SCIENCE CHINA Life Sciences

• COVER ARTICLE • August 2010 Vol.53 No.8: 909–915 doi: 10.1007/s11427-010-4031-3

Four new species and a new Chinese record of the nectrioid fungi

LUO Jing & ZHUANG WenYing*

Key Laboratory of Systematic and Lichenology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

Received April 20, 2010; accepted May 8, 2010

Four new species belonging to Bionectria, Calonectria, Haematonectria and Neonectria on plant substrates collected from na- ture reserves in southern and central China are described. Bionectria truncata has smooth perithecia of a flattened to shallow discoid apex, clavate asci with an apical ring, and ellipsoid, smooth to spinulose ascospores. Calonectria dicephalospora is characterized by pyriform perithecia with a warted surface, clavate asci with a simple apex and long, narrow stalk, and fusoid ascospores with a cap-like appendage at each end. Haematonectria lushanensis possesses warted perithecia which are laterally collapsing when dry, cylindrical asci with a simple apex, and ellipsoid, spinulose ascospores. Neonectria dinghushanica is dis- tinguishable by subglobose perithecia with a warted surface, clavate asci, and striate ascospores. Morphological features of these new species are described comprehensively and compared with their related fungi. Neonectria castaneicola is recorded as new to China.

Bionectriaceae, , morphology,

Citation: Luo J, Zhuang W Y. Four new species and a new Chinese record of the nectrioid fungi. Sci China Life Sci, 2010, 53: 909–915, doi: 10.1007/s11427- 010-4031-3

The nectrioid fungi (, , Asco- Nectriaceae and Bionectriaceae [1–4]. mycota) refer to species of Nectria (Fr.) Fr. and the related Studies on the nectrioid fungi from China were begun genera which are economically important as plant patho- with Teng’s reports of 25 species belonging to 9 genera up gens, biocontrol agents, producers of bioactive compounds to the 1960s [5–8]. A few decades later, 6 genera including or mycotoxins, and diverse in morphology. They are char- 14 species were reported from Taiwan Province [9], and 9 acterized by bright-colored, soft-textured, solitary to aggre- genera containing 15 species were found from Hong Kong gated ascomata, a Nectria-type centrum, unitunicate asci [10,11]. Upon publication of the monographic treatments of with a simple apex or an apical ring, non-disarticulating three families in Hypocreales by Rossman et al. [1], it be- ascospores, and anamorphs mostly with phialidic conidio- came possible to carry out the extensive investigations of genous cells. They are saprobes or parasites on all kinds of the nectrioid fungi in 25 provinces and regions of China. substrates, ranging from plants, dung, soil, other fungi, to Till now, 94 species are known from the country, including animals or human-beings. They occur more commonly in 35 species of 11 genera in Bionectriaceae and 59 taxa be- tropical and subtropical regions, while temperate climates longing to 10 genera in Nectriaceae [9–23]. are also favorable for some members of the group. On the In this study, specimens collected from Fujian, Hainan, basis of ascomatal color and reactions to KOH aqueous so- Henan, Guangdong, Guangxi, Jiangxi and Yunnan prov- lution and lactic acid, they were assigned to two families, inces were examined. Four new species, Bionectria truncata, Calonectria dicephalospora, Haematonectria lushanensis and Neonectria dinghushanica, are described and illustrated. *Corresponding author (email: [email protected]) Distinctions between the new species and their morpho-

