, which are aecia with pedicellate spores, are divided into three types based on the presence of peridia and peripheral paraphyses.
peridium present, peripheral paraphyses absent peridium absent, peripheral paraphyses present both peridium and peripheral paraphyses absent
Uraecium I (Figs 27, 28). Spores pedicellate (Fig. 28), hymenium subepidermal, and sori peridiate with a single-layered peridium (Fig. 27). The parasol-shaped peridia of this type do not grow any more once the sorus has ruptured through a small pore at its apex, whereas the cylindrical peridia of other types with catenulate spores are continuously produced in basipetal succession from peridial basal cells surrounding hymenia during sporulation. One species of Thekopsora belonged to this type. It forms aecia with determinate hymenia on the lower surface of needles of Tsuga. Aecia of Thekopsora (Pucciniastrum) vaccinii (Wint.) Magnus (Hiratsuka, 1965) and Thekopsora hakkodensis S. Ito & Hiratsuka f. (Sato & Katsuya, 1979) appear to correspond to this type.
233
uraecium I uraecium II uraecium III
Uraecium II (Fig. 29). Spores pedicellate, hymenium subepidermal, and peripheral paraphyses present (Fig. 29). Hymenia of this type are indeterminate. This type contains species of Phragmidium (Table 1). Some other species of the genus have aecia belonging to caeoma III type (Table 1). Thus the genus Phragmidium is correlated with peripheral paraphyses in aecia. Uraecium III (Fig. 30). Spores pedicellate, hymenium subepidermal, and both peridia and peripheral paraphyses absent (Fig. 30). This type has indeterminate hymenia and the simplest structure among the pedicellate types of aecia.
KEY TO MORPHOLOGICAL TYPES OF AECIA
Spores catenulate 2. Intercalary cells present, sporogenous cells distinct 3. Peridium present, peripheral paraphyses absent 4. Peridium single-layered 5. Hymenium flat, intramesophyllic 6. Spore surface structure of the annulate type, spore germ pores obscure . 6. Spore surface structure of the coronate type, spore germ pores distinct
1.
peridermium I roestelia
Figs 19-24. Vertical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IPP, inner pseudoparenchyma; IS, immature spore; M, host rnesophyll; OPP, outer pseudoparenchyrna; PP, pseudoparencbyma; PR, peripheral paraphysis; SP, small lining paraphysis. Stainings: 19, aniline blue; 20, 23, 24, Flemming's triple stain; 21, 22, safranin-fast green. Scales: 19,22, 2 )tm; 20, 24, 1 )tm; 21, 23, 10 )tm.
Fig. Fig.
19. 20.
Caeorna III type of an aeciurn of Phragmidium rubi-idaei with incurved peripheral paraphyses (PR). A basal pan of caeoma I type of an aeciurn of Phragmidium montivagum.
Fig. 21. Caeorna IV type ofanaeciurn of Mikronegeria alba showing well-developed, two-layered pseudoparencbymata (OPP, IPP) around the aeciwn. Fig. 22. Peripheral inner pseudoparencbyrna (IPP) and outer one (OPP) lined with small paraphyses (SP) of M. alba. Fig.
23.
Caeoma V type of an aecium of Caeoma radiatum.
Fig. 24. A basal pan of an aeciurn of Caeoma makinoi with neither conspicuous sporogenous cells nor intercalary cells.
234
Aecial morphology
29 Figs 25-30. Vertical sections of aecium. Symbols: A, aecium; AS, aeciospore; E, host epidennis; H, hymenium; I, intercalary cell; IS, immature spore; P, peridium; PC, pedicel; PR, peripheral paraphysis; S, spennogonium. Stainings: 25, 27, 28, 30, Flemming's triple stain; 26, Heidenhain's haematoxylin and orange G; 29, no staining. Scales: 25,27,30, 10 pm; 26, 29, 2 pm; 28, 1 pm. Fig. 25. Caeoma VI type of an aecium of Zaghouania phillyreae with a hemispherically concave hymenium. Fig. 26. A basal part of an aecium of Z. phillyreae showing immature spores (IS) with intercalary cells (I). Fig. 27. Uraecium I type of an aecium of Thekopsora sp. bearing pedicellate spores. Fig. 28. Aeciospores (AS) of Thekopsora sp. produced on pedicels (PC). Fig. 29. Uraecium II type of an aecium of Phragmidium itoanum with peripheral paraphyses (PR). Fig. 30. Uraecium III type of an aecium of Uromyces truncicola (A) associated with a spennogonium (S).
T. Saw and S. Sata 6. Spore surface structure of the verrucose or nail-headed type, spore germ pores obscure 5. Hymenium flat, subepidermal 4. Peridium multi-layered, hymenium flat, intraconical . 3. Peridium absent, peripheral paraphyses present, hymenium flat, subepidermal . 3. Peridium and peripheral paraphyses absent 7. Hymenium concave hetnispherically, intramesophyllic 7. Hymenium flat, subepidermal 8. Rudimentary peridial cells present 8. Rudimentary peridial cells absent 2. Intercalary cells absent 9. Sporogenous cells distinct 9. Sporogenous cells obscure 1. Spores pedicellate 10. Peridium present, peripheral paraphyses absent . 10. Peridium absent, peripheral paraphyses present . 10. Both peridium and peripheral paraphyses present
235 aecidium . peridermium II peridermium III .caeoma III .caeoma VI · caeoma I · caeoma II .caeoma IV · caeoma V .uraecium I uraecium II uraecium III
DISCUSSION
The morphological types of aecia described herein correspond well with rust genera. Of fourteen genera in which more than two species were examined, all of the species iIi 'each of Uredinopsis, Pucciniastrum, Chrysomyxa, Coleosporium, Cronartium, Gymnosporangium, Puccinia, Phakopsora and Pucciniostele had the same type of aecia (Table 2), while two aecial types were recognized in each of Thekopsora, Uromyces, Phragmidium, Melampsora and Caeoma (Table 2). Related genera often possess the same aecial type. Aecia of Uredinopsis, Milesina, Hyalopsora, Melmpsorella, Thekopsora, Pucciniastrum and CalYPtospora belonging to Pucciniastraceae (Savile, 1976; Cummins & Hiratsuka, 1983) all correspond to peridermium I type. Two phragmidiaceous genera, Phragmidium and Xenodochus, parasitic on rosaceous plants, possess caeoma III aecia, and two coleosporiaceous genera (Cummins & Hiratsuka, 1983), Coleosporium and Chrysomyxa with caeomoid uredinia, form peridermium II aecia. Moreover, Puccinia, Uromyces and Miyagia, which Savile (1976) put together in a subgroup in the Pucciniaceae, have the aecidium type of aecia, and two phakopsoraceous genera, Cerotelium and Phakopsora (Cummins & Hiratsuka, 1983), also produce the aecidium-type aecia. Aecia of the uraecium types are morphologically similar to uredinia of the same species. The species with uraecium types except for uraecium I are all autoecious. It is possible that they have ceased to produce aecia with catenulate spores, and thus sori with pedicellate spores identical to uredinia have replaced the aecial state in the course of simplification of the life cycle, as suggested by Jackson (193 1). If such a simplification actually took place, it is likely that uraecium II or uraecium III aecia coexist with another type of aecium within single
genera, e.g. Phragmidium and Uromyces (Table 2). The heteroecious species of Thekopsora examined in the present study (T. (Pucciniastrum) vaccinii and T. hakkodensis) with uraecium I aecia seem to have little phylogenetic affinity with other species of the genus because of fundamental differences between their aecial morphology. The aecial types are interrelated with aeciospore surface-structure types (Sato & Sato, 1982; Table 2). Aeciospores of peridermium I, II and III all correspond to the annulate type. Roestelia, caeoma V and caeoma VI are characterized by coronate, aciculate and reticulate types of aeciospores, respectively. Verrucose types of aeciospore are distributed among aecidium, caeoma I, II, IV and V, while echinulate types are observed in caeoma III, uraecium I, II and III. Only one species of the aecidium type and a genus of caeoma II type have nail-headed and tubulate types of spores, respectively. In the present study, the spermogonial types (Hiratsuka & Cummins, 1963; Hiratsuka & Hiratsuka, 1980) of the representative species were also examined and are listed in Tables 1 and 2. The majority of the aecial types correspond to single spermogonial groups, but in the aecidium, caeoma II and uraecium III types, two to three groups of spermogonial types are found (Table 2). This suggests that aecia have not always co-evolved with spermogonia, though they usually associate closely with each other in rust life cycles (Fig. 30). Considering the differences in their function, it is not surprising that their morphological types do not always correlate. According to Cummins & Hiratsuka (1983), about 70 genera are known to have aecial states. Aecia of only 33 genera of these have been
Aecial morphology
236
.-<'
I
L~'"
~~
1\\
Peridermium-Il
\.
