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A new species of Pucciniastrum on Enkianthus campanulatus from Japan

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A new species of rust fungus, Pucciniastrum hakkodaense on Enkianthus campanulatus, is described from Japan. This species is characterized by aculeate ostiolar celles of peridia and uniformly echinulate urediniospores.
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MYCOTAXON
Volume 92, pp. 371–376 April–June 2005
*Contribution no. 197, Laboratory of Plant Parasitic Mycology, Graduate School of Life and
Environmental Sciences, University of Tsukuba, Japan.
A new species of Pucciniastrum
on Enkianthus campanulatus from Japan*
YING-MEI LIANG1, CHENG-MING TIAN2,
KAZUYUKI HIRATSUKA3 & MAKOTO KAKISHIMA1
kaki@sakura.cc.tsukuba.ac.jp
1 Graduate School of Life and Environmental Sciences, University of Tsukuba
Ibaraki 305-8572, Japan
2 The Key Laboratory for Silviculture and Conservation of Ministry of Education,
Beijing Forestry University, Beijing 100083, China
3 Department of Environment and Natural Sciences, Yokohama National University
Kanagawa 240-8501, Japan
AbstractA new species of rust fungus, Pucciniastrum hakkodaense on Enkianthus
campanulatus, is described from Japan. This species is characterized by aculeate
ostiolar celles of peridia and uniformly echinulate urediniospores.
Key wordsBasidiomycota, Pucciniastraceae, Pucciniastrum pyrolae, Uredinales,
taxonomy
Introduction
Pucciniastrum Otth (1861) is a worldwide genus. Most species are known to
have a heteroecious life cycle, and their uredinial and telial stages mainly occur in
dicotyledonous plants, and their spermogonial and aecial stages on the Pinaceae (Abies,
Picea and Tsuga). Recently, Cummins and Hiratsuka (2003) placed the Pucciniastrum
as separate genus from Thekopsora Magnus (1875) and Calyptospora J. G. Kühn (1869)
based on the position of the telia in the plant tissue. Pucciniastrum produces its telia
underneath the epidermis of host plants, while Thekopsora and Calyptospora produce
them within the epidermal cells (Pady 1933, Sato et al. 1993).
In Japan, the taxonomic studies of Pucciniastrum have been extensively carried out by
Hiratsuka (1927, 1930, 1936, 1958) and 21 species were reported in Japan (Hiratsuka et
al. 1992). The specific distinctions have to a considerable extent been based on the host
plants attacked, and the taxonomic identity of species is sometimes artificial. During the
study on morphology and phylogeny of Pucciniastrum spp. in Japan we examined two
specimens borrowed from the Hiratsuka Herbarium in Tokyo (HH103630, HH103631),
which were collected by Hiratsuka et al. in Aomori prefecture, and identified as
372
Pucciniastrum kusanoi Dietel on Clethra barbinervis Sieb. et Zucc. However, we
found that the host plant of these specimens was misidentified and it was Enkianthus
campanulatus (Miq.) G. Nicholson in the Ericaceae. Observations with light (LM) and
scanning electron microscopy (SEM) showed that these two specimens morphologically
differed from P. kusanoi and other species in the genus (Arthur 1934, Hiratsuka et al.
1992, Kuprevich et al. 1957, Wilson and Henderson 1966, Ziller 1974). Therefore, we
describe it as a new species.