© Science China Press and Springer-Verlag Berlin Heidelberg 2010 life.scichina.com www.springerlink.com 910 Luo Jing, et al. Sci China Life Sci August (2010) Vol.53 No.8 logically similar relatives are discussed. Neonectria casta- Ascomata on thin and basal stroma, perithecial, solitary neicola is a new record for China. or gregarious up to 7 in a group, superficial, subglobose to globose, 120–170 μm high, 110–160 μm diam., not col- lapsing when dry, pale yellow when young and brown at 1 Materials and methods maturity, not changing color in 3% KOH or lactic acid, sur- face smooth, with a flattened to shallow discoid apex due to Following the methods by Rossman et al. [1] and Schroers wall thickening at the subapical region; discoid apex [24], characteristics of teleomorphs and anamorphs were 100–130 μm wide. Ascomatal wall 13–20 μm thick, con- recorded in detail. Colony characteristics and measurements sisting of one or two layers; outer layer 7–15 μm thick, cells of conidiophores and conidia were described from cultures angular, 3–8×3–7 μm, cell walls 0.5–2 μm thick; inner layer on potato dextrose agar (PDA) [25] and corn meal dextrose 2–6 μm thick, cells flattened, 4–11.5×1–3 μm, cell walls agar (CMD) [25] after 14 d. Color name of colonies fol- 0.5–1 μm thick. Asci clavate, 8-spored, with an apical ring, lowed Ridgway’s nomenclature [26]. Water was used as 25–42×3.5–6 μm (n=50). Ascospores ellipsoid, uniseptate, mounting fluid for microscopic examinations and measure- not constricted at septum, hyaline, smooth to spinulose, ments, and photographs were taken from water or cotton 1–2-seriate, 8–10×1.5–3.5 μm (n=50). Anamorph un- blue lactophenol solution mounts [27]. Except for specifi- known. cally noted, continuous measurements of each structure are Holotype: CHINA. Guangxi, Damingshan, on decaying based on 30 units. The specimens examined are deposited in leaves of Podocarpus sp., 18-XII-1997, W.P. Wu W1406b, the Mycological Herbarium, Institute of Microbiology, HMAS 183525. Chinese Academy of Sciences (HMAS). Etymology: The specific epithet refers to the truncate perithecial apex. 2 Results and discussion Notes: Characteristics of our fit the concept of Bionectria Speg., including perithecial anatomy, negative reactions to KOH and lactic acid, clavate asci with an apical Taxonomy ring, ellipsoid and 1-septate ascospores, and foliicolous New species habit. Bionectria truncata J. Luo & W.Y. Zhuang, sp. nov. Among the known species of Bionectria, B. truncata is Figures 1A, 2A–D, and 3A most similar to B. gibberosa Schroers in thin and basal MycoBank: MB 518369 stroma, subglobose to globose and smooth perithecia, flat- Peritheciis subglobosis vel globosis, 110–160 μ m diam.; tened to shallow discoid perithecial apex, clavate asci with ascis clavatis, 8-sporis, 25– 42×3.5–6 μ m; ascosporis el- an apical ring, ellipsoidal and 1-septate ascospores, and fo- lipsoideis, uniseptatis, 8–10×1.5–3.5 μ m. liicolous habit. The latter species, however, differs from B. truncata in its pale yellow to pale orange and larger perithe- cia (280 μm diam.), which is pinched laterally or in the subapical region when dry, thicker perithecial walls (30 μm), larger asci ((43–)52.5–59(–65.5)×(6.5–)7.5–8.5(–10.5) μm), larger and smooth-walled ascospores ((9–)11–13(–15)× (2–)3–4(–5.5) μm), and on decaying leaves of Magnolia sp. [24]. Calonectria dicephalospora J. Luo & W.Y. Zhuang, sp. nov. Figures 1B, 4A− F and 3B MycoBank: MB 518370 Peritheciis pyriformibus, papillatis, 165–245 μ m diam.; ascis late clavatis, 8-sporis, 68–95.5×11–22 μ m; asco- sporis fusoideis, utroque processis gelatinosis praeditis, uniseptatis, 27–35.5×5.5–8 μ m. Ascomata on basal stroma, perithecial, solitary, superfi- cial, pyriform, papillate, 200–280 μm high, 165–245 μm diam., not collapsing or laterally collapsing when dry, or- ange red when fresh and orange when dry, turning dark red Figure 1 Ascomata on natural substrates. A, Bionectria truncata (HMAS in 3% KOH and orange-yellow in lactic acid, surface warted; 183525); B, Calonectria dicephalospora (HMAS 183522); C, Haematonectria lushanensis (HMAS HMAS 183547); D, Neonectria warts orange red, 8–24.5 μm high, cells angular, dinghushanica (HMAS 183179). Scale bars=200 μm. 10–24×8–20 μm, cell walls 0.5–1.5 μm thick. Ascomatal

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Figure 2 Morphology of Bionectria truncata (HMAS 183525). A, Median section of an ascoma; B, Asci with an apical ring; C and D, Ascospore.

