Mycoscience
Online ISSN : 1618-2545
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Short Communication
Discovery of teliospores of a Cape jasmine rust fungus, Hemileia gardeniae-floridae (Pucciniales), and its occurrence in Thailand
Yoshitaka OnoIzumi OkaneJintana UnartngamChanjira Ayawong
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2021 年 62 巻 5 号 p. 336-340

詳細
Abstract

Hemileia gardeniae-floridae is an accepted name for a Cape jasmine (Gardenia jasminoides) rust fungus distributed in East Asia. The fungus name was based on uredinial anamorph collected in Taiwan in 1931. The fungus was rarely collected in Taiwan and southern Japan, and its telial stage remained unknown. Microscopic examination of the type materials of H. gardeniae-floridae and Uredo gardeniae-floridae, which was once proposed to replace H. gardeniae-floridae, resulted in discovery of teliospores on the type of U. gardeniae-floridae. The teliospores are mostly napiform and produced on a sporogenous cell emerging through host stoma. A hemileioid rust fungus, producing both urediniospores and teliospores on Golden gardenia (G. sootepensis), was found in Thailand and morphologically identified to H. gardeniae-floridae. Another Hemileia species on Forest jasmine (G. thunbergia), H. gardeniae-thunbergiae, first found in Angola, Africa, is distinct from H. gardeniae-floridae in producing smaller urediniospores than those of H. gardeniae-floridae.

The genus Hemileia (Berkeley & Broome, 1869) (Zaghouaniaceae, Pucciniales) has captured the attention of people all over the world because the type species of the genus, H. vastatrix Berk. & Broome, commonly known as coffee leaf rust fungus or orange coffee rust fungus, is one of the most devastating invasive fungal pathogens of economically important commodity crops (Avelino et al., 2015; Anonymous, 2016; McCook, 2019). Hemileia is comprised of some forty named species (Ritschel, 2005; Judith & Rossman, 2014). The genus is characterized by suprastomatal sori and hemispherical or kidney-shaped urediniospores with dorsal echinulate and ventral smooth surfaces. Because of these unique uredinial characteristics, about one-third of species named under the genus name Hemileia are based only on the uredinial morph. Current International Code of Nomenclature for algae, fungi, and plants (the Shenzhen Code; Turland et al., 2018) accepts the priority of names of Hemileia species even if they are based on the uredinial anamorph.

Species of Hemileia occur on forty genera in nine vascular plant families and mostly in subtropical and tropical regions worldwide (Ritschel, 2005). Among those plant families, each of two plant families, Apocynaceae and Rubiaceae, harbors about one-third of Hemileia species. In addition to the fact that one-third of species are anamorphic, because of often faced difficulty in identification of host species, particularly in old sterile specimens, and because of poor morphological features available as taxonomic characters, species delimitation and their classification in Hemileia have remained indecisive.

This study aimed at confirming generic assignment a poorly understood hemileioid anamorphic fungus on Cape jasmine (Gardenia jasminoides J. Ellis) first collected in Taiwan and named as H. gardeniae-floridae by Sawada (1931) and identifying a hemileioid fungus on Golden gardenia, G. sootepensis Hutch., found in Thailand.

Specimens and morphological examination

Sawada (1931) did not designate the type for H. gardeniae-floridae in the original description. The type specimen was discovered at the Mycological Herbarium, the University of Tsukuba (TSH), on which specimen label, “Type” was clearly hand-written by K. Sawada (Fig. 1A). The specimen designated as the type of Uredo gardeniae-floridae (Sawada) Hirats. f. (Hiratsuka, 1960) and additional two specimens on G. jasminoides deposited at TSH were also examined. Three specimens on G. sootepensis from Thailand deposited at the Herbarium of Systematic Mycology, Ibaraki University (IBAR) were compared to those on G. jasminoides for taxonomic identification. Individual specimen data are listed in the Taxonomy section. Morphological examinations, both by light microcopy and scanning electron microscopy, were undertaken by the methods described by Ono et al. (2020a, b).

Fig. 1 –Morphology of sorus and spores from the holotype specimen of Hemileia gardeniae-floridae on Gardenia jasminoides collected in Taiwan (TSH-R30286). A: Label of the specimen, exhibiting the type designation by K. Sawada. B: Symptom on a G. jasminoides leaf. Minute rust sori occur on abaxial surface of angular, light brownish orange lesions delimited by veins. C: Transverse section of a sorus. Sporogenous cells (arrow) develop in a substomatal cavity and emerge through a stoma. D: Surface view of a sorus. Spores are produced on a fascicle of sporogenous cells in acropetal order. Thus, mature echinulate urediniospores are positioned at the periphery of developing immature spores. E: Mature urediniospores. One of the spores at side view exhibits typical smooth ventral (arrow) and echinulate dorsall surface. F: Surface view of a urediniospore. Bars: C, E 20 µm; D 10 µm; F 5 µm.