I rJ.
Peridermium-l ~
7(;~~
...
~ 1 f
11]
II[
.llI\
r'A
I I
I
Roestelia
Peridermium-III
~
•,
'0 f
Caeoma-I
Aecidium
Fig. 31. For caption see opposite.
examined in the present study. In those genera not examined, there may be aecial types not corresponding to any. of the 14 types recognized here, for example Hiratsukamyces and Elateraecium. Recently, Cummins & Hiratsuka (1983) adopted Elateraecium as representative of a new type of aecium_ Obviously, further studies on aecial morphology of genera and species not examined in the present study are necessary, not only for the phylogenetic discussion of aecial types but also for taxonomic revision of form genera of aecial states. It is concluded that morphological types of aecia correlate with rust genera, reflect relationships between genera, and appear to be very important for studies of natural classification and phylogeny of the Uredinales.
The authors wish to express their thanks to Dr Y. Hiratsuka, Northern Forest Research Centre, Canadian Forestry Service, and to Dr K. Katsuya, Dr K. Tubaki and Dr M. Kakishima, University of Tsukuba, for valuable advice and criticism rendered during the course of this work and the preparation of the manuscript. Thanks are also due to Dr N. Hiratsuka and Dr S. Kaneko, Tonori Mycological Institute, Dr T. Kobayashi, Dr H. Sabo and Dr T. Hama, Forestry and Forest Products Research Institute, Dr Y. Harada, Hirosaki University and Dr Y.Ono, Ibaraki University for material and literature used in this work. Contribution no. 44, Laboratories of Plant Pathology and Mycology, Institute of Agriculture and Forestry, University of Tsukuba. An outline of
T. Sata and S. Sata
2 37
"1r---11'--"'I_,"'~""'T"'-I"""'Ir-"I"" f~fY t
Caeoma-III
Caeoma-I1
Caeoma-IV
Caeoma-V
Caeoma-VI
Uraecium-I
'TI--'-I--'-l-~ IYI y I rf~
Uraecium-I1
Uraecium·II1
Fig. 31. Schematic illustrations of the morphological types of aeeia.
this paper entitled 'Morphology of aecia in the Uredinales' appeared in Rep. Tottori Mycol. Inst. n, 133-140 (1984) as part of the proceedings of the Third International Mycological Congress.
REFERENCES
BLACKMAN, V. H. (1904). On the fertilization, alternation of generation and general cytology of the Uredineae. Annals of Botany 18, 323-373. BLACKMAN, V. H. & FRASER, H. C. I. (1906). Further studies on the sexuality of the Uredineae. Annals of Botany ZO, 35-47. CHRISTMAN, A. H. (1905). Sexual reproduction in the rusts. Botanical Gazette 39, 267-275. CHRISTMAN, A. H. (1907). The nature and development ofthe primary urcdospore. Transactions of the Wisconsin Academy of Sciences, Arts and Letters 15,517-526. CoLLEY, R. H. (1918). Parasitism, morphology, and cytology of Cronartium rihicola. Journal of Agricultural Research 15, 619'-659. CuMMINS, G. B. (1959). Illustrated Genera of Rust Fungi. Minneapolis, U.S.A.: Burgess.
CUMMINS, G. B. & HIRATSUKA, Y. (1983). Illustrated Genera of Rust Fungi, revised edition. St Paul, Minn.: the American Phytopathological Society. DUMEB, P. & MARIE, R. (1902). Remarques sur Ie Zaghouania phillyreae Pat. Bulletin de La Societe Mycologique de France 18, 17-24. FROMME, F. D. (1912). Sexual fusions and spore development of the flax rust. Bulletin of the Torrey Botanical Club 39, 113-131. FROMME, F. D. (1914). The morphology and cytology of the aecidium cup. Botanical Gazette 58, 1-35. HJ!NNllN, J. F. & BURITICA, P. (1980). A brief summary of modem rust taXonomy and evolutionary theory. Report of the Tottori Mycological Institute (Japan) 18, 2 43-2 56 . HIRATSUICA, N. (1955). Uredinological Studies. Tokyo: Kasai. HIRATSUKA, Y. (1965). The identification of Uraecium holwayi on hemlock as the aecial state of Pucciniastrum vaccinii in western North America. Canadian Journal of Botany 43, 475-478. HIRATSUICA, Y. (1973). The nuclear cycle and the tertninology of spore states in Uredinales. Mycologia 6 5,432-443·
Aecial morphology HIRATSUKA, Y. & CUMMINS, G. B. (1963). Morphology of the spermogonia of the rust fungi. Mycologia 55, 4 87-507.
