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Nematococcomyces rhododendri, a new species in a new genus of the Rhytismatales from China

     Botanisches Institut, J.W. Goethe-Universität Frankfurt am Main, 60054 Frankfurt/M., Germany

Franz Oberwinkler

     Spezielle Botanik, Eberhard Karls Universität, Auf der Morgenstelle 1, 72076 Tübingen, Germany

	ABSTRACT

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A fungus belonging to the Rhytismatales found on twigs of Rhododendron lutescens in Yunnan, southwestern China, is described as a new species in a new genus. It is characterized by Coccomyces-like ascomata but differs in having elliptical ascospores with filiform, hyaline appendages. The ascospores of this new taxon are somewhat similar to those of species of Parvacoccum, but the latter has symmetrical, fusiform ascospores with funnel-shaped appendages. The new genus also is distinct from Hypoderma, Hypodermella, Myriophacidium, Ploioderma, Neococcomyces and Therrya.

Key words: Discomycetes, plant pathogen, Rhododendron, Rhytismataceae

	INTRODUCTION

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Fungi belonging to the Rhytismatales are distributed worldwide and many of them are plant pathogens, some of which cause economically important diseases of trees (Cannon and Minter 1986). Hawksworth et al (1995) included three families in the Rhytismatales, Ascodichaenaceae, Cryptomycetaceae and Rhytismataceae (syn. Hypodermataceae), but Kirk et al (2001) considered the Crytomycetaceae to be a synonym of the Rhytismataceae. Members of the Rhytismataceae usually have ascomata that are more or less embedded in host tissue and open by longitudinal or radial splits, thin-walled, J– asci and ascospores usually with gelatinous sheaths (Sherwood 1980, Di-Cosmo et al 1984, Cannon and Minter 1986, Johnston 1986, Livsey and Minter 1994). The Ascodichaenaceae have erumpent ascomata and ascospores without gelatinous sheaths. Members of the Phacidiaceae, which have J+ asci, ascospores without a gelatinous sheath, and conidia with mucous appendages on both ends, are separated from the Rhytismatales and placed in the Helotiales (syn. Leotiales) (Di-Cosmo et al 1984).

The morphology of ascomata and ascospores is important in the classification of the Rhytismataceae at the generic level (Darker 1967). Many new genera were erected based on ascospore shape, characteristics of ascomata and the depth to which ascomata are embedded in host tissue. Although most mycologists argue that some aspects of Darker’s system are artificial and unsatisfactory, no suitable alternative has been proposed yet. Cannon and Minter (1986) largely adopted Darker’s system in their monograph for the Rhytismataceae on the Indian subcontinent, as have a number of other authors (Powell 1974, Sherwood 1980, Minter et al 1987). Johnston (1988, 1989) attempted to use aspects of ascomatal development to define genera of the Rhytismatales, and some new genera were erected ( Johnston 1990, 1991). Other mycologists, however, still use Darker’s system (Hunt and Funk 1988, Merrill et al 1996, Minter et al 1998, Lin et al 1999). Therefore we accept the generic classification and the system elaborated by Darker (1967) and Cannon and Minter (1986) in the current paper.

The Rhytismatales have been well documented in Europe, North America, Australia, the Indian subcontinent and parts of southeastern Asia (Darker 1932; Minter 1981; Cannon and Minter 1986; Johnston 1986, 1989; Spooner 1990, 1991), and 72 genera including 411 species currently are recognized (Hawksworth et al 1995). Only a few species have been reported from China until recently. Since 1990, however, many new members of this order were described, especially from tropical and subtropical regions of China (He et al 1986, Lin and Tang 1988, Hou and Liu 1993, Lin et al 1995, Hou et al 1996, Lin 1998). A total of 11 genera with 80 species were known from China by the end of 2000. Among them 42 species had been described as new to science. As a continuation of this effort the authors made an expedition to Yunnan Province in southwestern China and to Anhui Province in southeastern China in Jul and Aug 2001.