Taxonomy

Hemileia gardeniae-floridae Sawada, Trans. Nat. Hist. Soc. Formosa 21: 234, 1931; emend. Y. Ono Figs. 13.

MycoBank no.: MB 265817.

MycoBank Typification no.: MBT 10001355.

Synonym: Uredo gardeniae-floridae (Sawada) Hirats. f. [as floribundae], Sci. Bull. Agric. Div. Univ. Ryukyus 7: 279, 1960.

Type: TAIWAN, Kaohsiung Prov., Hengchun Co. (now Pingtung Co.), Mudan, Kusku Sinja (Koushifutsu), on G. jasminoides, 26 Apr 1931. K. Sawada (holotype designated here, TSH-R30286). JAPAN, Tosa Prov. (now Kochi Pref.), Tochi-mura (now Nankoku-shi, Tochi), Kompira-yama, on G. jasminoides, 12 Dec 1929, T. Yoshinaga (epitype designated here, TSH-R1173; isotype of U. gardeniae-floridae).

Diagnosis: Differs from H. gardeniae-thunbergiae in producing larger, thick-walled urediniospores and larger teliospores.

Spermogonia and aecia are unknown. Sori are minute, densely or loosely aggregate, or scattered on the abaxial leaf surface. Light brownish yellow lesions demarcated by leaf veins are apparent on G. jasminoides leaves (Fig. 1B), while diffused yellowing is commonly observed on G. sootepensis leaves. Sporogenous cells differentiate in substomatal cavity and emerge through a stoma (Figs. 1C, 3A). Spores are produced on swollen tips of a fascicle of emergent sporogenous cells in acropetal order (Figs. 1D, 2A, 3C). Urediniospores are obovoid, hemispherical or reniform, often weakly angular, 24–(29.8)–37 µm long, and 18–(21.8)–29 µm high at side view (Figs. 1E, 2A, 3B; Supplementary Table S1). The spore wall is colorless, evenly 1.5–3.5 µm thick, ventrally smooth, and dorsally echinulate. No germ pore is observable. Teliospores are napiform, obovoid or subglobose, 19–(24.9)–30 µm long, and 18–(22.9)–28 µm high at side view (Figs. 2C, 3D; Supplementary Table S1). The wall is thin, colorless, and smooth (Figs. 2C, 3D).

Fig. 2 – Spore morphology of Hemileia gardeniae-floridae on Gardenia jasminoides collected in Japan (epitype, TSH-R1173). A: Urediniospores produced on a fascicle of sporogenous cells in acropetal order. B: Surface view of urediniospore, showing ventral smooth and echinulate dorsal surface. C: Urediniospores and teliospores (arrows) produced on a fascicle of sporogenous cells. D: Surface view of a sorus, exhibiting urediniospores and teliospores (arrows). Bars: A, C, D 20 µm; B 10 µm.
Fig. 3 –Spore morphology of Hemileia gardeniae-floridae on Gardenia sootepensis collected in Thailand (IBAR4077). A: Transverse section of sorus. Spores are produced on a fascicle of sporogenous cells (arrow) emerging through a stoma. B: Urediniospores, exhibiting smooth ventral and echinulate dorsal surface. C: Surface view of a uredinium. Urediniospores are produced on emergent sporogenous cells in acropetal order. Thus, mature spores are surrounding successively produced immature spores at the center of the apically developing sorus. D. Teliospores produced on a fascicle of emergent sporogenous cells. Bars: A–D 20 µm.

Other specimens examined

JAPAN, Tosa Prov. (now Kochi Pref.), Oko-mura (now Nankoku-city), Takimoto, on G. jasminoides, 10 Dec 1911, T. Yoshinaga (TSH-R1172); TAIWAN, Kaohsiung Prov., Hengchun Co. (now Pingtung Co.), Gangkou, on G. jasminoides, 25 Apr 1931, K. Sawada (TSH-R1174). THAILAND, Phetchabun Prov., Nam Nao Distr., Nam Nao National Park, on G. sootepensis, 22 Dec 1985, M. Kakishima, Y. Ono and P. Lohsomboon (IBA4077); Chiang Mai Prov., Chiang Mai, Doi Suthep, Medicinal Plant Garden, on G. sootepensis, 21 Nov 2004, Y. Ono and W.S. Chung (IBAR9256); Chiang Mai Prov., Mae Rim, Queen Sirikit Botanic Garden, on G. sootepensis, 17 Feb 2015, Y. Ono, C. Ayawong and P. Janruang (IBAR10699).

Commentary

This fungus was first found on G. jasminoides in Nankoku-city, Kochi Pref. (formerly Oko-mura, Prov. Tosa) in 1911 by Yoshinaga (1913). It was uredinial anamorph, but identified as H. vastatrix (Yoshinaga, 1913; Yoshinaga & Hiratsuka, 1931). Subsequently, Sawada (1931) collected the same fungus on the same host species in Taiwan. He concluded that this fungus is distinct from H. vastatrix in spore size, i.e., smaller in the former vs. larger in the latter species, symptoms, and haustorial morphology. He named the fungus as H. gardeniae-floridae as new. His taxonomic decision was based only on the uredinial morphology, i.e., suprastomatal sori and reniform urediniospores with ventral sooth and dorsal echinulate surfaces, which are prominent taxonomic characters defining the genus. Our discovery of the teliospores in the type of U. gardeniae-florida confirmed its assignment in the genus Hemileia.