HIRATSUKA, Y. & HIRATSUKA, N. (1980). Morphology of spermogonia and taxonomy of rust fungi. Report of the Tottori Mycological Institute (Japan) 18,257-268. HIRATSUXA, Y. & SATO, S. (1982). Morphology and taxonomy of rust fungi. In The Rust Fungi (ed. K. J. Scott & A. K. Chakravorty), pp. 1-36. London: Academic Press. JACKSON, H. S. (1931). Present evolutionary tendencies and the origin of life cycles in the Uredinales. Memoirs of the Torrey Botanical Club 18, 1-108. KENNY, M. J. (1970). Comparative morphology of the uredia of the rust fungi. Ph.D. Thesis, Purdue University. KERN, F. D. (1910). The morphology of the peridial cells in the Roesteliae. Botanical Gazette 49, 445-451. KERN, F. D. (1973). A Revised Taxonomic Account of Gymnosporangium. University Park, Penn.: Pennsylvania State University Press. KURSANOV, L. (1922). Recherches morphologiques et cytologiques sur les Uredinees. Bulletin de la Societe Nationale de Moscou 31, 1-109. LAUNDON, G. F. (1967). The taxonomy of the imperfect rusts. Transactions ofthe British Mycological Society 50, 34tr353·
PETERSON, R. S. (1967). The Peridermium species on pine stems. Bulletin of the Torrey Botanical Club 94, 5 11 -542 . PETERSON, R. S. (1974). Rust fungi with Caeoma-like sori on conifers. Mycologia 66, 242-255.
PETERSON, R. S. & OEHRENS, E. (1978). Mikronegeria alba (Uredinales). Mycologia 70, 321-331. SAPPIN-TROUFFY, M. (1896). Recherches histologiques sur la famille des Uredinees. Le Botaniste 5, 5tr244· SATO, S. & KATSUYA, K. (1979). Heteroecism of two rust fungi on the needles of Tsuga diversifolia and T. sieboldii. Transactions of the Mycological Society of Japan 20,1-4. SATO, T. & SATO, S. (1980). The caeomoid uredinium of Xenodochus carbonarius (Uredinales). Transactions of the Mycological Society ofJapan 21, 411-416. SATO, T. & SATO, S. (1982). Aeciospore surface structure of the Uredinales. Transactions of the Mycological Society of Japan 23, 51-63. SAVILE, D. B. O. (1976). Evolution of the rust fungi (Uredinales) as reflected by their ecological problems. Evolutionary Biology 9,137-207. SHAW, C. G. III (1976). Rust on Phyllocladus trichomanoides - the first recorded on a member of the Podocarpaceae. Transactions of the British Mycological Society 67,506-509. SINGH, B. V. (1969). Studies on aecial development in rust fungi, Puccinia polliniae. Canadian Journol of Botany 47, 741-744. SYDOW, P. & SYDOW, H. (1915). Monographia Uredinearum, 3, 58tr590. Leipzig: Fratres Borntrager. THIRUMALACHAR, M. J., KERN, F. D. & PATIL, B. V. (1966). Elateraecium, a new form genus of Uredinales. Mycologia 58, 391-396. THIRUMALACHAR, M. J., KERN, F. D. & PATIL, B. V. (1973). Hiratsukamyces, a new genus of the Pucciniastreae. Sydowia 27, 78--81.
(Received for publication
11
October 1984)
Printed in Great Britain
MORPHOLOGY OF AECIA OF THE RUST FUNGI By TOYOZO SATO· AND SHOJI SATO Institute of Agriculture and Forestry, University of Tsukuba, Sakura-mura, Niihari-gun, Ibaraki 305, Japan Using light and scanning electron microscopy, comparisons of aecial states of 80 species belonging to 33 genera of rust fungi were made. Aecia were classified into 14 morphological types on the basis of spore ontogeny, shape of hymenium, position of hymenium in host tissues, presence of intercalary cells, presence of sporogenous cells, presence and number of layers of peridium, presence of peripheral paraphyses, aeciospore surface structure, and germ pores of spores. Peridermia, roestelia and aecidium could be distinguished by spore surface structure. The three traditional types, peridermium, caeoma and uraecium were divided into 3,6 and 3 types, respectively. Related genera were often included in one aecial type of the 14 aecial types recognized. Aecial morphology is important in the natural classification and phylogeny of the Uredinales. Since Brongniart recognized the rust fungi as an order' U redinees ' , a number of taxonomic systems have be~n proposed (Hiratsuka, 1955; Hennen & Buritica, 1980). Most of these have been based on the morphology of the mature telial state, with little regard for characters of other spore states. During the last two decades spermogonia (Hiratsuka & Cummins, 1963; Hiratsuka & Hiratsuka, 1980) and uredinia (Kenny, 1970) have been studied in detail throughout the Uredinales, and it has been pointed out that morphology of spermogonia and uredinia are significant for supraspecific classification as well as for discussions on intergeneric relationships in the Uredinales. However, there has been no report of morphological comparisons of the aecial states throughout the order, though numerous studies of aecial ontogeny and morphology of individual species or genera have been reported since 1896 (Sappin-Trouffy, 1896; Blackman, 1904; Christman, 1905, 1907; Blackman & Fraser, 1906; Kern, 1910, 1973; Fromme, 1912, 1914; Colley, 1918; Kursanov, 1922; Thirumalachar, Kern & PatH, 1966; Peterson, 1967, 1974; Singh, 1969; Sato & Katsuya, 1979). Laundon (1967) proposed an aecial classification based on macroscopic morphology of aecia, their host plants, host organ bearing them, and spermogonial characters. Five types of aecia, namely peridermioid, roestelioid, aecidioid, caeomoid and uredinoid, have been generally accepted (Cummins, 1959; Hiratsuka & Sato, 1982).. Precise morphological definition of these types, however, has not been
* Present address: Ogasawara Subtropical Agriculture Center, Chichi-jima Is., Ogasawara-mura, Tokyo 100-21, Japan.
possible, and some of them appear to contain several different types (Peterson, 1974). Cummins (1959) defined the aecidioid, peridermioid and roestelioid aecia by 'gentleman's agreement', because they were difficult to define and separate purely on morphological bases. Hiratsuka & Sato (1982) pointed out that the caeomoid type contained aecia with rudimentary peridial cells or with peripheral paraphyses besides naked ones. In the present study, morphological comparisons of aecial states of rust fungi mainly collected in Japan were carried out to clarify morphological differences among the aecial types and to reclassify them. The present paper follows the definition of aecial state in the 'ontogenic system' (Hiratsuka, 1973). In the present paper the words peridermium, roestelia, aecidium, caeoma and uraecium do not represent anamorphic generic names but five morphologically different spore-producing structures that may occur in the aecial position in rust life cycles. MA TBRIALS AND METHODS
Fresh material fixed with FAA or dry herbarium specimens of aecia of 80 species in 33 rust genera listed in Table 1 were sectioned with a microtome or by hand, and stained for observation by light microscopy. The FAA-fixed materials were dehydrated by ethanol and xylene series, embedded in paraffin and sectioned at 15-20 pm. Sections were stained with Flemming's triple stain orHeidenhain's iron alum haematoxylin and orange-G double stain after the paraffin had been dissolved in two changes of xylene, and mounted in Canada balsam on glass slides. Dry herbarium material of some species was
Aecial morphology
224
Table
1.