Taxonomic description
Pucciniastrum hakkodaense Y. M. Liang & Kakishima, sp. nov. Fig.1
Spermogoniis et aeciis ignotis; urediniis hypophyllis, subepidermalibus, sparsis vel
rarius aggregatis, saepe in superficie folii totalis dense dispersis, minutis, rotundatis
vel ellipsoideis, 0.08~0.25 mm diam., luteo-brunneis vel pallide brunneis, aliquantum
pulveraceis; peridio hemisphaerico, firmo, apice dehiscente, ex cellulis supernis minutis
irregulariter polygonalibus cellulis lateralibus radiatim elongatis composito, cellulis
ostiolaribus ellipsoideis vel rotundatis superne grosse eaculeatis ad basim crassis
praedito; urediniosporis oblongis vel clavato-oblongis, 23.5~34.4 × 10.2~15.7µm,
episporio echinulato fere hyalino, 0.8~1.5 µm crasso; teliis plerumque hypophyllis,
subepidermalibus, planis, nervis foliae limitatis, minutis, flavo-brunneis; teliosporis
solitariis vel irregulariter aggregatis aut lateraliter comfertim conjunctis, subglobosis
vel ellipsoideis, 2~5-cellularibus, 16.5~35.0 µm altis, episporio subhyalino vel pallide
brunneolo, cinnamomeo-brunneo tenui levi.
Holotypus hic designatus: HH103630 in foliis Enkianthi campanulati (Miq.) G.
Nicholson (Ericaceae), Suirennume–Sukayu, Hakkoda Mts., Aomori Pref. in Japonia,
Aug. 28, 1953, a N. Hiratsuka, Shoji Sato & T.Yamagata leg. in Herbario Hiratukanorum,
Tokyo conservatus.
Spermogonia and aecia unknown. Uredinia hypophyllous, subepidermal, scattered or
rarely grouped, often thickly scattered over the whole leaf surface, round or ellipsoid,
minute, up to 0.08~0.25 mm in longest axis, yellowish brown or pale yellow, at last
somewhat pulverulent; peridia hemispherical, firm, dehiscent from an apical pore,
upper peridial cells small, isodiametrical or irregular, lateral ones radially elongate,
walls smooth, nearly colorless; ostiolar cells ellipsoid or roundish, coarsely aculeate
above, greatly thickened below; urediniospores oblong or clavate-oblong, 23.5~34.4 ×
10.2~15.7µm, spore wall uniformly about 0.8~1.5 µm thick, nearly colorless, minutely
echinulate. Telia hypophyllous, subepidermal, flat, minute, limited by veins, generally
in dense clusters, yellow to yellowish brown; teliospores forming under the epidermis,
mostly loosely aggregated, often compacted laterally under the epidermis, subglobose
or ellipsoid, 16.5~35.0 µm high, walls uniformly thin, smooth, cinnamon-brown.
Holotype: on Enkianthis campanulati (Miq.) G. Nicholson (Ericaceae), Suirennume–
Sukayu, Hakkoda Mts., Aomori Pref. in Japan. (Aug. 28, 1953, N. Hiratsuka, Shoji Sato
& T. Yamagata; HH103630, Hiratsuka Herbarium, Tokyo).
Other specimen examined: on Enkianthus campanulatus (Miq.) G. Nicholson
(Ericaceae), Japan, Hakkoda Mts., Aomori (N. Hiratsuka, Shiji Sato & T. Yamagata;
HH103631).
373
Fig.1. Pucciniastrum hakkodaense. A. Ostiolar cells of peridia observed by SEM (Bar=15µm);
B. Uniformly echinulate urediniospores (Bar=5µm); C. Uredinia (Bar=15µm); D. Ostiolar cells
(Bar=20µm); E. Urediniospores (Bar=12µm); F. Subepidermal telia (Bar=20µm).
374
Discussion
The present species has characteristic peridia with ostiolar cells in uredinia (Fig. 1A,
1C, 1D), subepidermal telia, and teliospores with two to four cells divided by septa
(Fig.1F). From these morphological characteristics this species is recognized as a
Pucciniastrum (Hiratsuka 1958).
Hiratsuka (1958) reported 23 species of Pucciniastrum and these were separated into
four morphological groups based on the structure of ostiolar cells of peridia in the
uredinia. The first group including three species is characterized by coarsely or sparsely
aculeate ostiolar cells. The second group including two species is characterized by the
minutely echinulate ostiolar cells which sometimes became smooth in wet conditions.