Rhododendron species is one of the most important hosts for the members of Rhytismatales. In China only a small number of species, such as Rhytisma rhododendri Fr. R. rhododendrioldhamii Saw. Lophodermiun rhododendri Ces., were reported (Dai 1979). The current paper treats a particularly interesting species with a unique combination of morphological characteristics, which therefore is described as a new species in a new genus.

	MATERIALS AND METHODS

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Ascomata were sectioned by hand and sections were placed either in water, Melzer’s reagent, 5% KOH, 0.1% (w/v) cotton blue in water, KOH plus cresyl blue (CRB) saturated solution, or KOH plus congo red saturated solution. Measurements were made with material mounted in 5% KOH. Ascus and ascospore sizes are based on 20 measurements of each.

	RESULTS

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Nematococcomyces C.-L. Hou, M. Piepenbr. & Oberw., gen. nov.

Etymology. – Nemato- referring to the filiform appendages, -coccomyces, referring to some characteristics of this genus similar to Coccomyces.

Type species: Nematococcomyces rhododendri C.-L. Hou, M. Piepenbr. & Oberw., described below.

Ascomata multiangulata vel elliptica vel irregularia, apertura radiali vel irregularia. Paraphyses filiformes. Asci clavati, J– , 4-spori. Ascosporae ellipsoideae, ambabus apicibus filiformibus appendicibus, in tunica gelatinosa non inclusae.

Ascomata in peripheral tissue of living stems or twigs, multiangular, dark brown, opening by teeth or slightly irregular splits. Paraphyses filiform, simple or branched. Asci ripening sequentially, broadly clavate, thin-walled, J– , without circumapical thickening, containing 4 ascospores at maturity. Ascospores elliptical, hyaline, aseptate, with filiform, hyaline appendages at apex and base, without a gelatinous sheath.

Nematococcomyces rhododendri C.-L. Hou, M. Piepenbr. & Oberw. sp. nov. FIGS. 1–11

View larger version (95K): [in this window] [in a new window]   FIGS. 1–3. Nematococcomyces rhododendri on Rhododendron lutescens. 1. Part of the bush from which N. rhododendri was collected. Note enrolled leaves. 2. Ascomata (arrow) on a twig. 3. Detail of ascomata on the twig. Scale bar = 1 mm.

View larger version (38K): [in this window] [in a new window]   FIGS. 9–11. Paraphyses, asci, and ascospores with appendages of Nematococcomyces rhododendri. 9. Young asci with ascospore initials. Scale bar = 10 µm. 10. Mature asci with four ascospores and paraphyses. One ascus additionally includes four rudimentary ascospores, and one discharged ascus. Scale bar = 10 µm. 11. Liberated ascospores with hyaline appendages. Scale bar = 5 µm

Ascomata primo immersa, dein erumpentia, trigona, tetragona vel irregulariter elliptica, apertura radiali 3–4 lobata vel irregulari. Periphysoidea nulla. Excipulum nullum. Paraphyses filiformes, simplices vel ramosae, in epithecio gelatinoso non inclusae. Asci 75–110(–130) x 15–20 µm, late clavatae, J–, 4-spori. Ascosporae 18–25 x5–8 µm, ellipticae, hyalinae, aseptatae, ambabus apicibus filiformibus appendicibus, in tunica gelatinosa non inclusae.