Aecial types of rust species examined
Species Aecidium foetidum Diet.
Caeoma deformans (Berk. & Br.) Tubeuf Caeoma makinoi Kusano Caeomapeltatum C.G. Shaw III & c. G. Shaw Caeoma radiatum Shirai Calyptospora goeppertiana KUhn Ceraceopsora elaeagni Kakishima et al. Cerotelium dicentrae Mains & Anderson Chrysomyxa succirrea (Sacc.) Tranz. Chrysomyxa woroninii Tranz. Coleosporium asterum (Diet.) P. & H. Sydow Coleosporium bletiae Diet. Coleosporium clematidis Barclay Coleosporium clematidis-apiifoliae Diet. Coleosporium eupatorii Hiratsuka f. Coleosporium horianum Hennings Coleosporium paederiae Diet. ex Hiratsuka f. Coleosporium phellodendri Komarov Cronartium kamtschaticum Jerstad Cronartium ribicola Fischer d. Waldh. Gymnoconia peckiana (Howe) Trotter Gymnosporangium asiaticum Miyabe ex Shirai Gymnosporangium miyabei Yamada & I. Miyake Gymnosporangium yamadae Miyabe ex Tanaka Hyalopsora aculeata Kamei Leucotelium pruni-persicae (Hori) Tranz. Melampsora abietis-populi S. Imai ex S. Ito Melampsora chelidoni-pierotii Matsumoto Melampsora larici-capraearum Kleb. Melampsora larici-populina Diet. Melampsora occidentalis Jackson Melampsora yezoensis Miyabe & Matsumoto Melampsorella caryophyllacearum Schrot. Melampsoridium hiratsukanum S. Ito ex Hiratsuka f. Mikronegeria alba Oehrens & Peterson Milesina sp. Miyagia anaphalidis Miyabe ex P. & H. Sydow Nyssopsora cedrelae (Hori) Tranz. Ochropsora kraunhiae (Diet.) Diet. Phakopsora ampelopsidis Diet. & P. Sydow Phakopsora meliosmae Kusano Phragmidium itoanum Hiratsuka f. Phragmidium montivagum Arthur Phragmidium rosae-multiflorae Diet. Phragmidium rubi-idaei (DC.) Karsten Phragmidium rubi-thunbergii Kusano Pileolaria klugkistiana Diet. Puccinia caricis-petasitidis Y. Harada Puccinia coronata Corda Puccinia crepidis-japonicae Diet. Puccinia dieteliana P. Sydow Puccinia graminis Pers.
Specimen no. TS-R 1125 TS-R 1002 TS-R 1003 TS-R 1004 TS-R 1006 TS-R 1126 TS-R 1008 TS-R 1086 TS-R 1082 TS-R 1087 TS-R 1010 TS-R 1011 TS-R 1116 TS-R 1123 TS-R 1090 TS-R 1091 TS-R 1015 TS-R 1014 TS-R 1092 TS-R 1093 TS-R 1016 TS-R 1018 TS-R 1020 TS-R 1096 TS-R 1097 TS-R 1021 TS-R 1024 TS-R 1101 TS-R 1026 TS-R 1027 TS-R 1028 TS-R 1127 TS-R 1029 TS-R 1102 TS-R 1103 TS-R 1104 TS-R 1105 TS-R 1128 TS-R 1032 TS-R 1107 TS-R 1124 TS-R 1033 TS-R 1034 TS-R 1123 TS-R 1037 TS-R 1038 TS-R 1040 TS-R 1113 TS-R 1042 TS-R 1043 TS-R 1114 TS-R 1046 TS-R 1047 TS-R 1117 TS-R 1120 TS-R 1048 TS-R 1050 TS-R 1085
Spermogonial type (group)· Aecial type 4 (V) Aecidium 4 (V) Aecidium 12 (III) Caeoma IV 12 (III) Caeoma IV 4 (V) Caeoma V 12 (III) Caeoma IV 4 (V) Caeoma V ? Peridennium I 7 (VI) Aecidium 7 (VI) Aecidium 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridermium II 2 (I) Peridermium II 2 (I) Peridermium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II 2 (I) Peridennium II Peridermium III 9 (II) Peridermium III 9 (II) 6 (IV) Caeoma II 6 (IV) Caeoma II Roestelia 4 (V) Roestelia 4 (V) Roestelia 4 (V) 2 (I) Peridennium I 7 (VI) Aecidium Caeoma II 3 (I) Caeoma II 3 (I) Caeoma I 3 (I) Caeoma I HI) Caeoma I 3 (I) Caeoma I 3 (I) Caeoma I 3 (I) Caeoma II 3 (I) Peridermium I 3 (I) Peridermium II 3 (I) Caeoma IV 12 (III) Peridermium I 1 (I) Aecidium 4 (V) Uraecium III Aecidium 7 (VI) Aecidium 7 (VI) Aecidium 7 (VI) 10 (IV) Uraecium II 11 (IV) Caeoma III Caeoma III ? ? Caeoma III 10 (IV) Uraecium II Uraecium III 7 (VI) Aecidium 4 (V) 4 (V) Aecidium Aecidium 4 (V) Aecidium 4 (V) Aecidium 4 (V)
T. Sato and S. Sato Table Species Puccinia linosyridi-caricis Ed. Fischer Puccinia m;scanthi Miura Puccinia nolitangeris Corda Puccinia osmorrhizae Cooke & Peck Puccinia podophylli Schw. Puccinia polygoni-amphibii Pers. Puccinia pulchella Ono & Kakishima Puccinia punctata Link Puccinia recondita Roberge ex Desm. Puccinia zoysiae Diet. Pucciniastrum fag; Yamada Pucciniastrum kusanoi Diet. Pucciniastrum tiliae Miyabe ex Hiratsuka Pucciniostele clarkiana (Barel.) Diet. Pucciniostek mandschurica Diet. Thekopsora areolata (Fr.) Magnus Thekopsora sp. Tranzschelia pruni-spinosae (Pers.) Diet. Triphragmium ulmariae Link Uredinopsis jilicina Magnus Uredinopsis komagatakensis Hiratsuka f. Uromyces amurensis Komarov Uromyces erythronii Passerini Uromyces heimelianus Magnus Uromyces truncicola Hennings & Shirai Uromyces f)iciae-fabae (Pers.) Swot. Xenodochus carbonarius Schlecht. Zaghouania phillyreae Pat.
1
225
(Cont.)