Hemileia gardeniae-floridae has been rarely collected only on G. jasminoides in southern Taiwan and southern Japan (Hiratsuka & Shimabukuro, 1954; Shimabukuro, 1961), and its real host range and geographic distribution remained unclear. Our study on Thai rust collections revealed a hemileioid rust fungus on G. sootepensis. Shape and size of urediniospores and teliospores observed in three specimens on G. sootepensis agree with those observed in the holotype on G. jasminoides from Taiwan, an additional Sawada’s collection from Taiwan, and two Yoshinaga’s collections from Japan. Thus, we concluded the taxonomic identity of the Thai fungus to H. gardeniae-floridae.

Sawada (1931) distinguished H. gardeniae-floridae from another hemileioid species on G. thunbergia from Africa, Uredo (Hemileia) gardeniae-thunbergiae (Hennings, 1903), in spore size, i.e., larger in the former vs. smaller in the latter species. Uredo gardeniae-thunbergiae was first found in Angola, southwestern Africa (Hennings, 1903). Later, Maublanc & Roger (1934) found teliospores of the fungus on the same host species collected in Gabon, on the Atlantic coast of central Africa, and, thus, proposed a new name, H. gardeniae-thunbergiae, for this species. Ritschel (2005) re-examined the holotype of H. gardeniae-thunbergiae but was unable to find measurable teliospores. Thus, the teliospore measurement in Ritschel’s (2005) monograph of the genus Hemileia was adapted from the description of Maublanc & Roger (1934). Most records of this fungus are from Africa and only three records from Asia, i.e., those on G. latifolia from India and Indonesia and on G. radicans from Indonesia (Farr, D.F. & Rossman, A.Y. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Retrieved May 8, 2021, from https://nt.ars-grin.gov/fungaldatabases/). Ritschel (2005) determined the taxonomic identity of the two Asian collections from India and Indonesia to H. gardeniae-thunbergiae.

Urediniospores of H. gardeniae-thunbergiae do not differ from those of H. gardeniae-floridae in gross morphology but are 18–33(–35) µm long and 16–24 µm high at side view (Hennings, 1903; Thirumalachar & Narasimhan, 1947; Ritschel, 2005; Supplementary Table S1). The wall is described as uniformly 1–1.5 µm thick (Ritschel, 2005). Teliospores are mostly inversely conical (turbinate), rarely ovoid, 18–28 µm long, and 15–25 µm high at side view (Ritschel, 2005). Hemileia gardeniae-floridae differs from H. gardeniae-thunbergiae in producing larger urediniospores and teliospores. In addition, the urediniospore wall is uniformly 1.5–3.5 µm thick (Supplementary Table S1), which is contrary to Sawada’s description (ca. 1 µm thick). Our morphological comparisons confirmed Sawada’s taxonomic decision on Hemileia species on Gardenia.

Sori of H. gardeniae-floridae are suprastomatal at an early developmental stage (Fig. 3A, C). Sporogenous cells differentiate in the substomatal cavity of the host leaf and emerge through the stoma as a fascicle of sporogenous cells. As the fascicle of sporogenous cells enlarges, some sori disrupt gird cells of the stomata, appearing as erumpent. Gopalkrishnan (1951) and Rajendren (1972) studied several selected species of Hemileia for characterization of the sorus structure and developmental process. They proposed different sorus types, i.e., three by Gopalkrishnan (1951) vs. seven by Rajendren (1972). However, it is still premature to differentiate patterns of sorus structure and underlying developmental process as pointed out by Ritschel (2005). It is tempting to elucidate evolution of sorus development and resultant patterns in relation to environmental selections and speciation. Extensive sampling of species and collections in each species for morphological and molecular phylogenetic analyses would elucidate morphological and molecular diversity of the genus Hemileia, which has been considered as an early diverged group (classified in the family Zaghouaniaceae P. Syd. & Syd.) in the rust phylogeny.

Disclosure

The authors declare no conflict of interest. This study complies with current laws of Thailand.

Acknowledgments

We are grateful to the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation, Thailand, for permission to conduct the study on the diversity of rust fungi at national parks. Our gratitude is extended to the Queen Sirikit Botanic Garden for allowing us to survey rust fungi. This study was supported, in part, by a Grant-in-Aid for Scientific Research Nos.25450056 (YO) and 20H03006 (IO) from the Japan Society for the Promotion of Sciences, and a Research Grant (G-2018-019) from Institute for Fermentation, Osaka (IFO) (YO).

References
 
© 2021, by The Mycological Society of Japan

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