distinctive by its fusoid ascospores with a gel cap at both ends. Calonectria kyotensis Terashita and C. pauciramosa C.L. Schoch & Crous are similar to C. dicephalospora in warted perithecia, shape, size and apical apparatus of ascus, and 1-septate ascospores. Calonectria kyotensis differs from C. dicephalospora in its larger perithecia (280–550× 210–425 μm), and narrower ascospores ((4–)5(–7) μm), which are typically fusoid and lacking of any appendage at ends [28,29]. Calonectria pauciramosa differs from C. dicephalospora in its larger perithecia (250–400 μm high), Figure 3 Ascus and ascospores. A, Bionectria truncata (HMAS 183525); B, Calonectria dicephalospora (HMAS 183522); C, Haematonectria larger cells (40–55×15–35 μm) in perithecial warts, longer lushanensis (HMAS 183547); D, Neonectria dinghushanica (HMAS ascospores ((30–)33–38(–40) μm), fusoid ascospores and 183179). Scale bars=10 μm. lacking the cap-like appendage at ends [30]. Haematonectria lushanensis J. Luo & W.Y. Zhuang, sp. walls 19–30 μm thick, consisting of two layers; outer layer nov. Figures 1C, 5A–I, and 3C 13.5–24.5 μm thick, cells angular, 6–21×5–17 μm, cell MycoBank: MB 518371 walls 0.5–1.5 μm thick; inner layer 5–9.5 μm thick, cells Peritheciis subglobosis vel pyriformibus, papillatis, flattened, 7–19.5×1–5 μm, cell walls 0.5–1.5 μm thick. Asci 205–330 μ m diam.; ascis cylindricis, (4–)8-sporis, 87–115× broadly clavate to fusoid with a narrow stalk, 8-spored, with 6–12 μ m; ascosporis ellipsoideis, uniseptatis, 13–19×5.5–9 a simple apex, 68–95.5×11–22 μm (n=50). Ascospores fu- μ m. soid with blunt ends, uniseptate, not constricted at septum, Ascomata on well-developed stroma, perithecial, gre- hyaline, smooth, irregularly 3–4-seriate, (24.5–)27–35.5 garious up to 8 in a group, superficial, subglobose to pyri- (–38)×(4–)5.5–8 μm (n=50), with a translucent gel cap at form, papillate, 305–365 μm high, 205–330 μm diam., lat- each end, of 0.5–2 μm thick (n=50). Anamorph unknown. erally collapsing when dry, orange red when fresh and red Holotype: CHINA. Yunnan, Xishuangbanna, on when dry, turning dark red in 3% KOH and orange yellow decaying leaves of a dicotyledonous plant, 16-X-1999, W.P. to yellow in lactic acid, surface warted; warts 12–43.5 μm Wu & Y. Huang W2739, HMAS 183522. high, cells angular, of the same type as cells of the outer Etymology: The specific epithet refers to the presence of ascomatal wall, 8–17×6–12.5 μm, cell wall 1–2.5 μm thick. gel cap at each end of ascospores. Ascomatal wall 33–57.5 μm thick, consisting of two layers; Notes: The combination of the presence of basal stroma, outer layer 19–46.5 μm thick, cells angular, 9.5–17×6.5–13 pyriform perithecia with warts on the surface, positive reac- μm, cell wall 1–2.5 μm thick; inner layer 9.5–23 μm thick, tions to KOH and lactic acid, clavate asci with a simple cells flattened, 8–30×4–9 μm, cell wall 0.5–1.8 μm thick. apex and a long stalk, long-fusoid ascospores, and folii- Asci cylindrical, (4–)8-spored, apex simple, 87–115×6–12 colous habit indicates its position in Calonectria De Not. µm (n=50). Ascospores ellipsoid, uniseptate, not constricted Among the known species of the genus, it is unique and at septum, hyaline to yellowish, with 2–4 guttules, spinulose,

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Figure 4 Morphology of Calonectria dicephalospora (HMAS 183522). A, Median section of an ascoma; B and C, Ascus with a simple apex; D–F, Asco- spore.

Figure 5 Morphology of Haematonectria lushanensis. A, Median section of an ascoma; B and C, Asci with simple apices; D–F, Ascospores; G and H, Conidiophores bearing conidia from sporodochia; I, Conidia. A–F from HMAS 183547, G–I from HMAS 173262.