Specimen no. TS-R 216 TS-R 1051 TS-R 1084 TS-R 1052 TS-R 1053 TS-R 1118 TS-R 1055 TS-R 1056 TS-R 1083 TS-R 1057 TS-R 1121 TS-R 1058 TS-R 1059 TS-R 1115 TS-R 1060 TS-R 1062 TS-R 1063 TS-R 1109 TS-R 1069 TS-R 1110 TS-R 1111 TS-R 1070 TS-R 1112 TS-R 1072 TS-R 1073 TS-R 1074 TS-R 1076 TS-R 1077 TS-R 1122 TS-R 1078 TS-R 1080
Aecial type Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Aecidium Peridermium I Peridermium I Peridermium I Peridermium I Caeoma II Caeoma II Peridermium I Uraecium I Aecidium Aecidium Uraecium II Peridermium I Peridermium I Aecidium Aecidium Aecidium Uraecium III Aecidium Caeoma III Caeoma VI
Spermogonial type (group)"* 4 4 4 4 4
(V) (V) (V) (V) (V)
? 4 (V)
4 (V) 4 (V) 4 (V) 3 (I) 3 (I) 3 (I) 3 (I) 7 (VI) 7 (VI) 3 (I) 3 (I) 7 (VI) 7 (VI) 11 (IV) 3 (I) 2 (I) 4 (V)
4 (V) 4 (V) 4 (V) 4 (V) 10 (IV) 4 (V)
"* Mter Hiratsuka & Hiratsuka (1980).
also examined under a scanning electron microscope (SEM). Small pieces of the leaves bearing aecia or aeciospores only were placed on double adhesive tape on specimen holders, and coated with gold under a high vacuum with an Eiko IB-3 ion coater. The preparations were examined under a Hitachi S-430 SEM operating at 20 kV. RESULTS
The following characters of the aedal state were examined in detail: (1) spore ontogeny, (2) shape of hymenium, (3) position of hymenium in host tissues, (4) lateral growth of hymenium, (5) presence of intercalary cells, (6) presence of sporogenous cells, (7) presence of number of layer(s) of peridium, (8) presence and peripheral paraphyses, (9) germ pores ofspores, and (10) spore surface structure. These seemed to be stable characters of aeda. The lateral growth of hymenia 8
appeared to depend on the position of hymenia formed in host tissues. Aecia were classified into 14 morphological types (Fig. 31) on the basis of the nine characters listed above except for the lateral growth ofhymenia. The morphological types of aecia of species examined are listed in Table 1, and genera included in each type are listed in Table 2. Descriptions ofthe types follow. Peridermium Aecia recognized previously as of the peridermioid type could be divided into three morphological types mainly on the basis of hymenial positions in host tissues: intramesophyllic, peridermium I; subepidermal, peridermium II; intracortical, peridermium III. Peridermium I (Figs 1-3). Spores catenulate, spore surface structure of the annulate type (Sato & Sato, 1982), germ pores obscure, intercalary cells present MYC
85
Aecial morphology
226 Table
2.
Aeciospore surface-structure types, groups of spermogonial types and rust genera corresponding to the aecial types
Aecial type Peridermium I
Aeciospore surfacestructure type Annulate
Peridermium II
Annulate
I
Peridermium III Roestelia
Annulate Coronate Coronate and verrucose Verrucose
II V V
Verrucose
VI
Nail-headed Verrucose Verrucose Verrucose Tubulate Echinulate
VI I I IV VI IV
Verrucoset Verrucose and aciculate Nail-headed:j: Verrucose Aciculate Reticulate Echinulate Echinulate Echinulate§ Echinulate§ Echinulate§
III III
Aecidium
Caeoma I Caeoma II Caeoma III Caeoma IV
Caeoma V Caeoma VI Uraecium I Uraecium II Uraecium III
(Ridgy) II
Group of spermogonial type*
V
III V V V I IV V IV VI
Rust genus (no. of species examined) Calyptospora (1), Hyalopsora (1), Melampsorella (1), Milesina (1), Pucciniastrum (3), Thekopsora (1), Uredinopsis (2) Chrysomyxa (2), Coleosporium (8), Melampsoridium (1) Cronartium (2) Gymnosporangium (2) Gymnosporangium (1) Aecidium (1), Miyagia (1), Uromyces (4), Puccinia (14) Cerotelium (1), Leucotelium (1), Ochropsora (1), Phakopsora (1), Tranzschelia (1), Ceraceopsora (1) Phakopsora (1) Melampsora (3) Melampsora (3) Gymnoconia (1) Pucciniostele (2) Phragmidium (3), Xenodochus (1) Mikronegeria (1) Caeoma (1) Caeoma (1) Caeoma (1) Caeoma (1) Zaghouania (1) Thekopsora (1) Phragmidium (2) Uromyces (1) Triphragmium (1) Nyssopsora (1) Pileolaria (1)
* After Hiratsuka & Hiratsuka (1980). t After Peterson & Oehrens (1978). :j: After Shaw (1976). § Determined by light microscopy only. II Not contained in the aeciospore surface-structure types (Sato & Sato, 1982) because of lack of SEM observations.
Figs 1--6. Venical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IS, immature spore; M, host mesophyll; P, peridium; PC, peridial cell; PP, pseudoparenchyma; SC, sporogenous cell. Stainings: 1,2,3,4,6, Heidenhain's haematoxylin and orange G; 5, Flemming's triple stain. Scales: 1,4, 10llm; 2, 3, 1llm; 5, 6, 21lm. Fig. 1. Peridermium I type of an aecium of Pucciniastrum fagi showing an intramesophyllic hymenium' (H). Fig. 2. Basal periphery of peridermium I type of an aecium of Milesina sp. Fig. 3. Peridial cells (PC) of Milesina sp.
T. Sata and S. Sata
227
Fig. 4. Peridermium II type of an aecium of Chrysomyxa succinea showing a subepidermal hymenium (H). Fig. 5. Basal periphery of peridermium II type of aecium of Coleosporium eupalorii. Fig. 6. A basal part of peridermium II type of an aecium of Ch. succinea, 8-2
228
Aecial morphology
PO
8
....... . ~
.... ;.
Figs 7-13. For caption see opposite.
T. Sato and S. Sato (Fig. 2), hymenium intramesophyIlic, sori peridiate with single-layered peridia (Fig. 3), inner walls of peridial cells usually thicker than outer walls (Fig. 3). This type of aecium is formed in two rows on the lower surface of needles of coniferous plants, and lateral growth of their hymenia is so detertninate that aecial shapes are slenderly cylindrical except for aecia of Thekopsora areolata. Peridermium I is similar to the roestelia and aecidium types, but these three types are clearly distinguished by spore surface structures. Aeciospores of peridermium I, roestelia and aecidium types correspond toannulate, coronate and verrucose or nail-headed surface structure types, respectively (Sato & Sato, 1982).
PerUkrmium II (Figs 4~). Spores catenulate (Figs 4, 5), intercalary cells present (Figs 5, 6), hymenium subepidermal (Fig. 4), and sori peridiate with single-layered peridium (Fig. 5). In this type, lateral growth of hymenia is so indeterminate longitudinally on ne~es of coniferous plants that aecia like tongues or pillows develop (Fig. 4). Conspicuous palisade-like pleetenchymata under the epidermis surround the aecial margin of Coleosporium spp. examined. Peridermium III (Figs 7-9). Spores catenulate (Fig. 9), intercalary cells present (Fig. 9), hymenia intracortical (Fig. 7), and sori peridiate with multi-layered peridia (Fig. 8). This type of aecium was produced on trunks or branches of Pinus, and shape of hymenia depends on that of the host tissue bearing them because of the indeterminate nature of their lateral growth. Peridia of Cronartium ribieola were composed of 2-3 layers of cells, while those of C. kamtschaticum were 2- to 4-layered (Fig. 8). Pseudoparenchymata were well-developed beneath and around the sori of both species (Fig. 7).