The ostiolar cells of the third group is obscure and two species are included in this
group. The fourth group has smooth ostiolar cells and contains 16 species that are
separated based on differences of host plants because of morphological similarities
among these species.
This species belongs to the first group because of coarsely aculeate ostiolar cells of
the peridia (Fig. 1A). Three species P. pyrolae Dietel ex Arthur, P. americanum (Farl.)
Arthur, and P. arcticum Tranzschel have been reported in this group (Arthur 1934,
Hiratsuka 1936, 1958, Hiratsuka et al. 1992, Kuprevich et al. 1957, Ziller 1974).
Pucciniastrum hakkodaense is clearly different from the latter two species in the size
and the shape of urediniospores as well as host relations. The urediniospores size of P.
americanum and P. arcticum is 15~28 × 10~18 µm and 17~27× 12~16 µm, respectively,
which are smaller than those of P. hakkodaense (23.5~34.4 × 10.2~15.7µm). Moreover,
P. americanum and P. arcticum produce uredinia and telia on Rosaceae.
Pucciniastrum hakkodaense is similar to P. pyrolae in peridial structure of uredinia and
the shape of urediniospores. However, the urediniospore surface of P. hakkodaense is
uniformly echinulate without smooth area (Fig. 1B), whereas that of P. pyrolae has
smooth area (Fig. 2H). Many herbarium specimens of P. pyrolae, collected from USA,
Canada, Russia and Japan, and deposited in the Mycological Herbarium, Graduate
School of Life and Environmental Sciences, the University of Tsukuba, Japan (TSH-
R017, 8755, 8773, 12368, 12346, 12721, 13205, 13333, 13339, 18072, 18073, 18159,
18352), were observed with LM and SEM. All these specimens have smooth area in the
surface of urediniospores. Furthermore, the urediniospores size of P. pyrolae is larger
(23.4~42.5 × 10.8~19 µm) than that of P. hakkodaense. In addition, P. hakkodaense
and P. pyrolae parasitize different hosts. P. hakkodaense is parasitic on Enkianthus
campanulatus of Ericaceae, and P. pyrolae on Pyrolaceae.
Acknowledgments
We wish to express our thanks to Hiratsuka Herbarium, Tokyo, Japan for the loan of specimens. We
are also grateful to Prof. Toru Nakamura, University of Tsukuba for the identification of host plants
and Dr. Ken Katumoto for the checking Latin description. We thank Dr. J. Y. Zhuang, Academia
Sinica, China and Dr. Y. Ono, Ibaraki University, Japan for critically reading the manuscript.
375
Fig. 2. Pucciniastrum pyrolae. G.. Ostiolar cells of peridia observed by SEM (Bar=7.5µm);
H.. Urediniospores, note smooth area (Bar=10µm); I.. Urediniospores (Bar=15µm).
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... lar peridial cells in uredinia, subepidermal telia, and 2–4-celled teliospores divided by vertical or oblique septa without pedicels (Hiratsuka 1958; Sato et al. 1993). Hiratsuka (1958) accepted 23 species in Pucciniastrum. In following years, Laundon (1963) described 1 species, P. magnisporum Laundon on Acer davidi Franch. and A. rubescens Hayata. Liang et al. (2005) described a new species , Pucciniastrum hakkodaense Y.M. Liang & Kakishima on Enkianthi campanulati (Miq.) G. Nicholson. To date, of 25 species listed under Pucciniastrum, most species are heteroecious and have macrocyclic life cycles (Cummins and Hiratsuka 2003). Of the 25 species of Pucciniastrum, 22 species have been reported in Japa ...
... To date, of 25 species listed under Pucciniastrum, most species are heteroecious and have macrocyclic life cycles (Cummins and Hiratsuka 2003). Of the 25 species of Pucciniastrum, 22 species have been reported in Japan (Hiratsuka et al. 1992; Liang et al. 2005). These species can be divided into four morphological groups based on the characteristics of ostiolar peridial cells in the uredinia. ...