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1-seriate, 13–19×5.5–9 μm (n=50). asci (60−90×10−17 µm), and striate ascospores [1,31]. H. Colonies on PDA 1.8 cm diam. after 7 d in darkness at monilifera (Berk. & Broome) Samuels & Rossman and H. 24°C; Pale Salmon Color; surface floccus to cotteny; aerial termitum (Höhn) Samuels & Rossman are also similar with mycelium white to pinkish; colony reverse pigmented, H. lushanensis in the spinulose ascospores, but differ in the Warm Buff. Colonies on CMD 1.8 cm diam. after 7 d in absence of stroma, clavate asci, and disarticulating asco- darkness at 24°C; Light Buff; aerial mycelium sparse, white; spores [1]. colony reverse Light Ochraceous-Buff. Conidiophores from Neonectria dinghushanica J. Luo & W.Y. Zhuang, sp. sporodochia branched, straight, conidiogenous cells 14–27 nov. Figures 1D, 6A–F, and 3D μm long, 1.5–3.5 μm wide at base, 0.5–2 μm wide near MycoBank: MB 518372 aperture. Conidia falcate, with a narrowed apical cell and Peritheciis subglobosis, papillatis, 160–250 μm diam.; pedicellate foot cell, slightly curved, hyaline, smooth, ascis clavatis, 8-sporis, 42–60×5.5–11 μm; ascosporis (5–)6–9(–10)-septate; 5-septate: 50–68×4–5.5 μm (n=6); ellipsoideis, uniseptatis, striatis, 10–17×3.5–6 μm. 6-septate: 52–83×4–5.5 μm (n=50); 7-septate: 60–85× Ascomata perithecial, gregarious up to 13 in a group, 4.5–5.5 μm (n=50); 8-septate: 68–92×4.5–6 μm (n=50); with a basal stroma, superficial, subglobose, 170–290 μm 9-septate: 75–100×4.5–6 μm (n=20); 10-septate: 85–90× high, 160–250 μm diam., with a small, acute and red papilla, 5–5.5 μm (n=3). Microconidia, chlamydospores and not collapsing when dry, orange-red when fresh and red perithecia not observed in culture. when dry, turning dark red in 3% KOH and orange to yel- Holotype: CHINA. Jiangxi, Lushan, 800 m alt., on twigs, low in lactic acid, slightly warted, warts concolorous, 5–18 10-X-2006, J. Luo 7183, HMAS 183547, ex type culture μm high, cells in warts globose to angular, 6–17.5×5–13 μm, HMAS 173262. cell walls 1–3.5 μm thick. Ascomatal wall 16.5–30 μm Etymology: The specific epithet refers to the locality of thick, of two regions; outer region 11–24.5 μm thick, cells the fungus. Notes: The combination of perithecia lateral collapsing globose to angular, 5–13×4–8 μm, cell walls 1–3.5 μm thick; when dry, the presence of coarse warts on perithecial sur- inner region 2–6 μm thick, cells elongate, 7–18.5×2–4 μm, face, spinulose ascospores, a Fusarium anamorph, and oc- cell walls 0.5–2 μm thick. Asci clavate, 8-spored, with a curring on woody substrate indicates its position in the ge- simple apex, 42–60×5.5–11 μm (n=50). Ascospores ellip- nus Haematonectria Samuels & Nirenberg. soid to broad-fusoid, slightly constricted at the septum, hya- Among the existing species of the genus, our collection line to yellowish, finely striate, biseriate, 10–17×3.5–6 μm is most similar to H. haematococca (Berk. & Broome) (n=50). Anamorph unknown. Samuels & Nirenberg in well-developed stroma, perithecial Holotype: CHINA. Guangdong, Dinghushan, on rotten size and surface morphology, asci with an apical ring, shape twigs of Pinus sp., 9-X-1998, W.P. Wu W2054, HMAS and size of ascospores, and lignicolous habit. H. haemato- 183179. cocca differs from H. lushanensis in its shorter and wider Etymology: The specific epithet refers to the locality of

Figure 6 Morphology of Neonectria dinghushanica (HMAS 183179). A, Median section of an ascoma; B and C, Asci with a simple apex; D–F Ascospore.