Ascomata on living twigs, the surface of the twigs surrounding ascomata bleached (FIGS. 2–5). Ascomata in surface view 300–900 x240–600 µm, quadrate, triangular, elliptical, or slightly irregular, with conspicuous preformed dehiscence lines, opening by 3–4 lobes or slightly irregularly, strongly raising above the surface of the substrate, lip cells absent. Surface of ascomata dark brown, without a perimeter line. In median vertical section (FIGS. 6–7) ascomata intra-epidermal, covering stroma up to 60 µm thick near the center of the ascomata, slightly thinner toward the edges, consisting of the outer paradermal wall (with cuticula) of the host epidermis and an inner layer of dark brown, somewhat disorganized textura angularis. Cells forming the dehiscence lines (FIG. 7) thin-walled, pale, but slightly carbonized or disappearing at maturity. Periphysoids absent. Basal stroma well developed, flat, composed of dark brown textura angularis, 20–35 µm thick, with cells 4–8 µm diam. Subhymenium (FIGS. 6, 8) consisting of textura intricata, 10–15 µm thick. Excipulum absent. Paraphyses (FIG. 10) 80–120(–135) x1–2(–3) µm, filiform, sometimes branched, not swollen or slightly swollen at the tips, septate or aseptate, usually with a thin gelatinous sheath. Asci (FIGS. 9, 10) ripening sequentially, 75–110(–130) x15–20 µm, broadly clavate, immature asci cylindrical-clavate (FIG. 9), apex obtuse to rounded, thin-walled, J–, without circumapical thickening, discharging spores through a small apical hole, pore visible only in surface view of the apex of the ascus, with eight ascospore initials but four failing to develop, resulting in four spores in a mature ascus. Ascospores (FIGS. 10, 11) mostly uniseriate, 18–25 x5–8 µm, long elliptical, both ends slightly acute, hyaline, aseptate, with many guttulae, different measurement in size, irregular in shape, without a gelatinous sheath, both ends of ascospores with filiform, hyaline, aseptate appendages (FIG. 11), 2(–3) on one end and 1(–2) on the other end. The end with 2(–3) appendages is apparently at the apex, which often has a short, coniform, pale protrusion. Appendages less than 1 µm diam, up to 45 µm long, tapering apically, sometimes broken, observed in water, or CRB on liberated ascospores, not see in asci, hardly visible in 5% KOH, Melzer’s reagent, congo red, or 0.1% (w/v) cotton blue. Conidiomata not observed. Zone lines dark brown, frequent, sometimes rather inconspicuous.

View larger version (77K): [in this window] [in a new window]   FIGS. 4–8. Nematococcomyces rhododendri on Rhododendron lutescens. 4. Twig bearing ascomata at the internodes. Scale bar = 2 cm. 5. Ascomata and a zone line seen with a dissecting microscope. Scale bar = 400 µm. 6. Ascoma in vertical section. Scale bar = 100 µm. 7. Detail of an unopened covering stroma at the preformed opening line in vertical section. Scale bar = 50 µm. 8. Detail of one side of an ascoma. Scale bar = 50 µm

Specimens examined. – CHINA. YUNNAN: Jianchuang, Laojunshan, elevation ca 3400 m, 25 Jul 2001, C.-L. Hou, M. Piepenbring, Z.-L. Yang & R. Kirschner 112 (HOLOTY PE HMAS).

The ascomata of this material are old, so the fruiting period probably corresponds to Jun–Aug.

	DISCUSSION

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The fungus described in our study is considered a member of the Rhytismatales, Rhytismataceae because the embedded ascomata, thin-walled, J– asci without circumapical thickening and opening by teeth are consistent with the concept of that family (Cannon and Minter 1986, Darker 1967, Kirk et al 2001). In addition, molecular data of 28S rDNA show that it belongs to Rhytismataceae (Hou et al unpubl data).

N. rhododendri differs from all known species of the Rhytismataceae by its ascospores without gelatinous sheaths and with filiform, hyaline appendages. A few other members of the Rhytismataceae produce ascospores without gelatinous sheaths, such as Discocainia treleasei (Sacc.) J. Reid & A. Funk, Myriophacidium quercinum (S. Ahmad) P.F. Cannon & Minter, and some species of Therrya Sacc. However, none of those species has ascospores with filiform appendages.