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We analyzed the phylogenetic relationships of 49 specimens comprising 14 morphologically similar species of Pucciniastrum distributed in Japan based on the sequence data of the large subunit rDNA (D1/D2), 5.8S rDNA, and internal transcribed spacer (ITS) regions. Neighbor-joining and parsimony analyses generated six major groups for both the D1/D2 and ITS regions. Pucciniastrum circaeae and P. epilobii formed a single group. P. hydrangeae-petiolaris, P. coryli, P. fagi, P. hikosanense, P. tiliae, and P. boehmeriae were each a distinct clade, and P. fagi formed a close relationship with P. hikosanense. However, these analyses did not support the monophyly of the following species: P. kusanoi, P. actinidiae, P. corni, P. styracinum, P. yoshinagai, and P. miyabeanum.
... Hitherto, several genera in Pucciniastraceae have been delimitated based on morphological characters in teliospores (Cummins and Hiratsuka 2003), even at generic level, the position of telia and morphology of teliospores have long been used as important taxonomic criteria (Hiratsuka 1958;Cummins and Hiratsuka 2003;Liang et al. 2005;Yang 2015). Although there have been much debates concerning the generic classification based on telial morphologies, recent phylogenetic studies and our study supported the monophyly of all sampled genera in Pucciniastraceae, thus, supported the effectiveness of telial morphologies as taxonomic criteria at generic level. ...
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The genera that constitute the Pucciniastreae display a wide variation in the type of teliospore produced, as well as in the time and place of production. From the standpoint of development, however, there is a general situation that is common. In all genera primordial cells are formed from enlarged hyphal cells of the mycelium. These give rise to teliospore initials which are in the epidermal cells in Calyptospora, Milesia, Hyalopsora and Thecopsora, and are subepidermal in the other genera. These initials divide to form the mature teliospores, which are thick or thin walled, and few to many-celled. In all cases the teliospore is the product of a single primordial cell.The teliospores of Calyptospora goeppertiana are formed from a perennial mycelium, which causes a witches' broom and hypertrophied stems on species of Vaccinium. The mycelium gives rise to primordial cells in the cortex just below the epidermis. Each primordial cell pierces the host wall above and the contents pass in to form the initial, which by growth and division becomes the teliospore. The mature teliospores are one- to four-celled, with a thickened, dark brown wall. Development is not simultaneous, but progressive, and the teliospores are first formed in the basal parts, moving slowly upward until every cell of the hypertrophied portion of the stem is completely filled. In four species of Milesia the method of development is similar. The spores, however, are thin walled, and are formed in the epidermal cells of the overwintered fronds of their fern hosts. Thecopsora vacciniorum is similar to Milesia in many respects. The teliospores are intra-epidermal, thin walled and multicellular. In Pucciniastrum the teliospores are subepidermal, and arise from primordial cells, as in Calyptospora, Milesia and Thecopsora. The teliospore initials are closely packed, and the mature spores may form extended crusts. The simplest type of development is found in Uredinopsis, which is generally considered to be the most primitive of the fern rusts. Primordial cells are formed in the same way as in the other genera. These round up to form the initials, and cross walls are laid down to give the mature spores.From these studies two possible lines of development are suggested, both beginning with Uredinopsis. One line would lead through the intra-epidermal forms, as Milesia, Calyptospora, etc., and the other through the subepidermal genera, as Pucciniastrum and Melampsoridium.
1869. Calyptospora nov
  • J Kühn
Kühn J. 1869. Calyptospora nov. gen. Uredinearum. (Hedwigia, VIII: 81).
Über die Familie der Melampsoreae und ihre Gattungen
  • P Magnus
Magnus P. 1875. Über die Familie der Melampsoreae und ihre Gattungen. Sitzungsber. Ges. Naturf. Freunde Berl. P. 57-60.