229
Roestelia Spores catenulate (Fig. 11), spore surface structure of the coronate type, germ pores conspicuous (Fig. 13), intercalary cells present (Fig. 11), hymenium intramesophyllic (Fig. 10), sori peridiate with single-layered peridia (Fig. 12), inner walls of peridial cells usually thicker than outer ones (Fig. 12). Comute to cylindrical aecia of this type elongate from the lower surface of host leaves, and their determinate hymenia are seated in a deep portion of hypertrophied mesophyll (Fig. 10). Chains composed of immature spores and cylindrical to string-like intercalary cells are characteristically long (Fig. 11). Aecidium Spores catenulate, spore surface structure verrucose or of the nail-headed type, germ pores obscure or conspicuous, intercalary cells present, hymenium intramesophyIlic, sori peridiate with single-layered peridium (Fig. 14), inner walls of peridial cells usually thinner than outer one (Fig. 15). Hymenia·ofthis type are detertninate in general though some of the aecidioid aecia, e.g. Puccinia osmorrhizae and Uromyces erythronii, show considerable variation of hymenial size. In Puccinia crepidis-japonicae, Phakopsora meliosmae and Miyagia anaphalidis, inner walls of peridial cells are thicker than outer ones, and coherence of peridial cells of P. osmorrhizae and Ph. meliosmae is weak. Intercalary cells of the aecidium type are flat to wedge-shaped. Spore surface structure of all species of this type corresponds to the verrucose type except for those of Ph. meliosmae, as reported previously (Sato & Sato, 1982).
Figs 7-13. Vertical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IN, inner wall; IS, immature spore; M, host mesophyll; 0, outer wall; P, peridium; PO, host periderm; PP, pseudoparenchyma; T, host tissue. Stainings: 7, 8, 9,10,11,13, Flemming's triple stain; 12, Heidenhain's haematoxylin and orange G. Scales: 7, 10, :zo pm; 8, :1 pm; 9, 11, 12, 13, 10 pm. Fig. 7. Peridermium III type of an aecium of Cronartium kamtschaticum showing an intracortical hymenium (H). Fig. 8. A two- to three-layered peridium of C. kamtschaticum. Fig. 9. A basal part of an aecium of C. kamrschaticum. Fig. 10. Roestelia type of an aecium of Gymnosporangium asiaticum. Fig. 11. A basal part of an aecium of G. asiaticum showing elongated intercalary cells (I). Fig. 12. A peridial cell (PC) of G. asiaticum showing inner wall (IN) thicker than outer one (0). Fig. 13. Aeciospores of G. asiaticum with conspicuous germ pores.
2~O
Aecial morphology
-AM
Figs 14-18. Vertical sections and a scanning electron micrograph (16) of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; M, host mesophyll; P, peridium; PC, peridial cell; PP, pseudoparenchyma; RP, rudimentary peridial cell. Stainings: 14, lS, Heidenhain's haematoxylin and orange G; 17, no staining; 18, Flemming's triple stain. Scales: 14, 17, 18, 10,um; 16, 20,urn; lS, l,urn. Fig. 14. Aecidium type of an aecium of PUCciM pulchella. Fig. lS. A peripheral part of an aecium of P. pulchella. Fig. 16. A scanning electron micrograph of caeorna I type of an aecium of Melampsora occidentalis showing peripheral rudimentary peridial cells (RP). Fig. 17. Caeoma I type of an aecium of M. occidentalis. Fig. 18. Caeoma II type of an aecium of Pucciniosrele mandschurica.
T. Sato and S. Sato Caeoma Non-peridiate aecia with catenulate spores, currently lumped together under the anamorphic genus Caeoma, could be divided into six morphological types on the basis of shape of hymenia, Intercalary cells present Hymenia hemispherical. Hymenia flat Rudimentary peridial cells present Rudimentary peridial cells absent Peripheral paraphyses present Peripheral paraphyses absent . Intercalary cells absent Sporogenous cells conspicuous Sporogenous cells obscure
Caeoma I (Figs 16, 17). Spores catenulate, intercalary cells present, hymenia subepidermal, and rudimentary peridial cells present around sori (Fig. 16). This type of aecium is formed on the lower surface of needles of coniferous plants, where the hymenia are longitudinally indeterminate. Coherence of the rudimentary peridial cells was different among the species. Three- to four-celled pieces of peridium were observed in aecia of Melampsora larici-capraearum, while the peridial cells loosely lined aecia of M. larici-populina and M. occidentalis. Such variation may suggest that caeoma I is a transitional type between peridermium II and caeoma II described below. Caeoma II (Fig. 18). Spores catenulate, intercalary cells present, hymenium flat and subepidermal, and both peridia and paraphyses absent (Fig. 18). Hymenia ofthis type are indeterminate. Though this type lacks peridia, in the three species of Melampsora and Pucciniostele clarkiana subepidermal pseudoparenchyma was well-developed around the sori (Fig. 18). Caeoma III (Figs 19, 20). Spores catenulate, intercalary cells present, hymenium subepidermal, and peripheral paraphyses present (Fig. 19). This type of aecium is produced on rosaceous plants, and the hymenium develops indeterminately. Large, incurved peripheral paraphyses surround aecia of Phragmidium rubi-idaei (Fig. 19), whereas paraphyses of Xenodochus carbonarius are relatively small and cylindrical, as reported by Sato & Sato (1980). Caeoma IV (Figs 21, 22). Spores catenulate, intercalary cells absent, sporogenous cells conspicuous, hymenium subepidermal (Fig. 21).
231
presence of rudimentary peridial cells, peripheral paraphyses, intercalary cells and sporogenous cells as follows.
.caeoma VI · caeoma I .caeoma III · caeoma II .caeoma IV · caeoma V
This type of aecium is produced on needles of coniferous plants distributed in the southern hemisphere or on witches' brooms of Asian conifers. Hymenia of Caeoma peltatum and C. deformans are indeterminate, whereas those of Mikronegeria alba are determinate. Spore chains of C. peltatum and M. alba are surrounded with thick pseudoparenchyma (Fig. 21). In M. alba, they are surrounded with another inner pseudoparenchyma lined with many small paraphyses (Fig. 22). Aecia of C. deformans, which causes witches' brooms of Thuja and Thujopsis, have neither pseudoparenchymata nor peripheral paraphyses.