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Figure 7 Morphology of Neonectria castaneicola (HMAS 183542). A Median section of an ascoma; B and C, Asci with a simple apex; D–F, Ascospore. the fungus. W.Y. Zhuang, X.M. Zhang & Z.H. Yu H30, HMAS 83369; Notes: Among the known species of Neonectria Wol- Hainan, Lingshui, Diaoluoshan, 1100 m alt., on rotten twigs lenw., N. castaneicola (W. Yamam. & Oyasu) Tak. Kobay. of an unidentified plant, 13-XII-2000, W.Y. Zhuang, X.M. & Hirooka, N. coronata (Penz. & Sacc.) Mantiri & Samuels Zhang & Z.H. Yu H70, HMAS 76866; Henan, Jigongshan, and N. rugulosa (Pat. & Gaillard) Mantiri & Samuels have 400 m alt., on rotten wood, 14-IX-2003, W.Y. Zhuang & Y. been reported with warted perithecia and striate ascospores Nong 5099, HMAS 91773; Fujian, Wuyishan, on rotten which also show in N. dinghushanica. N. castaneicola twigs of an unidentified plant, 21-IX2006, W.Y. Zhuang, J. differs from N. dinghushanica in its larger perithecia Luo & W.Y. Li 6846, HMAS 183542. (250–470×350–430 μm), thicker perithecial walls (40–87 Notes: Neonectria castaneicola is characterized by its μm), larger asci (50–89×9–13 μm) and containing 4 spores, globose perithecia, warted perithecial surfaces, 4-spored and larger ascospores (18–28×7.5–11 μm) [32]. N. coronata asci and striate ascospores. It is most similar to N. rugulosa, differs from N. dinghushanica in its larger perithecia but they are different in the number of ascospore in an ascus ((200–)260–370(–450)×(110–)250–300(–400) μm), with a [32]. Our collections fit well to the original descriptions of distinctive large-celled fringe around apical portion, larger the fungus [33]. asci ((54–)68–88(–105)×(5.4–)11–18(–25) μm), and much larger ascospores ((10–)16–24(–37)×(3.5–)5.5–8.5(–11) μm) The authors would like to express their deep thanks to Dr. Wu WenPing for [31]. N. rugulosa differs from N. dinghushanica in its larger providing some specimens for this study, Dr. Zhuang JianYun for correc- tions of the Latin diagnoses, and Ms. Song Xia for technique help. This perithecia ((225–)270–370(–500) μm diam), much thicker work was supported by the Ministry of Science and Technology of China perithecial walls (80–100 μm), and larger asci ((53–)64– (Grant No. 2006FY120100). 83(–95)×(7.5–)11.3–15.5(–17) μm) [31]. So, this species is obviously new to the genus. 1 Rossman A Y, Samuels G J, Rogerson C T, et al. Genera of Bionec- A new record for China triaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol, 1999, 42: 1–260 Neonectria castaneicola (W. Yamam. & Oyasu) Tak. 2 Rossman A Y. Towards monophyletic genera in the holomorphic Kobay. & Hirooka J. Gen. Plant Pathol. 71: 124, 2005. Hypocreales. Stud Mycol, 2000, 45: 27–34 (Figure 7A–F). 3 Schoch C L, Crous P W, Wingfield M J, et al. Phylogeny of Ca- lonectria and selected hypocrealean genera with cylindrical macro- Specimens examined: CHINA. Hainan, Changjiang, conidia. Stud Mycol, 2000, 45: 45–62 Bawanling, 1100 m alt., on rotten twigs of Quercus patelli- 4 Samuels G J, Lu B S, Chaverri P, et al. Cyanonectria, a new genus formis Chun, 7-XII-2000, W.Y. Zhuang & X.M. Zhang H22, for Nectria cyanostoma and its Fusarium anamorph. Mycol Prog, HMAS 76854; ibid., on rotten twigs of an unidentified plant, 2009, 8: 49–58 5 Teng S C. Notes on Hypocreales from China. Sinensia, 1934, 4: 7-XII-2000, W.Y. Zhuang & X.M. Zhang H28, HMAS 269–298 76865; ibid., on barks of an unidentified plant, 7-XII-2000, 6 Teng S C. Supplementary notes on Ascomycetes from China. Sinen-

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