Parvacoccum pini R.S. Hunt & A. Funk has ascospores with appendages, but these appendages are funnel-shaped (Hunt and Funk 1988) and somewhat resemble the conidial appendages of Apostrasseria Nag Raj (Nag Raj 1983) and of other anamorph genera of the Phacidiaceae (Di-Cosmo et al 1984). The ascomata of P. pini are orbicular and open by an irregular longitudinal split, while ascomata of N. rhododendri are quadrate, triangular or elliptical, open by 3–4 teeth and have preformed opening lines. Furthermore, the asci of P. pini have long stalks and the ascospores are fusiform with obscure gelatinous sheaths and are quite different from those of N. rhododendri.

Four-spored asci are typical for species in Hypodermella (Höhnel 1917), Myriophacidium (Sherwood 1974) and Therrya (Reid and Cain 1966). Species of Hypodermella are characterized by elliptical ascomata opening with a longitudinal split and clavate ascospores. Species of Myriophacidium, which have multi-angular ascomata opening with several teeth and elliptical ascospores, are more similar to the new species. The type species, M. aphyophyllicum Sherw., however, differs by asci with 4–8 ascospores that are embedded in gelatinous sheaths and by paraphyses cemented in gel and forming an obvious epithecium. N. rhododendri has only four ascospores in a mature ascus, ascospores with unique filiform appendages and without gelatinous sheaths and no epithecium. Only one species in the genus Therrya, T. fuckelii (Rehm) Kujala, has four ascospores in a mature ascus. T. fuckelii, however, has filifusiform, multiseptate ascospores with acerose acute ends, ascospores embedded in gelatinous sheaths and a very strongly developed dark epithecium (Reid and Cain 1966, Di-Cosmo et al 1984).

The elliptical ascospores of the new taxon are similar to some species of Hypoderma De Not. and Ploioderma Darker. Species of these genera, however, have elliptical ascomata opening with a longitudinal split, asci with eight ascospores and ascospores with conspicuous gelatinous sheaths.

The morphology of the ascomata of N. rhododendri is similar to that of species of Coccomyces De Not. and Neococcomyces Y.-R. Lin, C.-T. Xiang & Z.-Z. Li. Species of Coccomyces, however, have filiform to filifusiform ascospores while species of Neococcomyces have bifusiform ascospores (Lin et al 1999). Ascospores of both genera have conspicuous gelatinous sheaths.

Only one specimen was collected on a bush of Rhododendron lutescens growing on a lawn at the roadside, apparently transplanted from the forest, although we have collected many other different members of Rhytismatales on twigs of Rhododendron spp. in the forest, so N. rhododendri might be rare in this area. The ascomata were found on 1–2 y old twigs, occasionally also on older ones. All the leaves of the bush hung down and the general growth of this bush appeared to be reduced (FIG. 1). We do not know whether this phenomenon is caused by N. rhododendri or by other biotic or abiotic factors, or both. Perhaps the plant suffered from being transplanted as well. More information on pathogenicity and ecology would be useful.

Only one fungus, Naohidemyces vaccinii (Alb. & Schwein) S. Sato, Katsuya & Hirats (syn. Pucciniastrum vaccinii [G. Winter] Jørst), has been reported on Rhododendron lutescens worldwide (Farr et al 1996). Nematococcomyces rhododendri is the first of an ascomycete on R. lutescens worldwide.

	ACKNOWLEDGMENTS

 
We are grateful to Z.-L. Yang (Kunming Institute of Botany, Academia Sinica, P.R. China) who organized the expedition and to R. Kirschner (Botanisches Institute J.W. Goethe-Universität, Frankfurt, Germany) as well as Mary Palm-Hernández (USDA/APHIS, Systematic Botany and Mycology Laboratory, USA) for reviewing the manuscript. The study was supported by the BMBF (biolog).

	FOOTNOTES

 
Accepted for publication April 8, 2004.

Corresponding author. E-mail: chenglin{at}em.uni-frankfurt.de

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