Caeoma V (Figs 23, 24). Spores irregularly chained (Fig. 24), intercalary cells absent, sporogenous cells obscure, sori subepidermal, and both peridia and peripheral paraphyses absent (Fig. 23). Aecia of two species of Caeoma corresponding to this type (Table 1) rupture on witches' brooms, and their hymenia are indeterminate. In aecia of Caeoma radiatum, peripheral pseudo-parenchymata are well-developed, while another species, C. makinoi, has poor ones. Because only spores and pseudoparenchymata are present, the aecium of this type has been concluded to have the most simple structure. Caeoma VI (Figs 25, 26). Spores catenulate, intercalary cells present, hymenia intra-mesophyllie, hemispherical (Fig. 25), and both peridia and peripheral paraphyses absent. Zaghouania phillyreae is the only species of this type, and its hemispherical hymenia are essentially determinate. In the present studies, light and scanning electron microscopy of many specimens did not show any peridia in aecia of the species, although Dumee & Marie (1902) and Sydow & Sydow (1915) have described its ephemeral peridia.
232
Aecial morphology
Figs 19-24. For caption see opposite.
T. Sato and S. Sato Intercalary cells are between newly differentiated spores only (Fig. 26). Peripheral pseudo-parenchymata are poorly developed. Chrysocelis lupini Lagerh. & Dietel seems to have aecia corresponding to caeoma VI type (Dr Y. Ono, Ibaraki Univ., pers. comm.).
Uraecia U raecia, which are aecia with pedicellate spores, are divided into three types based on the presence of peridia and peripheral paraphyses.
peridium present, peripheral paraphyses absent peridium absent, peripheral paraphyses present both peridium and peripheral paraphyses absent
Uraecium I (Figs 27, 28). Spores pedicellate (Fig. 28), hymenium subepidermal, and sori peridiate with a single-layered peridium (Fig. 27). The parasol-shaped peridia of this type do not grow any more once the sorus has ruptured through a small pore at its apex, whereas the cylindrical peridia of other types with catenulate spores are continuously produced in basipetal succession from peridial basal cells surrounding hymenia during sporulation. One species of Thekopsora belonged to this type. It forms aecia with determinate hymenia on the lower surface of needles of Tsuga. Aecia of Thekopsora (Pucciniastrum) vaccinii (Wint.) Magnus (Hiratsuka, 1965) and Thekopsora hakkodensis S. Ito & Hiratsuka f. (Sato & Katsuya, 1979) appear to correspond to this type.
233
uraecium I uraecium II uraecium III
Uraecium II (Fig. 29). Spores pedicellate, hymenium subepidermal, and peripheral paraphyses present (Fig. 29). Hymenia of this type are indeterminate. This type contains species of Phragmidium (Table 1). Some other species of the genus have aecia belonging to caeoma III type (Table 1). Thus the genus Phragmidium is correlated with peripheral paraphyses in aecia. Uraecium III (Fig. 30). Spores pedicellate, hymenium subepidermal, and both peridia and peripheral paraphyses absent (Fig. 30). This type has indeterminate hymenia and the simplest structure among the pedicellate types of aecia.
KEY TO MORPHOLOGICAL TYPES OF AECIA
Spores catenulate 2. Intercalary cells present, sporogenous cells distinct 3. Peridium present, peripheral paraphyses absent 4. Peridium single-layered 5. Hymenium flat, intramesophyllic 6. Spore surface structure of the annulate type, spore germ pores obscure . 6. Spore surface structure of the coronate type, spore germ pores distinct
1.
peridermium I roestelia
Figs 19-24. Vertical sections of aecia. Symbols: AS, aeciospore; E, host epidermis; H, hymenium; I, intercalary cell; IPP, inner pseudoparenchyma; IS, immature spore; M, host rnesophyll; OPP, outer pseudoparenchyrna; PP, pseudoparencbyma; PR, peripheral paraphysis; SP, small lining paraphysis. Stainings: 19, aniline blue; 20, 23, 24, Flemming's triple stain; 21, 22, safranin-fast green. Scales: 19,22, 2 )tm; 20, 24, 1 )tm; 21, 23, 10 )tm.
Fig. Fig.
19. 20.
Caeorna III type of an aeciurn of Phragmidium rubi-idaei with incurved peripheral paraphyses (PR). A basal pan of caeoma I type of an aeciurn of Phragmidium montivagum.
Fig. 21. Caeorna IV type ofanaeciurn of Mikronegeria alba showing well-developed, two-layered pseudoparencbymata (OPP, IPP) around the aeciwn. Fig. 22. Peripheral inner pseudoparencbyrna (IPP) and outer one (OPP) lined with small paraphyses (SP) of M. alba. Fig.
23.
Caeoma V type of an aecium of Caeoma radiatum.
Fig. 24. A basal pan of an aeciurn of Caeoma makinoi with neither conspicuous sporogenous cells nor intercalary cells.
234
Aecial morphology
29 Figs 25-30. Vertical sections of aecium. Symbols: A, aecium; AS, aeciospore; E, host epidennis; H, hymenium; I, intercalary cell; IS, immature spore; P, peridium; PC, pedicel; PR, peripheral paraphysis; S, spennogonium. Stainings: 25, 27, 28, 30, Flemming's triple stain; 26, Heidenhain's haematoxylin and orange G; 29, no staining. Scales: 25,27,30, 10 pm; 26, 29, 2 pm; 28, 1 pm. Fig. 25. Caeoma VI type of an aecium of Zaghouania phillyreae with a hemispherically concave hymenium. Fig. 26. A basal part of an aecium of Z. phillyreae showing immature spores (IS) with intercalary cells (I). Fig. 27. Uraecium I type of an aecium of Thekopsora sp. bearing pedicellate spores. Fig. 28. Aeciospores (AS) of Thekopsora sp. produced on pedicels (PC). Fig. 29. Uraecium II type of an aecium of Phragmidium itoanum with peripheral paraphyses (PR). Fig. 30. Uraecium III type of an aecium of Uromyces truncicola (A) associated with a spennogonium (S).
T. Saw and S. Sata 6. Spore surface structure of the verrucose or nail-headed type, spore germ pores obscure 5. Hymenium flat, subepidermal 4. Peridium multi-layered, hymenium flat, intraconical . 3. Peridium absent, peripheral paraphyses present, hymenium flat, subepidermal . 3. Peridium and peripheral paraphyses absent 7. Hymenium concave hetnispherically, intramesophyllic 7. Hymenium flat, subepidermal 8. Rudimentary peridial cells present 8. Rudimentary peridial cells absent 2. Intercalary cells absent 9. Sporogenous cells distinct 9. Sporogenous cells obscure 1. Spores pedicellate 10. Peridium present, peripheral paraphyses absent . 10. Peridium absent, peripheral paraphyses present . 10. Both peridium and peripheral paraphyses present
235 aecidium . peridermium II peridermium III .caeoma III .caeoma VI · caeoma I · caeoma II .caeoma IV · caeoma V .uraecium I uraecium II uraecium III
DISCUSSION
The morphological types of aecia described herein correspond well with rust genera. Of fourteen genera in which more than two species were examined, all of the species iIi 'each of Uredinopsis, Pucciniastrum, Chrysomyxa, Coleosporium, Cronartium, Gymnosporangium, Puccinia, Phakopsora and Pucciniostele had the same type of aecia (Table 2), while two aecial types were recognized in each of Thekopsora, Uromyces, Phragmidium, Melampsora and Caeoma (Table 2). Related genera often possess the same aecial type. Aecia of Uredinopsis, Milesina, Hyalopsora, Melmpsorella, Thekopsora, Pucciniastrum and CalYPtospora belonging to Pucciniastraceae (Savile, 1976; Cummins & Hiratsuka, 1983) all correspond to peridermium I type. Two phragmidiaceous genera, Phragmidium and Xenodochus, parasitic on rosaceous plants, possess caeoma III aecia, and two coleosporiaceous genera (Cummins & Hiratsuka, 1983), Coleosporium and Chrysomyxa with caeomoid uredinia, form peridermium II aecia. Moreover, Puccinia, Uromyces and Miyagia, which Savile (1976) put together in a subgroup in the Pucciniaceae, have the aecidium type of aecia, and two phakopsoraceous genera, Cerotelium and Phakopsora (Cummins & Hiratsuka, 1983), also produce the aecidium-type aecia. Aecia of the uraecium types are morphologically similar to uredinia of the same species. The species with uraecium types except for uraecium I are all autoecious. It is possible that they have ceased to produce aecia with catenulate spores, and thus sori with pedicellate spores identical to uredinia have replaced the aecial state in the course of simplification of the life cycle, as suggested by Jackson (193 1). If such a simplification actually took place, it is likely that uraecium II or uraecium III aecia coexist with another type of aecium within single
genera, e.g. Phragmidium and Uromyces (Table 2). The heteroecious species of Thekopsora examined in the present study (T. (Pucciniastrum) vaccinii and T. hakkodensis) with uraecium I aecia seem to have little phylogenetic affinity with other species of the genus because of fundamental differences between their aecial morphology. The aecial types are interrelated with aeciospore surface-structure types (Sato & Sato, 1982; Table 2). Aeciospores of peridermium I, II and III all correspond to the annulate type. Roestelia, caeoma V and caeoma VI are characterized by coronate, aciculate and reticulate types of aeciospores, respectively. Verrucose types of aeciospore are distributed among aecidium, caeoma I, II, IV and V, while echinulate types are observed in caeoma III, uraecium I, II and III. Only one species of the aecidium type and a genus of caeoma II type have nail-headed and tubulate types of spores, respectively. In the present study, the spermogonial types (Hiratsuka & Cummins, 1963; Hiratsuka & Hiratsuka, 1980) of the representative species were also examined and are listed in Tables 1 and 2. The majority of the aecial types correspond to single spermogonial groups, but in the aecidium, caeoma II and uraecium III types, two to three groups of spermogonial types are found (Table 2). This suggests that aecia have not always co-evolved with spermogonia, though they usually associate closely with each other in rust life cycles (Fig. 30). Considering the differences in their function, it is not surprising that their morphological types do not always correlate. According to Cummins & Hiratsuka (1983), about 70 genera are known to have aecial states. Aecia of only 33 genera of these have been
Aecial morphology
236
.-<'
I
L~'"
~~
1\\
Peridermium-Il
\.
I rJ.
Peridermium-l ~
7(;~~
...
~ 1 f
11]
II[
.llI\
r'A
I I
I
Roestelia
Peridermium-III
~
•,
'0 f
Caeoma-I
Aecidium
Fig. 31. For caption see opposite.
examined in the present study. In those genera not examined, there may be aecial types not corresponding to any. of the 14 types recognized here, for example Hiratsukamyces and Elateraecium. Recently, Cummins & Hiratsuka (1983) adopted Elateraecium as representative of a new type of aecium_ Obviously, further studies on aecial morphology of genera and species not examined in the present study are necessary, not only for the phylogenetic discussion of aecial types but also for taxonomic revision of form genera of aecial states. It is concluded that morphological types of aecia correlate with rust genera, reflect relationships between genera, and appear to be very important for studies of natural classification and phylogeny of the Uredinales.
The authors wish to express their thanks to Dr Y. Hiratsuka, Northern Forest Research Centre, Canadian Forestry Service, and to Dr K. Katsuya, Dr K. Tubaki and Dr M. Kakishima, University of Tsukuba, for valuable advice and criticism rendered during the course of this work and the preparation of the manuscript. Thanks are also due to Dr N. Hiratsuka and Dr S. Kaneko, Tonori Mycological Institute, Dr T. Kobayashi, Dr H. Sabo and Dr T. Hama, Forestry and Forest Products Research Institute, Dr Y. Harada, Hirosaki University and Dr Y.Ono, Ibaraki University for material and literature used in this work. Contribution no. 44, Laboratories of Plant Pathology and Mycology, Institute of Agriculture and Forestry, University of Tsukuba. An outline of
T. Sata and S. Sata
2 37
"1r---11'--"'I_,"'~""'T"'-I"""'Ir-"I"" f~fY t
Caeoma-III
Caeoma-I1
Caeoma-IV
Caeoma-V
Caeoma-VI
Uraecium-I
'TI--'-I--'-l-~ IYI y I rf~
Uraecium-I1
Uraecium·II1
Fig. 31. Schematic illustrations of the morphological types of aeeia.
this paper entitled 'Morphology of aecia in the Uredinales' appeared in Rep. Tottori Mycol. Inst. n, 133-140 (1984) as part of the proceedings of the Third International Mycological Congress.
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CUMMINS, G. B. & HIRATSUKA, Y. (1983). Illustrated Genera of Rust Fungi, revised edition. St Paul, Minn.: the American Phytopathological Society. DUMEB, P. & MARIE, R. (1902). Remarques sur Ie Zaghouania phillyreae Pat. Bulletin de La Societe Mycologique de France 18, 17-24. FROMME, F. D. (1912). Sexual fusions and spore development of the flax rust. Bulletin of the Torrey Botanical Club 39, 113-131. FROMME, F. D. (1914). The morphology and cytology of the aecidium cup. Botanical Gazette 58, 1-35. HJ!NNllN, J. F. & BURITICA, P. (1980). A brief summary of modem rust taXonomy and evolutionary theory. Report of the Tottori Mycological Institute (Japan) 18, 2 43-2 56 . HIRATSUICA, N. (1955). Uredinological Studies. Tokyo: Kasai. HIRATSUKA, Y. (1965). The identification of Uraecium holwayi on hemlock as the aecial state of Pucciniastrum vaccinii in western North America. Canadian Journal of Botany 43, 475-478. HIRATSUICA, Y. (1973). The nuclear cycle and the tertninology of spore states in Uredinales. Mycologia 6 5,432-443·
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(Received for publication
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October 1984)